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Plant root growth, architecture and function

Article  in  Plant and Soil · August 2009

DOI: 10.1007/s11104-009-9929-9

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Plant Soil (2009) 321:153–187
DOI 10.1007/s11104-009-9929-9

REVIEW ARTICLE

Plant root growth, architecture and function

Angela Hodge & Graziella Berta &
Claude Doussan & Francisco Merchan &
Martin Crespi

Received: 3 December 2008 / Accepted: 6 February 2009 / Published online: 5 March 2009
# Springer Science + Business Media B.V. 2009

Abstract Without roots there would be no rhizo- examine the physiological and genetic determinants
sphere and no rhizodeposition to fuel microbial of root growth and the complex, yet varied and
activity. Although micro-organisms may view roots flexible, root architecture that results. The main
merely as a source of carbon supply this belies the functions of root systems are also explored including
fascinating complexity and diversity of root systems how roots cope with nutrient acquisition from the
that occurs despite their common function. Here, we heterogeneous soil environment and their ability to
form mutualistic associations with key soil micro-
organisms (such as nitrogen fixing bacteria and
Responsible Editor: Yves Dessaux.
mycorrhizal fungi) to aid them in their quest for
A. Hodge (*) nutrients. Finally, some key biotic and abiotic
Department of Biology, constraints on root development and function in the
Area 14, P.O. Box 373, University of York,
York YO10 5YW, UK
soil environment are examined and some of the
e-mail: [email protected] adaptations roots have evolved to counter such
stresses discussed.
G. Berta
Dipartimento di Scienze dell’Ambiente e della Vita,
Università del Piemonte Orientale,
Keywords Root systems . Auxin . Root architecture .
via Bellini 25/G, Soil heterogeneity . Abiotic and biotic stresses .
Alessandria 15100, Italy Soil micro-organisms (including nitrogen-fixing
bacteria and mycorrhizal fungi)
C. Doussan
UMR 1114 EMMAH INRA/UAPV Domaine Saint-Paul,
Site Agroparc,
Avignon Cedex 9 84914, France Physiological and genetic determinants of root
growth and achitecture
F. Merchan
Departamento de Microbiología y Parasitología,
Facultad de Farmacia, Universidad de Sevilla,
A major difference between plant and animal devel-
c/ Profesor García González, opment is that positional information rather than cell
Sevilla 41012, España lineage determines cell fate in plants (Singh and
Bhalla 2006). Post-embryonically, plant development
M. Crespi
Institut des Sciences du Végétal (ISV), CNRS,
is essentially driven by stem cells localized in apical
1 Avenue de la Terrasse, regions of shoots and roots, and referred to as apical
Gif-sur-Yvette 91198, France meristems. This particular characteristic allows plants,
154 Plant Soil (2009) 321:153–187

which are sessile organisms, to adapt their morphol- pericycle cells are the initial event of the formation of
ogy and organ development to the encountered a lateral root. Several consequent divisions result in
environmental conditions. The spatial configuration the formation of a dome-shape primordium that grows
of the root system (number and length of lateral through outer cell layers and a meristem is estab-
organs), so-called root architecture, vary greatly lished. Upon activation of this meristem, the lateral
depending on the plant species, soil composition, root emerges from the parental root and continue to
and particularly on water and mineral nutrients grow in the soil (Malamy 1995 and references
availability (Malamy 2005). Plants can optimize their therein).
root architecture by initiating lateral root primordia
and influencing growth of primary or lateral roots. Phytohormonal regulation of the root system: Auxin
The root system results from the coordinated control as a major player
of both genetic endogenous programs (regulating
growth and organogenesis) and the action of abiotic The different stages of root development are con-
and biotic environmental stimuli (Malamy 2005). The trolled and regulated by various phytohormones with
interactions between these extrinsic and intrinsic auxin playing a major role (reviewed by Leyser
signals however complicate the dissection of specific 2006). In roots, auxin is involved in lateral root
transduction pathways. Such complex traits likely formation, maintenance of apical dominance and
depending on multiple genes may be analyzed adventitious root formation. All these developmental
through quantitative genetics via the identification of events require correct auxin transport and signaling.
quantitative trait loci (QTL) linked to root architecture During embryonic RAM formation many auxin-
(e.g. Mouchel et al. 2004, Fitz Gerald et al. 2006). related mutants, such as those involved in its
Understanding the molecular mechanisms governing biosynthesis yuc1 yuc4 yuc10 yuc11 quadruple mutant
such developmental plasticity is therefore likely to be (Cheng et al. 2007), or mutants affected in transport
crucial for crop improvement in sustainable agricul- or signaling (monopteros, bodenlos, auxin transport
ture. In this section, we focus on hormonal and inhibitor resistant 1 (tir1) and related tir1/afb1–3
genetic determinants of root architecture. quadruple mutant (Dharmasiri et al. 2005, Jenik et al.
The embryonic root apical meristem (RAM) 2007) are unable to form the embryonic RAM. The
specification occurs very early in embryo develop- auxin flux coming from the apical region of the
ment (Benfey and Scheres 2000). The RAM con- embryo into the hypophysis leads to TIR1 (and
stitutes the stem cell niche that eventually produces related redundant AFBs) pathway activation and
all below-ground organs, including lateral roots induction of auxin-response genes such as PIN genes
(Sabatini et al. 2003). The cellular organization of (coding for auxin efflux carriers), whose products will
Arabidopsis RAMs is very regular, with the initials of increase auxin transport and accumulation to further
the various tissue types surrounding a quiescent differentiate the hypothesis (Benkova et al. 2003).
center (QC). An asymmetric division of the hypoph- Auxin also plays a major role in lateral root
ysis generates a large basal daughter and a small initiation and development. Lateral root development
apical daughter, called the lens-shaped cell, which is can be divided in different steps: primordium initia-
the progenitor of the QC. During root initiation, the tion and development, emergence, and meristem
QC appears to act like an organizing center that can activation. Auxin local accumulation in Arabidopsis
direct surrounding cells to produce a set of initials root pericycle cells adjacent to xylem vessels, triggers
(Aida et al. 2004, Jenik et al. 2007). Different lateral root initiation by re-specifying these cells into
mechanisms specify the initials above the QC that lateral root founder cells (Dubrovsky et al. 2008).
give rise to the ground tissue and the stele (proximal Furthermore, it is also involved in the growth and
initials) as well as the initials below the QC that organization of lateral root primordia and emergence
produce the root cap (distal initials). This root cap and from the parent root (Laskowski et al. 2006). Indeed,
the underlying root apical meristem form the root mutants or transgenic lines with elevated auxin
zone called the distal root apex, where cells divide biosynthesis and endogenous levels of IAA display
actively. At certain distance from the RAM, the significant increased root branching (Seo et al. 1998,
anticlinal and asymmetric divisions of a group of King et al. 1995). In addition, overexpression of the
Plant Soil (2009) 321:153–187 155

DFL1/GH3-6 or the IAMT1 genes, which encode responsive elements (AuxREs) in the promoters of
enzymes modulating free IAA levels, results in a auxin-responsive genes, and activate or repress
reduction in lateral root formation (Staswick et al. transcription through interaction with specific Aux/
2005; Qin et al. 2005). Hence, normal auxin biosyn- IAA proteins (Liscum and Reed 2002). These loops
thesis and homeostasis are necessary for lateral root represent extensive feedback as well as feed-forward
initiation in Arabidopsis. However, overall auxin regulation (for further information on Aux/IAA pro-
content is not always positively correlated with lateral teins, their degradation and their interaction with ARF
root number (Ivanchenko et al. 2006). transcription factors see the review by Benjamins and
Auxin transport into the regions where lateral root Scheres 2008). Alterations in these control systems
initiate also seems crucial for the regulation of root affect several auxin-dependent plant pathways includ-
branching (Casimiro et al. 2001). Functional analyses ing root development. For example, normal differen-
of mutants impaired in auxin transport, such as the tiation of a root cap from the distal initials depends on
aux1, axr4, and pin multiple mutants (Benkova et al. a pair of redundantly acting auxin response factors,
2003; Marchant et al. 2002), have demonstrated the ARF10 and ARF16 (Wang et al. 2005). In double
crucial role of auxin transport in lateral root forma- mutants, the root cap initials overproliferate, thereby
tion. In the root, auxin is transported in both an generating a mass of undifferentiated progeny.
acropetal (base-to-apex; Ljung et al. 2005) and Another example are the gain-of-function solitary
basipetal (apex-to-base) direction within inner and root (slr) mutants which carries a stabilizing mutation
outer tissues of the root apex (Swarup and Bennett in the IAA14 negative regulator of auxin signaling
2003). Studies using auxin transport inhibitors have and cannot form lateral root primordia. Detailed
shown that the polarity of auxin movement provides analyses of the slr mutant demonstrated that the slr
an important developmental signal during lateral root mutation blocks early cell divisions during initiation
initiation (Casimiro et al. 2001) and root gravitropism (Fukaki et al. 2002)
(Parry et al. 2001). The strong bias in the direction of
auxin transport within a tissue results from the Other hormones involved in the control of root
asymmetrical cellular localization of an influx system development
involving the AUX1 protein (Swarup and Bennett
2003) and an efflux apparatus with PIN-type efflux Although auxin plays a fundamental role in root
facilitators (reviewed by Paponov et al. 2005). growth and development, several other phytorho-
The auxin efflux system regulated by PIN protein mones modulate auxin action and consequently affect
family members is also crucial for lateral root root development and architecture. In contrast to
development (Benkova et al. 2003). Although not all auxin, exogenous cytokinin application suppresses
pin mutations affect lateral root formation, multiple lateral root formation, and transgenic Arabidopsis
pin mutants have dramatic defects in root patterning, plants with decreased cytokinin levels display in-
including lateral root development (Benkova et al. creased root branching and enhanced primary root
2003; Blilou et al. 2005). Cellular localisation of PIN growth (Werner et al. 2003). The notion that cytokinin
proteins is also important as a gnom mutant allele is negatively regulates root growth has also been
defective in PIN-dependent developmental processes, verified by studies of cytokinin perception and
including lateral root primordium development, pre- signalling. For instance, double mutants for the
sumably due to disorganized PIN1 localization redundant Arabidopsis cytokinin receptors AHK2
(Geldner et al. 2004). and AHK3 display a faster growing primary root
When auxin reaches the target tissue it induces a and greatly increased root branching (Riefler et al.
transcriptional response. Several auxin-responsive 2006). To identify the stage of lateral root develop-
genes and gene families involved in auxin signalling ment sensitive to cytokinin, Laplaze et al. (2007)
have been identified, of which the Aux/IAAs and performed transactivation experiments that revealed
ARFs are the best studied. Auxin induces expression that xylem-pole pericycle cells, but not lateral root
of Aux/IAA proteins, which in many cases reduces primordial, are sensitive to cytokinin. Cytokinins
the sensitivity of cells toward auxin. This induction is perturb the expression of PIN genes in lateral root
mediated by ARF proteins that bind to the auxin- founder cells and prevent the formation of the auxin
156 Plant Soil (2009) 321:153–187

gradient required to pattern the primordia. Recently auxin signaling pathway to regulate root growth
cytokinin have also been shown to induce differenti- (Ruzicka et al. 2007).
ation of cells situated between the root meristem and Abscisic acid (ABA), a universal stress hor-
the elongation zone (Dello Ioio et al. 2007), providing mone, plays a significant role in stimulating
new insights on the molecular mechanisms involved elongation of the main root and emergence of
in root meristem maintenance. lateral roots in response to drought (De Smet et al.
The actively growing primary root of dicotyledon 2006b). As with other hormones, the complexity of
plants may exhibit apical dominance forcing their the plant responses induced by this hormone makes
lateral roots to develop further away from the root tip it difficult to distinguish primary from secondary
(Lloret and Casero 2002). Root apical dominance effects (e.g. stomata closure affects water movement
may be triggered by the root-cap-synthesized cytoki- in the plant). In general, ABA has an antagonistic
nin and the balance between auxin and cytokinin effect on lateral root primordial formation and
regulates root gravitropism, a major determinant of emergence to auxin, which initiates lateral roots
root architecture (Aloni et al. 2006). The control of (Malamy 2005). This role of ABA in the control of
lateral root initiation depends on the primary root the activity of the lateral root meristems has a
vascular system which conveys spatial information as significant impact on the final size and architecture
well as photosynthetic carbon to the newly formed of the root system (De Smet et al. 2006b). Indeed,
primordial (Parizot et al. 2008). Three types of responsiveness to certain abiotic factors is lost in
vascular differentiation can be distinguished: (1) certain ABA signaling mutants (Signora et al. 2001;
primary differentiation, which occurs in cells origi- He et al. 2005; Fujii et al. 2007) such as the systemic
nating from the primary vascular meristem, the inhibition of lateral root formation in high N
procambium; (2) secondary differentiation, where conditions in the ABA-insensitive mutant abi4
the derivates originate from the vascular cambium; (Signora et al. 2001).
and (3) regenerative differentiation, in which the
vascular elements re-differentiate from parenchyma Genetic and genomic approaches to analyze root
cells at lateral root junctions. The vascular tissues are growth and architecture
induced by polar auxin movement along the plant
body, from the hydathodes of young leaves downward Forward and reverse genetic approaches have been
to the root tips. Cytokinin by itself does not induce undertaken to elucidate the genetic control of lateral
vascular tissues, but in the presence of auxin, it root formation. As expected, most of the lateral root
promotes vascular differentiation and regeneration, a mutants (approximately 40%) identified in A. thaliana
critical process for the establishment of a root system are affected in a specific component of the auxin
(Aloni et al. 2006). pathways. Their phenotypes can usually be rescued or
Another hormone involved in lateral root for- mimicked through auxin application. Several mutants
mation is ethylene. Treatments that induce C2H4 having lateral root phenotypes (De Smet et al. 2006a)
production (i.e. flooding) promote adventitious and have been linked to auxin signaling (axr mutants, tir1,
lateral root formation (Mergemann and Sauter 2000). msg2-1, shy2), auxin transport (aux1 and pin
Ethylene stimulates auxin biosynthesis and basipetal mutants), and auxin homeostasis (alf1, ydk1, dfl1).
auxin transport toward the elongation zone, where it Analysis of these mutants has led to the identification
activates a local auxin response leading to inhibition of several genes that regulate lateral root formation
of cell elongation. Stepanova et al. (2005) showed and/or coordinate this process in response to environ-
that ethylene-triggered inhibition of root growth is mental cues (reviewed in Osmont et al. 2007). Few
mediated by the action of the weak ethylene Arabidopsis mutants such as the previously men-
insensitive2/anthranilate synthase α1 (WEI2/ASA1) tioned slr-1/AUXIAA14 (Fukaki et al. 2002) and alf4-
and wei7/anthranilate synthase ß1 (ASB1) genes that 1 (Celenza et al. 1995), are not capable of initiating
encode rate-limiting tryptophan biosynthesis any lateral roots. The encoded ALF4 protein is
enzymes In addition, ethylene modulates the tran- conserved among plants and has no similarities to
scription of several components of the auxin trans- proteins from other kingdoms. The Arabidopsis gene
port machinery and induces a local activation of the is involved in lateral root initiation but not in primary
Plant Soil (2009) 321:153–187 157

root formation as the alf4-1 mutant forms a primary Genomics have provided new tools to explore
root. DiDonato et al. (2004) have shown that ALF4 downstream and upstream genes of broad regulatory
functions are required to maintain the pericycle in a signals such as hormone-responsive factors. Tran-
mitosis-competent state needed for lateral root forma- scriptional changes during root branching in Arabi-
tion. Other mutants are affected in vascular tissues dopsis have been monitored to identify key regulators
and consequently cannot produce lateral roots (e.g. of root architecture (Himanen et al. 2004), including
Ohashi-Ito and Bergmann 2007). several core cell cycle genes. In addition, Vanneste et
In contrast, ectopic expression of PLT genes, al. (2005) compared the early transcriptome of lateral
coding for AP2-type transcription factors, trigger de root formation using synchronised induction of these
novo formation of roots from shoot structures. PLT1 organs in wild type and slr mutants. This revealed
was isolated by reverse genetics technologies based negative and positive feedback mechanisms that
on the identification of a QC– and stem-cell–specific regulate auxin homeostasis and signalling in the
enhancer trap line. Indeed, PLT genes are pivotal pericyle initial cells.
determinants of QC and stem cell identity (Aida et The advent of genomic resources have allowed
al. 2004). Although plt1 mutants only display mild the combination of global profiling with novel
root growth defects, the establishment and mainte- biological approaches such as enhancer trap lines
nance of the QC and stem cells in the root meristem, driving green fluorescent protein (GFP) expression
are severely impaired in the plt1 plt2 double mutant. in specific root cell types (Brady et al. 2007). These
NAC1 is another transcription factor implicated in authors used transgenic lines that expressed GFP in
lateral root development since its overexpression specific root tissues to isolate corresponding fluores-
enhances lateral root initiation (Xie et al. 2002). A cent protoplast populations derived from them and
genetic framework for the control of cell division characterise their expression patterns using micro-
and differentiation in root meristematic cells have arrays. Thus were able to determine which genes were
been recently proposed (Dello Ioio et al. 2008). expressed and at what level in a particular root cell
A second strategy used to identify non-essential type. Recently, these transgenic plants were used to
modulators of root development, is exploiting characterise the transcriptional response to high
natural genetic variation by analysis of quantitative salinity of different cell layers and developmental
trait loci (QTL). QTL mapping has the advantage stages of the Arabidopsis root (Dinneny et al. 2008).
of identifying genomic regions containing genes Transcriptional responses are highly constrained by
with subtle effects masked in a particular genetic developmental parameters further revealing interac-
background. For instance, in A. thaliana and maize tions between developmental fates and environmental
QTLs linked to root architecture have been identified stresses.
(Mouchel et al. 2004; Tuberosa et al. 2002; Loudet et Genomic approaches mainly rely on the expression
al. 2005). Exploring the polymorphisms underlying patterns of protein-coding genes. However, the dis-
natural variation can identify the DNA sequence covery of small RNAs (microRNAs, miRNA; and
changes that lead to a modified root system architec- small interfering RNAs, siRNA) in the last decade
ture in nature. In recent years, several new genomics altered the paradigm that protein coding genes are the
resources and tools (e.g. genome sequences, tens of only significant components of gene regulatory net-
thousands of molecular markers, microarrays, and works (Chapman and Carrington 2007). Small RNAs
knock-out collections) have become available to are involved in a variety of phenomena that are
assist in QTL mapping and cloning, even if these essential for genome stability, establishment or main-
genes have subtle effects on phenotype (see Paran and tenance of organ identity, adaptive responses to biotic
Zamir 2003). For example, quantitative morpholog- and abiotic stresses. In plants, MIRNAs are genes
ical and physiological variation analysis of a cross generally encoded in intergenic regions whose matu-
between isogenized Arabidopsis accessions revealed ration requires a particular type III RNase named
that the BREVIS RADIX (BRX) transcription factor DICER-LIKE 1 (DCL1) (Chapman and Carrington
controls the extent of cell proliferation and elonga- 2007). The small mature miRNA is then incorporated
tion in the growth zone of the root tip (Mouchel et al. in a protein complex, the so-called RISC (RNA-
2004). Induced Silencing Complex) that can recognize
158 Plant Soil (2009) 321:153–187

mRNAs partially complementary to the miRNA Root system achitecture

nucleotide sequence. This recognition event mediated
by the RISC-loaded miRNA leads to cleavage or Root systems and architecture definitions
translational inhibition of the target mRNA. Mutants
affected in miRNA metabolism (biosynthesis, action Soil is a complex medium with high spatial and
and transport as dcl1, ago1, hen1, hyl1, hst1, se) show temporal environmental variability at a wide range of
pleiotropic phenotypes confirming the role of miR- scales, including those relevant to plant roots. The
NAs in diverse developmental processes (Chapman root system, with its extensive but structured devel-
and Carrington 2007). opment, can be considered as an evolutionary
Several MIRNAs have been involved in root response to such spatio-temporal variability in re-
development. For example, Arabidopsis mir164a and source supply and associated constraints upon growth
mir164b mutant plants produced more lateral roots (Harper et al. 1991). As a consequence, the extension
than wild-type plants (Guo et al. 2005). These in space and time of the root system is governed by
phenotypes are similar to those obtained by NAC1 genetically driven developmental rules which are
overexpression, a transcription factor targetted by modulated by environmental conditions. As demon-
miR164 (Xie et al. 2002). Overexpression of strated by QTL mapping which recently revealed that
miRNA-resistant NAC1 mRNA results in slight root morphology is in most cases regulated by a suite
increases in lateral root numbers. In addition, the of small-effect loci that interact with the environment
auxin-related transcription factors ARF10 and ARF16 (de Dorlodot et al. 2007).
are also targets of three related microRNA (miRNA) The architecture of a root system is the result of
genes, miR160a, miR160b and miR160c. These miR- developmental processes and is a dynamic notion.
NAs limit the expression domain of ARF10 and ARF16 Root architecture addresses two important concepts:
to the columella, and have a complementary pattern. the shape of the root system and its structure. The
The over-expression of a miRNA-resistant ARF16 shape defines the location of roots in space and the
mRNA under its own promoter results in pleiotropic way the root system occupies the soil. Its quantifica-
developmental defects. MIR160 overexpressing plants, tion is generally achieved by measuring variables
in which the expression of ARF10 and ARF16 is such as root depth, lateral root expansion and root
repressed, and the arf10-2 arf16-2 double mutants length densities. In contrast, root structure describes
display the same root tip defect, with uncontrolled cell the variety of the components constituting the root
division and blocked cell differentiation in the root system (roots and root segments) and their relation-
distal region showing a tumor-like root apex and loss ship (e.g. topology: connexion between roots; root
of gravity-sensing (Wang et al. 2005). Apart from these gradients). While, root differentiation has important
examples, due to the large diversity of these novel impacts upon structure—function relations (Clarkson
regulatory RNAs, it is likely that many other miRNAs 1996).
or other small RNAs participate in the regulation of The rhizosphere (i.e. the volume of soil around
root development and architecture. living plant roots that is influenced by root activity;
Root meristematic cells integrate signals from the Hinsinger et al. 2005), is often simply thought of as a
environment to regulate specific developmental cylindrical shape around the root. However, this
responses and cope with external constraints. This oversimplification does not account for integration at
post-embryonic growth and development requires the the root system level or for the inherent complexity of
activation of hormone homeostasis and signalling root systems which arise from geometry, temporal
pathways, transcriptional regulation by specific tran- dynamics and the heterogeneous aspects of roots.
scription factors and post-transcriptional regulation of These complexities are incorporated into the concept
developmental regulators by non-coding RNAs. of root architecture. Root geometry is complex
These regulatory mechanisms may be particularly because of the specific motion in space of each root,
relevant to adjust differentiation processes to the the relative locations between roots and the possible
environmental conditions encountered during growth, overlapping of their zones of influence. The temporal
notably on primary and lateral root developmental dynamic comes both from the growth of the different
programs. root axes and from physiological processes associated
Plant Soil (2009) 321:153–187 159

with root segments (i.e. tissue differentiation) result- (Cannon 1949; Harper et al. 1991; Klepper 1992),
ing in temporal and spatial variability of function the formation of which has been shown to be
along the root axes. The diversity among roots within genetically separable (Hochholdinger et al. 2004).
the root system and soil heterogeneity further increase This classification also reflects differences between
this variability. monocot– and dicotyledon species: dicots root system
is derived from primary roots and lateral branching
Root classification and elaboration of the root system (primary root system), with roots that may exhibit
radial growth. Depending on the extension of laterals
It has long been recognized that the in situ morphol- relative to the primary axis, the morphology of the
ogy of a root system can be complex and may vary root system will vary between taprooted and diffuse
greatly, even within a species (Weaver 1926; Cannon or fasciculate (Fig. 1). In monocots, root systems
1949; Kutschera 1960), reflecting the interplay be- derive not only from branching of primary roots but
tween developmental processes and environmental also from emmited nodal roots (adventitious root
constraints (Fig. 1). Consequently, the complexity of system). Monocot roots do not undergo secondary
root systems has led to a number of different radial growth. The primary root differentiates from
classification systems. These classifications can be the seed’s radicle already present in the seed embryo.
based on: branch structure (topology) (Fitter 1987; This generally gives rise to a single-axis root system,
2002), root activity (Wahid 2000) or development or taproot system, with dominant vertical growth
(Cannon 1949). The latter is the more classical (gravitropism). Adventitious (or nodal) roots differ-
approach and is useful in understanding growth as entiate from organs other than roots (e.g. rhizomes,
well as obtaining a more global view of root stems etc) and are initiated at precise locations (near
architecture, for example, in relation to plant habitat. stem nodes for example) with a defined temporal
Thus, developmental classification has been widely pattern, in coordination with the development of the
used in modelling approaches to simulate architecture shoot. They are often abundant and give rise to a
(cf section below). fasciculated root system. Adventitious roots are much
From a developmental stand point roots are less sensitive to gravitropism than primary roots
classified according to their ontogenesis into three (Klepper 1992). Lateral roots originate from the
main categories: primary, nodal and lateral roots branching of a parent axis, often at near right angles,

Fig. 1 Diversity of root

systems. On the top row,
root systems are little
branched, while more
profusely branched on the
bottom row. Dominance of a
single main axis increases
from left to right (from
Kutschera 1960)
160 Plant Soil (2009) 321:153–187

and differentiate from parent roots by initiation of a (ii) Branching, which is the development of lateral
primordium in the pericycle cells located adjacent to roots along a bearing root of lower order. This is
protoxylem poles (although with some exceptions e.g. the main process for multiplying the number of
wheat, see Demchenko and Demchenko 2001) at roots. Root elongation and branching are coor-
some distance from the apex. This process results in a dinated processes (Lecompte and Pagès 2007)
branching front which follows the parent root’s apex and an equilibrium is maintained between root
(acropetal branching). However, lateral roots may also number and length. Formation of lateral root
appear out of this main sequence, differentiating from primordia (in terms of locations and cell divi-
older tissues generally near the main root base. The sion) are now well described (see Physiological
maximum number of branching orders seems to be a and genetic determinants section and Lloret and
genotypic feature. Branching can also develop by Casero 2002). In the acropetal branching se-
reiteration. Here the parent axis duplicates into two quence under homogeneous conditions, lateral
(or three) axes of the same morphological type and emergence occurs after a defined thermal time,
creates forks in the root system which can profoundly allowing the length of the unbranched apical
impact upon tree root system architecture (Vercambre bearing axis to vary with its growth rate (Pellerin
et al. 2003). and Tabourel 1995). However, under heteroge-
In a number of plant species (e.g. cereals), the neous soil conditions root branching is highly
primary root system will dominate the early growth sensitive to environmental stimuli, particularly
stages while the adventitious root system will nutrient availability (Drew and Saker 1975; see
dominate in older plants. In the latter case, the also Root Function section below). It has been
location and dynamic of the nodal root emissions shown that not all lateral root primordia develop
are of prime importance for the general structure of into lateral roots and that hormones influence
the root system as has been demonstrated using primordia development (Malamy 2005). The
cereals (Klepper 1992; Pellerin 1993; Yamazaki and rapid activation of primordia and the consecutive
Nakamoto 1983). growth of lateral roots may be how plants
The respective importance of the primary and respond to nutrient perception. For example, in
adventitious root systems (i.e. the relative growth Arabidopsis four effects of N supply on root
rates of main axes and laterals, and the number of development have been identified (Zhang et al.
branching orders), varies among plant species and can 2007) namely: (1) a localized stimulatory effect
be further modulated by environmental conditions. of external nitrate on lateral root elongation; (2)
Hence, different plant species develop different soil a systemic inhibitory effect of high tissue nitrate
exploration strategies. For example, maize (a mono- concentrations on the activation of lateral root
cotyledon) emits nodal roots throughout its vegetative meristems; (3) a suppression of lateral root
phase allowing shallow soil horizons to be repeatedly initiation by a high C:N ratio, and (4) an
explored. In contrast, narrow leaf lupine (a dicotyle- inhibition of primary root growth and stimula-
don) explores shallow soil horizons by means of a tion of root branching by external L-glutamate
single generation of branch roots and much less new (organic N).
roots are emitted (see Fig. 2). (iii) Axial growth, defines the length and trajectory
of roots and contributes to the dynamic coloni-
zation of new soil zones. From an architectural
Developmental processes contributing to root system
point both the elongation and the direction have
architecture
to be considered as elongation will define the
dynamics of soil colonization, while direction
Common basic developmental processes act simulta-
will define its shape. Moreover, both are highly
neously upon root system dynamics as follows:
variable between roots and are sensitive to
(i) Emission of new main axes (primary or adventi- external conditions. Axial root growth occurs
tious), which is highly coordinated with shoot from the distal end (root tip) as a result of both
system growth (leaf and tiller development) as cell division in the meristem and elongation
discussed above; within the elongation zone. The optimal soil
Plant Soil (2009) 321:153–187 161

Fig. 2 The difference in the

rooting pattern of a a mature
maize plant, with numerous
adventitious roots repeti-
tively exploiting the soil
(from Weaver 1926) and b a
narrow leaf lupine plant
with a typical herring-bone
root system and with less
roots emitted with time for
exploiting the soil surface
(from Doussan et al. 2006)

A B

temperature range for root growth varies roots, the denser the soil in which they were
depending on the species and their origin (17– located, indicating that soil pores of varying
35°C; McMichael and Burke 2002). Trajectory radius were accessed by different root types
of the root is influenced by different tropisms from main axes to laterals of different order.
and the root cap seems to be involved in sensing (iv) Radial growth: some, but not all, roots of
these (e.g. gravitropism, hydrotropism, P tro- dicotyledonous plants show a radial growth that
pism etc; Kaneyasu et al. 2007; Svistoonoff et results from the activity of laterally situated
al. 2007). The influence of tropisms varies secondary meristems (cambium). Aside from
among root branching order or adventitious/ morphological variations, this process is important
seminal roots (Lynch and Brown 2001). During for a range of root functions including increased
elongation, the root tip is pushed forward into axial transport properties (particularly axial hy-
the soil, the root part behind the elongation zone draulic conductivity), increased mechanical
being anchored in soil. However, during move- strength and anchorage, storage capacity and
ment, the root tip has to overcome the mechan- protection against predation, drought or pathogens.
ical resistance of the soil (see section on Root (v) Root senescence and decay: root mortality and
response to abiotic stress below). Presence of turnover are important processes in the devel-
zones of high mechanical impedance is one of opment and function of root systems, particu-
the most common physical limitations to soil larly in perennial plants. From a plant resource
root exploration (Hoad et al. 1992) as it impacts allocation view, if root systems exhibit plastic-
not only on root growth rate and morphology ity in producing new roots in favorable soil
(Dexter 1987; Masle 2002) but also growth zones, they should also be able to shed these
direction with tortuous trajectories (Pagès roots when resource uptake is no longer
2002), soil colonization (Tardieu and Katerji efficient. Replacement of decaying roots by
1991), and the local soil-root environment more efficient new ones (i.e. root turnover) may
(Pierret et al. 2007). Consequently, in natural account for c. 30% of global terrestrial net
soil roots follow the path of least mechanical primary production (Jackson et al. 1997).
resistance such as through cracks and biopores Considerable variations in root longevity are
(Rasse and Smucker 1998). Root colonization found (Fig. 3), which may be due to the
of soil macropores leads to a specific biological methodology used: ≤ 1 year from minirhizotron
and chemical environment from that of the bulk techniques, to > 4 years from data derived from
soil (Pierret et al. 1999), but this environment carbon isotopes techniques (Pritchard and Strand
may also vary with root type. Indeed, Pierret et 2008). In addition, the influence of environmen-
al. (2005) demonstrated that the thinner the tal conditions (e.g. temperature, nutrients) on
162 Plant Soil (2009) 321:153–187

Fig. 3 The relationship

between root longevity (yr)
and root diameter for roots
produced in shallow (0–
15 cm) and deep soil (15–30)
at the Duke FACE forest site
from Fall 1998 through
January 2007. Longevity was
determined based on visual
observations of roots using
minirhizotrons. Root longev-
ity was not influenced by
diameter in shallow soil, but
increased with diameter in
deeper soil. The data high-
light the heterogeneity in
longevity of fine roots
(< 2.0 mm in diameter). From
Pritchard and Strand (2008)

root life span is contradictory (see Eissentat and the heterogeneity of root functioning in-situ. This
Yanai 2002). Roots originating from the seed (i.e. anatomical, physiological, and morphological diversity
radicle, seminal) or primary adventitious roots are has been called “heterorhizy” (Noelle 1910; Waisel and
generally perennial, determining root system Eshel 1992; Hishi 2007). Variations in morphology or
shape. Higher orders lateral roots may live longer function can occur among roots of different origin
when they undergo secondary growth or devel- (ontogenesis) or along the root (differentiation).
opment of a periderm, often signaled by brown- Morphologically, large differences among roots
ing of the root (Hishi and Takeda 2005; Eissentat occur due to root diameter: for example in the
and Yanai 2002). Fine roots lacking secondary monocotyledon, Musa acuminate (Banana tree) var-
growth, wall thickening or with a low C:N ratio iations in root diameter can reach 2 orders of
are shorter lived. Morphological markers, such as magnitude (i.e. from 0.06 to 6 mm; Lecompte et al.
root tip diameter, have been shown to correlate 2001). Such variations are common in many species,
with root longevity (Thaler and Pagès 1999). although generally at lower orders of magnitude (c. 1)
Decaying roots enter a necrosis process starting and are linked to variation in root structure (Fitter
from the distal end and superficial tissues which 2002, Varney and McCully 1991a). In dicotyledons
progressively extends to the whole root. Howev- species such variations are reinforced by secondary
er, a decaying root may still be functional growth. This has large consequences on root transport
(Robinson 2001). properties: roots showing secondary growth may
exhibit a 100–1,000 increase in axial hydraulic
conductivity compared to roots without secondary
Diversity of roots within the root system growth (Vercambre et al. 2002). Morphologically
different, specialized roots may also be present in
The diversity of root function is illustrated by water and different species such as contractile roots, cluster
nitrate uptake. If all roots behave identically, ex-situ roots, dauciform roots and so forth (see Specialized
measured rates of uptake based on root length result in a root morphologies section below).
large over-estimation of uptake rates (Robinson 1991). Differences in functioning between roots of differ-
In contrast, actual measured uptake rates suggest that ent origins have been demonstrated. For example, in
only 10% and 30% of the total root system length is maize, seminal roots, even if relatively few in
involved in nitrate and water uptake respectively. This number, play a dominant role in water supply during
raises the question of which parts of the root system a significant part of the plants life span (Navara
are active and does this value vary with nutrient 1987), but are able to acquire less P than nodal roots
availability? The answer relies on the assessment of (Mistrik and Mistrikova 1995). Variations between the
Plant Soil (2009) 321:153–187 163

taproot and laterals in Cl or K uptake have been Fourcaud et al. 2008; Pierret et al. 2007), thus is only
demonstrated in pea (Waisel and Eshel 1992), while in briefly considered here. Such models are helpful in
maize, nitrate uptake rate was 1.5 times greater in linking knowledge gained at the level of the individ-
branch roots compared to the main axis (Lazof et al. ual root to that of the entire root system. Moreover,
1992). because they include explicit quantitative information
Large changes in physiological properties also about the soil volume occupied as well as the
occur along roots as a result of tissue aging and location, number and, possibly, functionality of roots,
differentiation. Consequently, variation in root func- modeling approaches provide opportunities to under-
tion including nutrient uptake rates are observed at stand root exploration of soil in combination with soil
increasing distance from the root tip (Clarkson 1996). bio-physico-chemical processes (Pagès et al. 2000,
These include gradients in: Wang et al. 2006). Modeling approaches also open
new avenues for genetic improvement of crops by
& respiration : high respiration variation was found in
estimating the importance of different root traits/
the vicinity of the apex and also up to 20 cm from
functions in low-input or low-fertility soils (Lynch
the root tip in Prunus persica (Bidel et al. 2000);
2007; de Dorlodot et al. 2007, Wu et al. 2005) or in
& ion uptake : NO3 and NH4 uptake and P, K, Ca
plant competition (Dunbabin 2007).
uptake and translocation, varies along roots with
Conceptually, root system architecture can be
different zones of active (mainly apical) and passive
modeled in different ways, depending on the goals
uptake (Cruz et al. 1995; Lazof et al. 1992;
and actual knowledge and parameterization of the
Clarkson 1996);
different processes available. Root architecture can be
& proton/hydroxyl excretion: parts of roots may
described by synthetic descriptors such as fractal
excrete H+, while other release OH- depending
dimensions, which represent the space filled by the
on the N source (Jaillard et al. 2000);
roots (Tatsumi et al. 1989), or the relationship
& carbon exudation, which is mainly concentrated in
between the basal root and total root system size
the apical zone (Personeni et al. 2007);
(van Noordwijk and Mulia 2002). Topological mod-
& axial and radial root water transport properties
eling is another synthetic way of describing root
which is linked to tissue maturation (i.e. suberiza-
system architecture. Here, the root system is repre-
tion and opening of xylem vessels). In maize this
sented by a set of links which can connect two
resulted in a tenfold decrease of radial root
branching points (interior link) or an apex to a
hydraulic conductivity while the root axial con-
branching point (external link) allowing derived
ductance increased by c. three orders of magnitude
topological parameters such as the magnitude (num-
(Doussan et al. 1998). Radial growth in perennial
ber of external links), altitude (largest number of links
roots of dicotyledons also results in a drastic
between an external link and the base link) and the
increase of root axial conductance (Vercambre et
ratio of magnitude to expected altitude, to be defined
al. 2002).
(see Fitter 2002). These attributes have been related to
Thus, the global functioning of a root system is the the carbon cost, the transport properties and the
reflection of more or less independent physiological exploitation efficiency of topologically different
processes coordinated at the root system level but architectures (Fitter 2002, Bernston 1994) and has
varying among different roots and even along a single proved fruitful in describing the global implications of
root according to its age. This has a profound contrasted branching patterns (e.g. herringbone vs
influence upon root-soil interactions and the dynamics dichotomous).
of the rhizosphere as shown by water flux along a Another approach to modeling root system archi-
maize and peach tree root system, estimated from a tecture and growth is to represent the developmental
coupled hydraulic-root architecture model (Fig. 4). processes of the root system. This results in a three-
dimensional set of connected axes or segments,
Modeling of the root system architecture and function defining the roots and their apex, each characterized
by properties such as age, root type, diameter, length
Modeling of root architecture and function has been and possibly water or nutrient-uptake ability. Such
the subject of many recent reviews (see Pagès 2002, models have been developed with variable degrees of
164 Plant Soil (2009) 321:153–187

Fig. 4 The heterogeneity of functioning of root systems in the distinct distal-proximal gradient for the peach tree, while uptake
case of water uptake. Graphs show the uptake rates of water is more distributed along the root system and patchy for the
along roots derived from modelling of a a maize root system maize. This intra- and interspecific variations of fluxes linked to
and b a young peach tree root system, both taking up water root system architecture may have significant impacts upon
from a homogeneous medium of freely available water. The rhizospheric processes (redrawn from Doussan et al. 1999)
pattern of uptake is heterogeneous for both plants, but show a

dynamic complexity: for example, Ge et al. (2000) ing power, will likely allow interactions between root
showed the effect of altered gravitropism of the basal and soil biogeochemistry to be invesigated in the near
roots of bean plants in P acquisition efficiency; future. Coupling between mycorrhiza processes and
Somma et al. (1998) and Dunbabin et al. (2002) root systems also has yet to be fully achieved but
incorporated aspects of the effect of nitrate availabil- may, in conjunction with experimental data, provide
ity upon root system development in an attempt to clues to the respective importance of these key soil
simulate root plasticity and efficiency. Doussan et al. micro-organisms upon plant nutrition (Smith 2000).
(1998, 2006) introduced root functional heterogeneity To this end, a first attempt in modeling mycorrhizal
into root architectural models to address the interac- growth, uptake and translocation of P has been done
tion between water uptake by the root system and soil by Schnepf and Roose (2006). Finally, although not
water transfer and hydrodynamic properties. A similar all the interactions and processes of the soil-plant
approach was recently conducted by Javaux et al. system need, or can, be simulated with the same
(2008) also for water (Fig. 5) and is important as it degree of accuracy, progress will be made by focusing
tries to define which parts of the root system are models on some key, specific processes while
effectively active. approximating others.
However, very few, if any, of these models have
thus far coupled interactions among the spatial pattern
of resource availability (e.g. P availability may be Root functions
greater at the surface while water may be available at
depth), heterogeneity of roots in physiological capac- General root functions in the heterogeneous soil
ity and interactions between the root and above environment
ground parts. In relation to rhizosphere interactions
integration of detailed geochemical soil processes as As indicated above, the main functions of a root
relates to, for example, nutrient mobility, have only system are anchorage and uptake of water and
been vaguely incorporated into such models and nutrients. In trees and other woody species, extensive
presently lack rigor. Further, the interactions between belowground structures whose main role is to provide
exudates, nutrient uptake and the root system are still support rather than nutrient acquisition are required
in their infancy (Dunbabin et al. 2006). However, but in smaller plant species anchorage occurs largely
progress in reactive transport codes and root models as a secondary function of root growth and develop-
(Nowack et al. 2006), along with enhanced comput- ment in soil. The overall form or ‘architecture’ of the
Plant Soil (2009) 321:153–187 165
Fig. 5 Functional root
architecture models
interacting with their envi-
ronment using water as an
example. a Cross-sections
of the three-dimensional soil
water potential distribution
after 7 days with constant
water flux at the root collar
for three soil types. High
gradients are found in the
vicinity of roots, depending
on the soil type. Barley root
architecture is shown in
white (from Javaux et al.
2008). b Propagation with
time of a water extraction
front along the root system
during daily transpiration
for a (modified) Lupine root
system in a sandy soil.
Water flux density is in
cm3 cm-2 s-1 (from Doussan
et al. 2006)

root system is also important for anchorage and ropism (growth towards water) in Arabidopsis
water-nutrient uptake. Root system architecture is (Kobayashi et al. 2007). While the genetic controls
very varied among different plant species but within remain largely undiscovered, it is well established that
species architecture is flexible (see above) and can roots exhibit a high degree of physiological and
alter as a result of prevailing soil conditions. This morphological plasticity in order to capture nutrients
flexibility arises due to the modular structure of roots from transient patches in the soil (reviewed by Hodge
which enables root deployment in zones or patches 2004, 2006). Physiological responses, which tend to
rich in moisture or nutrients. The genetic controls on occur first, can be both large and rapid: roots of
this root deployment are still largely unknown perennial species common to the Great Basin region
although the gene ANR1 is involved in the first stages of North America showed as much as an 80%
of the nitrate (NO3-) signalling system when NO3- increase in phosphate (P) uptake rates in patches
levels are locally enhanced (Zhang and Forde 1998) enriched with P compared to those roots present in
and a novel gene, miz1 (from mizu-kusseil meaning control (distilled water) patches after only a few days
‘water’ and ‘tropism’ respectively in Japanese) has (Jackson et al. 1990). Morphological responses where
recently been identified which is essential for hydrot- roots proliferate in response to nutrient patches tend
166 Plant Soil (2009) 321:153–187

to take longer as, strictly speaking, root proliferation flora. Kembel and Cahill (2005) found no relation-
involves the initiation of new laterals (rather than ship between root foraging precision and scale in
simply root elongation). any of the three data sets examined. There was
It is often stated that fast-growing species from however, weak support for a relationship between
fertile habitats are capable of greater morphological relative growth rate (RGR) and precision, but only
plasticity than slow-growing plants from infertile in the Great plains flora subset, which was the only
habitats, as the former have more resources to allocate data set where root surface area (rather than
to new root construction (Chapin 1980; Grime et al. biomass) was used as the parameter for root
1986). However, in a survey of the literature foraging response, and the only case were all
Reynolds and d’Antonio (1996) found that while species came from a single plant community. Root
more biomass was allocated below-ground to roots biomass although commonly reported (and easily
under low nitrogen (N) conditions, this was a general measured) is not necessarily the best measurement
plant response and did not differ among plants from to determine foraging ability as changes in the
habitats of contrasting fertility. While Reynolds and architecture of the root system can occur without a
d’Antonio (1996) considered gross partitioning change in biomass (see Hodge 2004). Biomass
above- and below-ground to high or low N, Campbell measurements also do not take into account root
et al. (1991) investigated biomass allocation within longevity which can increase (Pregitzer et al. 1993),
the root system of competitively dominant and decrease (Hodge et al. 1999c) or remain unchanged
subordinate plant species in a nutrient patchy envi- (Hodge et al. 2000d) in nutrient patches. The nature
ronment. Campbell et al. (1991) created nutrient of the patch itself (i.e. duration, size and concentra-
patches by dripping nutrient solution continuously tion) may influence how long roots persist (see Hodge
onto the surface of sand resulting in two-nutrient rich et al. 1999b, 2000d) but to fully understand root
and two nutrient poor quadrants in the microcosm demography in relation to soil heterogeneity, we need
units without the use of barriers thus allowing free to understand the controls on root production and
root growth within the microcosm. When the incre- death. Although there is information on the former,
ment in root biomass in nutrient-rich sections was we know little about what causes roots to die. Some
examined competitively dominant plants had the are inevitably eaten, but the plant controls on root
greatest amount of roots in the nutrient rich quadrants death remain elusive.
but the subordinate plants allocated more of their new Root length (a measure of root surface area) has
root growth into the nutrient-rich zone: i.e. subordi- been shown to be a good predictor of nutrient capture
nates placed their new roots with more precision. from patches (see Hodge et al. 1999a, 2000c;
Campbell et al. (1991) referred to this as a trade-off Robinson et al. 1999) however the context in which
between the scale and precision of the response. the proliferation response is produced also needs to be
Although this is an intriguing idea it has proved to be considered. For example, although plants grown
controversial, with the results of some studies individually respond to complex N-rich patches by
suggesting that larger root systems actually show root proliferation, an actual benefit of this prolifera-
greater precision than smaller (subordinate) ones (e.g. tion in relation to plant N capture could not be shown
Einsmann et al. 1999; Farley & Fitter 1999). Kembel (van Vuuren et al. 1996; Hodge et al. 1998).
and Cahill (2005) recently re-examined support for However, when plants were grown in interspecific
the scale/precision hypothesis by using published data competition for these N-sources, then the root length
for 121 plant species in total. To allow for differences produced in the patch was directly related to the
between experimental conditions, in particular if root amount of patch N each plant captured (Hodge et al.
biomass or surface area was measured, Kembel and 1999a). Thus, in the absence of interspecific plant
Cahill (2005) divided the data into three subsets: competition the importance of root proliferation for N
British flora, Great plains flora and combined bio- capture was obscure. The activity of soil micro-
mass. In the first two subsets data was derived from a organisms and fauna in releasing nutrients from
single study in each case whereas in the third subset complex patches for plant uptake is also critical
numerous studies were combined. Root surface area (Bradford et al. 2007; Hodge et al. 2000a, d, e), thus
was only used as a parameter for the Great plains studies need to be conducted under more ecologically
Plant Soil (2009) 321:153–187 167

relevant conditions for the root response to be When both AMF and colonised roots are present in
correctly interpreted. organic patches the root responses appear to be more
important than that of the actual fungus, at least in
Root-mycorrhiza enhanced nutrient capture terms of N capture from the patch (Hodge 2001a, b).
However, when only the fungus was permitted access
Most plants have an additional mechanism of to the patch, the amount of patch N in the plant
nutrient acquisition, namely that of mycorrhizal increased and was directly related to the extent which
(literally meaning ‘fungus-root’) symbiosis, and in the AMF proliferated hyphae in the patch zone
the natural environment being mycorrhizal is the (Hodge et al. 2001). Often in controlled pot experi-
norm rather than the exception (for the impact of ments, and from which much of this data is derived,
mycorrhizal colonisation upon actual root structure conditions for root growth are more favourable than
see ‘Root responses to micro-organisms’ section they would be in the field. Thus the benefit of AMF
below). Of the seven types of mycorrhizal associ- under field conditions will likely be greater than the
ations that can form depending on the fungal-plant studies with both roots and AMF experiencing the
combination, the three most important and globally patch suggest. In addition, because of its extensive
widespread are the ericoid (ERM), ecto- (ECM) and external mycelium the AMF hyphae should be able to
arbuscular mycorrhizal (AM) associations. Of these access patches the plant cannot, either because of
three, the AM is the ancestral condition and likely distance from the root or because they are too small or
aided the first land plants to colonise the terrestrial transient to evoke a root response. Moreover, coloni-
environment (Smith and Read 2008). The AM sation by AMF can enhance the host root proliferation
association is also the most widespread type of response specifically in a patch zone (Hodge et al.
mycorrhizal symbiosis forming on two-thirds of all 2000b), although this did not result in a net benefit in
plant species (Smith and Read 2008). terms of N capture, when plants were grown in
ERM and ECM fungi are known to have sapro- monoculture. However, as stated previously, root
phytic capabilities that can enhance nutrient acquisi- proliferation responses only conferred a net benefit
tion (particularly N) for their host plant (Read and in terms of N capture when plants were grown in
Perez-Moreno 2003). Arbuscular mycorrhizal fungi interspecific competition (Hodge et al. 1999a). Thus,
(AMF) were traditionally thought to be important when the effects of AM colonisation on plants grown
only for P acquisition (see Smith and Read 2008). in interspecific competition were specifically tested,
Phosphate ions form insoluble complexes with most colonisation by AMF did enhance N capture for their
of the abundant cations (e.g. Al3+, Fe3+ and Ca2+) in associated host plant (Hodge 2003a) but this affect
soil. Consequently phosphate diffuses very slowly may depend upon the plant species present (see
and depletion zones rapidly develop around roots. Hodge 2003b). Although AMF are well known to
AM fungi extend out from these depletion zones and enhance P capture for their associated host plant few
thus can explore a larger soil volume for P acquisi- studies have actually considered heterogeneous (i.e.
tion. However, there is now evidence that AMF can patchy) supplies of P. Cui and Caldwell (1996a, b)
also capture and transfer N to their associated host studied the impact of AMF colonisation when both
plant (Govindarajulu et al. 2005) including from roots and AMF were present in a P-rich solution patch
complex organic sources in the soil (Hodge et al. and when the fungus only was allowed access to the
2001). The exact mechanism by which AMF can enriched P zone. Colonisation by the AMF enhanced P
capture N from these complex patches still needs to capture under both conditions. However, large differ-
be defined, as these fungi have no known saprophytic ences among different AMF may exist in their ability
capabilities (Smith and Read 2008). Although there to enhance P (Cavagnaro et al. 2005) and N (Leigh et
are vast amounts of literature on the nutritional al. 2009) capture from a patchy environment.
benefits of mycorrhizal associations much less is
known about how mycorrhizal fungi alter the Specialised root morphologies
responses of roots in heterogeneous nutrient environ-
ments, and data from those studies that have Along with mycorrhizal and nitrogen-fixing symbio-
investigated this tend to be on the AM association. sis (see Root response to micro-organisms section
168 Plant Soil (2009) 321:153–187

below), cluster roots represent the third major strategy Both formation of cluster roots and the exudative
of nutrient acquisition to have evolved among land burst are regulated by P concentrations in the shoot
plants (Skene 1998). Unlike the other two however, rather than in the soil (Shane et al. 2003), although the
cluster root formation does not involve a tight root- actual exudative burst is the more tightly regulated of
microbial interaction. Although some cluster rooted the two (Keerthisinghe et al. 1998). This regulation
species, such as lupins, can also form nitrogen-fixing makes economic sense for the plant given that cluster-
symbiosis, they tend to be non- or very weakly roots under P stress can exude 3–23% (depending on
mycorrhizal (but see Boulet and Lambers 2005). Thus, plant age) of their dry weight as citrate (Johnson et al.
cluster roots represent an alternative mechanism to 1996; Gardner et al. 1983; Dinkelaker et al. 1989).
capture soil P, although Fe uptake may also be This concentrated release of carboxylates allows
important (Zaïd et al. 2003). Originally thought to be much more P to be extracted from smaller volumes
confined to the Proteaceae, these roots were previously of soil than a mycorrhizal fungus would be able to
termed ‘proteoid’ (Purnell 1960), however, root clus- capture from the same soil volume, thus in these
ters have now been shown to develop on a range of nutrient deficient soils this is a much more effective
different plant species belonging to a number of P capture mechanism, albeit at a higher carbon cost
different families including Betulaceae, Fabaceae (no- to the plant. In some species such as lupins the
tably lupins), Casuarinaceae, Myricaceae, Mimosaceae, release of protons (H+) is also thought to be
Eleagnaceae and Moreacea (Skene 1998), thus, the important in acidifying the rhizosphere to further
more inclusive ‘cluster roots’ is now used. enhance P capture (Dinkelaker et al. 1989), although
There are two main types of cluster roots: H+ release may simply be related to carboxylate
‘simple’, bottle-brush-like cluster roots and ‘com- export (Neumann et al. 1999).
pound’ cluster roots made up of a collection of Exudation of acid phosphatases (APases) by
many ‘simple’ cluster roots together and which can cluster roots may further enhance P acquisition by
form dense mats of roots in the upper soil-organic allowing organic forms of P to be utilised (Adams
horizons (Shane and Lambers 2005). The rootlets and Pate 1992; Gilbert et al. 1999; Neumann and
that make up a cluster root grow only 0.6–35 mm Martinoia 2002). In many soils the availability of
long but can be densely covered in root hairs, thus organic P is limited by the low solubility of
further increasing the root’s surface area. According recalcitrant organic P forms (such as Ca/Mg-phytates
to Lamont (2003) individual ‘clusters’ are generally and Fe/Al-phytates). Solubilization of these organic P
2–75 mm in length and 1–34 mm in width, although forms by the exuded carboxylates may allow these P
some can be much larger (i.e. up to 200 mm long and forms to be broken down by the APases, thus
70 mm wide in some Hakea species). The develop- releasing P that would otherwise be unavailable to
ment of cluster roots is generally followed by a short, the plant. Braum and Helmke (1995) showed that in
marked exudative burst of predominantly carboxy- lupins isotopically exchangeable P values were
lates (notably citrate and malate) and other organic significantly larger (by 2–5 times) and 32P specific
chelators such as phenolics as well as enzymes such activities were lower than those of soybean indicating
as acid phosphatases (Gardner et al. 1983; Gilbert et lupin was accessing a chemically different (and
al. 1999; Roelofs et al. 2001; Weisskopf et al. 2006a). larger) P pool than soybean. Cluster roots can also
The tri-carboxylate citrate is particularly effective at release isoflavonoids at higher rates than non-cluster
replacing P held on exchange surfaces (such as roots (Weisskopf et al. 2006a). Bacterial populations
crystalline Al(OH)3 or Fe(OH)3) and complexing in the rhizosphere of cluster roots are reduced at the
with metal ions in the solid phase which constitute time of citrate release (Weisskopf et al. 2006b). As
the exchange matrix on which the P is held (e.g. Ca in isoflavonoids potentially have anti-microbial proper-
rock phosphate, Fe3+ in Fe(OH)3; Jones 1998). In ties, their function may be to inhibit microbial
many soils P is only released in appreciable amounts activity in the rhizosphere prior to the release of
following these very high levels of carboxylate citrate to reduce the possibility of microbial degrada-
addition. The exudative burst can last a few days tion (Weisskopf et al. 2006a, b).
and in lupins at least, follows a diurnal pattern (Watt Many cluster root studies have used lupins as the
and Evans 1999). model plant (e.g. Dinkelaker et al. 1989; Gardner et
Plant Soil (2009) 321:153–187 169

al. 1983; Watt and Evans 1999) probably due to their extent to which Cyperaceae rely on dauciform roots in
economic value. Therefore it remained to be deter- different habitats remains to be addressed.
mined if different species varied in the compounds
exuded from their cluster roots under comparable
experimental conditions. Roelofs et al. (2001) Root response to biotic and abiotic stress
addressed this question by studying a range of
Australian Banksia, Hakea and Dryandra species Root response to micro-organisms
(Proteaceae) for the carboxylates released. The rela-
tive contributions of different carboxylates did vary Though root systems are genetically determined (see
between species, although certain compounds (e.g. ‘Physiological and genetic determinants of root
malate, malonate, lactate, citrate and trans-aconitate) growth and architecture’ above) they can be strongly
made up a large proportion of the total carboxylates influenced by a wide range of abiotic and biotic
released. Unlike lupins however, no proton release factors, including the presence of soil micro-
accompanied the release of the carboxylates in these organisms. In some cases the effect upon root growth
species (Roelofs et al. 2001). Similarly, Denton et al. and morphogenesis are clearly evident with the
(2007) found that widespread Banksia species did not formation of visible novel organs (e.g. root nodules
exhibit greater plasticity in the composition of exuded in the Rhizobium-legume symbioses), while in others
carboxylates compared to rare Banksia species. Thus, the impact upon roots are much less evident (e.g.
rarity could not be explained by limited phenotypic following colonisation by AMF or rhizobacteria)..
adjustment to carboxylate exudation. Moreover, when
the widespread species were grown on the soil in Pathogenic fungi
which the rare species occurred, the widespread
species did not exude the same composition of Pathogenic fungi reduce plant growth (see other
carboxylates as that by the rare species. This is chapters in this volume), and affect root architecture.
important as it argues against a particular carboxylate In tomato plants infected by Rhizoctonia solani, the
composition being optimal for maximising phospho- root system is characterized by the scarcity of short
rus acquisition from a particular soil. adventitious roots and the emergence of many short
In sedges (Cyperaceae) another specialised root laterals, leading to a more branched root system
morphology has been recognised: dauciform roots (Berta et al. 2005; Sampò et al. 2007) and a reduction
(after the Latin daucus for carrot; Lamont 1974). of mitotically active apices (Fusconi et al. 1999). A
Dauciform roots can vary in size and shape among higher degree of branching has also been reported for
plant genera but tend to be short lateral roots with tomato roots infected with Phytophthora nicotianae
dense clusters of long root hairs, cone or ‘carrot-like’ var. parasitica (Trotta el al. 1996). R. solani and
shaped and are short-lived (Shane et al. 2005). Pithium sp. have been shown to induce a more
Although Lamont (1974) noted up to forty differences monopodial type of branching pattern, with fewer
in the morphological and anatomical characters of orders of branching than uninfected controls in
dauciform and cluster roots, and while cluster roots tomato and Medicago sativa, respectively (Larkin
are associated with dense clusters of roots while 1995; Sampò et al. 2007). These modifications, which
dauciform roots are associated with dense mats of result in a root system that is inefficient both in
root hairs, these two root forms are actually function- nutrient capture and transport (Fitter and Stickland
ally similar. Both release large amounts of carbox- 1991), may be explained by hormonal imbalance.
ylates (notably citrate) and at similar rates from
mature roots, in both the composition of carboxylates Cyanobacteria-invaded coralloid roots
released alters with developmental stage, both release
APases, both are short lived and both are induced at These roots are typical of Cycads, a very ancient
low plant P and suppressed at high plant P levels group of Gymnosperms naturally distributed over four
(Playsted et al. 2006; Shane et al. 2006). The of the five continents with the exception of Europe,
distribution of the Cyperaceae is much more wide- although here they are cultivated for ornamental
spread than that of cluster rooted species but the purposes. Coralloid roots are characterized by dichot-
170 Plant Soil (2009) 321:153–187

omous branching, forming coral-like shapes. Their induced by Bradyrhizobium (the name is associated
development begins with the formation of young with the slow growth of these bacteria) on tropical
roots named precoralloids that, when mature, are legumes. Nodule formation is a multistep process.
invaded by cyanobacteria located between the cells of Rhizobia move to roots by positive chemotaxis in
the root cortex (Douglas 2002). New precoralloid response to root exudates. The bacteria then infect the
roots originate at the basis of preexisting ones (Ahern host roots via root hairs, or via wounds and lesions, or
and Staff 1994). through spaces occurring around root primordia or
Coralloid roots infected by cyanobacteria are adventitious roots. In the case of root-hair infection,
surrounded by a pronounced layer of mucilaginous the attachment of Rhizobia leads to root hair curling,
material, where cyanobacteria occur as short hormo- Rhizobia then enter the root by invagination of the
gonial filaments, the infective units of the Nostoc plasma membrane, and induce formation of an
species involved in the symbiotic association (Grilli infection thread, a growing tube with cell wall
Caiola 2002). Hormogonia penetrate the roots through material filled with growing bacteria (Sadowsky
breaks in the dermal layer and reach, through a 2005). Rhizobia move down the infection thread
cortical channel, the cyanobacterial zone, which is the towards the root cortex, where cell division leads to
structural and physiological site of the Cycas- the production of nodule primordia, functioning as a
Cyanobacteria symbiosis. In this zone, even though meristem (Amor et al. 2003). The primordium gives
the cyanobionts contain photosynthetic pigments, rise to the mature nodule, in which meristem, invasion,
they behave as mixotrophic in terms of their carbon infected and degenerative zones occur. The bacteria are
source, while they perform nitrogen fixation in released (but are always surrounded by the host plasma
specialized cells ( i.e. heterocysts), where the nitro- membrane) in the invasion zone, in cells which
genase enzyme is synthesized and protected (Grilli elongate and increase in size while bacteria proliferate
Caiola 2002). and differentiate into the active form (bacterioids)
(Nardon and Charles 2002). In pea, the genes
Legume nodules controlling nodule morphogenesis have been identified
for plant tissue colonization and differentiation of
Nodules are specialized root organs in which symbi- bacteria into bacterioids and for the development of
otic bacteria (Rhizobia) are able to convert atmo- nodule tissue (Borisov et al. 2007). The genetic system
spheric nitrogen into ammonia as a nitrogen source controlling nitrogen-fixing symbiosis development in
(see also Biological nitrogen fixation section in this plants likely evolved from the system controlling AM
volume). Establishment of the Rhizobium-legume symbiosis (Borisov et al. 2007).
symbiosis depends on a molecular dialogue: flavo- Rhizobia obtain carbon compounds, especially
noids excreted by host plant roots induce the malate, from their host and in turn perform nitrogen
expression of bacterial nod genes, which encode fixation at the centre of the nodule in a microaerobic
protein involved in the synthesis and excretion of zone surrounded by a layer of very closely packed
specific lipochitooligosaccharide signalling molecules cells with few air spaces. In this zone, the nitrogenase
called Nod factors, that in turn are recognised by host enzyme can catalyze the reaction of nitrogen fixation
legumes (Amor et al. 2003; Sadowsky 2005). without being inactivated by oxygen (Douglas 2002).
Responses to Nod factors by root hairs include: Rhizobia respire aerobically which is possible due to a
altered ion fluxes and plasma membrane depolarisa- plant pigment, leghemoglobin, that binds oxygen with
tion, calcium spiking, root hair deformation (due to high affinity, so carrying it to bacterial cells. When
changes in the actin cytoskeleton), and early nodulin symbiotic interactions are efficient, the result is a pink
gene expression. In cortical cells, Nod factors induce root system, due to the presence of this pigment
nodulin gene expression and cell division leading to (Andersson et al. 1996; Kawashima et al. 2001).
nodule primordium formation (Amor et al. 2003).
In legumes Rhizobia induce two types of nodules: Ectomycorrhizal (ECM) roots
determinate and indeterminate (Douglas, 2002). The
latter are the most commonly formed on temperate ECM are formed by mutualistic interactions between
legumes by Rhizobium species, while the former are soil fungi and the roots of woody plants (see also the
Plant Soil (2009) 321:153–187 171

section on Rhizosphere micro-organisms, this vol- growth of the root apices was normal (Harley and
ume). In ECM plants, roots usually have very few, or Smith 1983). However, developmental and topologi-
no, root hairs and tend to be short and thick. The root cal approaches have now revealed that AMF do
apices are generally covered with a fungal mantle influence the root system structure of their host and
(sheath), from which hyphae extend into the soil, and that these effects occur in both monocotyledon and
become mitotically inactive (Clowes 1981). Within dicotyledon plants. Developmental approaches de-
the root, hyphae always remain apoplastic and can scribe the root system based on chronology of
colonize the epidermal (angiosperms) and the cortical development, where higher order laterals develop
cell (gymnosperms) layers, forming the Hartig net, a from a lateral of lower order whereas topological
complex branched structure, which mediates nutrient analysis is based on graph theory, a mathematical
transfer between fungus and plant (Smith and Read approach that describes branch structure (see Root
2008). The most evident root modifications are the architecture section above). The latter, applied to root
early formation of lateral roots and a dichotomy of the systems by Fitter (1985), allows a branching analysis
apical meristems in a number of species. External not confined to just the degree of branching, but
hyphae extend out of the depletion root zones, to extended to the root arrangement or pattern: i.e. two
explore the soil substrate and are responsible for the root systems with the same degree of branching can
nutrient capture and water uptake of the symbiotic differ in their structure (from herringbone-like to
tissues. ECM fungi provide phosphate, the most dichotomous). Berta et al. (1990) demonstrated
immobile ion in the soil, and ammonium and in increased branching of secondary roots of leek, and
return they receive plant carbonic compounds (Harley an overall longer root system when colonized by the
and Smith 1983). The fungi may also acquire AMF Glomus sp. (strain E3), however, although
nutrients from more complex organic substrates, but single roots were shorter than those from uncolonised
large differences between different species and even plants, no evidence was found for an altered topology.
among strains of the same fungus exist in accessing Similarly, Schellenbaum et al. (1991) also reported
these complex substrates (Read and Perez-Moreno increased branching of Vitis vinifera roots when
2003; Hodge et al. 1995). The structure of ECM is colonised by the AMF G. fasciculatum, with greater
essentially determined by the fungal species rather effects on higher order laterals, whose length, con-
than the host plant, however there is considerable trary to the resuts from leek, also increased. Effects on
variation in the degree of host specificity among number and length of laterals, rather than of primary
species and even among strains of ECM fungi (Le roots, have been also shown in another woody plant,
Quéré et al. 2004). Platanus acerifolia (Tisserant et al. 1996). In contrast
to the data on leek, both these latter studies showed
Arbuscular mycorrhizal (AM) associations evidence of altered topology, with AM V. vinifera root
systems exhibiting a more random pattern and P.
AM are symbioses between soil fungi (order Glom- acerifolia a more dichotomous one, thus suggesting a
eromycota) and the roots of most terrestrial plants (see higher capability for nutrient adsorption (Fitter 1985;
also Rhizosphere micro-organisms section, this vol- Tisserant et al. 1992). Other studies also support the
ume). Colonization of the root system by the fungal finding that AMF colonization effects root system
partner is restricted to parenchymatous cells of the development generally by an increase in root branch-
cortex, where it grows both intra- and inter-cellularly. ing (Berta et al. 1995, 2005; Citernesi et al. 1998)
Intracellular haustoria invaginate the host protoplast (Fig. 1 b,c-d) which in turn will increase the surface
and form structures known as arbuscules. These finely area for nutrient absorption although this response
branched hyphae are surrounded by a metabolically may not be universal (Forbes et al. 1996; Vigo et al.
active plant cytoplasm, bounded by a plant mem- 2000).
brane; reciprocal exchanges of metabolites are The root system depends on variations in the
thought to occur at this interface (Smith and Read structure and activity of its apices. All the factors
2008). that directly or indirectly affect root morphogenesis,
It was previously believed that AM fungi did not affect apical meristem activity. Mycorrhizal colonisa-
influence the development of the root system and that tion is one of these factors, but its impact upon root
172 Plant Soil (2009) 321:153–187

meristem structure and activity has received little reported in mycorrhizal plants. However, other more
attention (see Berta et al. 2002). Studies on leek show specific aspects of the mycorrhizal interaction may be
that adventitious roots when colonized by AMF have influenced by hormones. For example, the lengthen-
a determined pattern of growth. In the colonised ing of the mitotic cycle reported for mycorrhizal root
tissue vacuolation and differentiation of stele and apices of A. porrum, may be related to an increase of
cortex tissues occur close to the apical tissues, thus abscisic acid, known to have an inhibitory effect on
root apices display a pattern of senescence and/or the progression of the cell cycle, and which was
necrosis more rapidly than in non-colonized roots, found at high levels in AM roots of Zea mays
(Berta et al. 1990; Varney and McCully 1991b), and (Danneberg et al. 1992) and also in extraradical
the mitotic cycle of meristematic cells become longer hyphae of two Glomus sp. isolates (Esch et al.
with increasing colonization (Berta et al. 1991). 1994). Other morphogenetic factors that have been
Another effect of AM colonization is an increase of observed in AM roots include hyperpolarization of
the diameter of root apices, leading to thicker roots the root cortical cells (Fieschi et al. 1992).
(Berta et al. 2002). Root growth inhibition observed More recently, studies using the model plant
in A. porrum and in maize, however, is not a general Medicago truncatula have demonstrated that AMF
characteristic of mycorrhizal roots and it does not effect root morphogenesis through an increase in
occur in M. truncatula (Oláh et al. 2005), hence, it lateral root number at a very early stage of the root-
may be related to a specific strategy of growth (or of fungus interaction before hyphae have established
resource acquisition). contact with roots, suggesting that secretion of
The modifications described, especially an increase diffusible factors may be involved (Oláh et al.
in root branching, lead to an increased volume of 2005). Lateral root initiation is triggered by the plant
tissue available for AMF colonisation (Fusconi et al. hormone auxin (De Smet et al. 2006b), but in M.
1999), but could also potentially result in higher truncatula the diffusible AMF factors are unlikely to
susceptibility to pathogens. However, in strawberry be an auxin-like substance because of the different
plants infected by Phytophthora fragariae, disease morphogenetic effect following auxin administration.
was found to decrease as the degree of root branching Moreover, Nod factors stimulate lateral root formation
increased (Norman et al. 1996), as a consequence of in a way similar to that of AMF, suggesting that these
different root exudates from AM colonised roots that molecular signals may have a general role as plant
stimulated the production of sporangia by the patho- growth regulators, in addition to their role in the
gen less than exudates from non mycorrhizal straw- nodulation process (Oláh et al. 2005).
berry plants (Norman and Hooker, 2000). Studies The form of a root system is a consequence not
with Lycopersicon esculentum have suggested a only of root development but also of root mortality.
similar involvement of AM root exudates in the How long a root lives (i.e. root longevity) is important
biocontrol of the pathogen P. nicotianae (Vigo et al. both in driving the final form of the root system, and
2000). impacting upon nutrient and carbon fluxes between
One of the main benefit of AMF on plants is the plants and the soil (Berta et al. 2002). The precocious
increased uptake of nutrients, particularly phosphate, inactivation and loss of the meristem of the AM root
and, as a consequence, the P status of the plant tissues apices of A. porrum does not lead to the senescence of
is higher than in non-AM plants grown on the same the differentiated, colonized root tissues. On the
medium (Fusconi et al. 2005). The tissue P content contrary, in these tissues senescence is delayed
may be, by itself, a cause of growth modification (Lingua et al. 1999). In contrast, in tree roots AMF
(Fusconi et al. 1994, 2000). Morphogenetic effects of promote senescence of the fine rootlets and, conse-
AMF on the root system, dependent or not by P, are quently, their turnover, so making a significant
probably mediated by changes in hormone synthesis, contribution to biogeochemical cycling (Atkinson et
transport or sensitivity. Altered levels of auxin al. 1994). The different fungal effects on root
(Kaldorf and Ludwig-Müller 2000; Torelli et al. longevity could be related to root function, as A.
2000), cytokinin (Barker and Tagu 2000; Torelli et porrum adventitious roots are primarily engaged in
al. 2000), ethylene (Vierheilig et al. 1994) and exploration, whilst higher order roots of trees are
gibberellins (Shaul-Keinan et al. 2002) have all been primarily engaged in absorption. These two strategies
Plant Soil (2009) 321:153–187 173

(delayed senescence and root turnover) enable AM ical impedance, water stress and poor aeration which
fungi to accomplish the same result, namely a more can all severely limit root growth in soil. The root
vital and efficient root system. response to poor aeration will be considered in detail
and the impacts on global processes as well as
Plant growth promoting rhizobacteria (PGPR) microbial activity and nutrient cycling discussed.

Root system structure is also influenced by other Mechanical impedance

beneficial soil micro-organisms such as the root
colonizing “Plant Growth Promoting Rhizobacteria Roots are subject to mechanical impedance when the
(PGPR)” (see sections on Plant growth promotion and force required to displace soil particles as the root
beneficial bacteria, elsewhere in this volume). grows increases. As a result, root diameter behind the
PGPR’s affect root architecture by increasing total root tip increases and root elongation decreases with
root length and branching as a consequence of increasing soil strength. Materechera et al. (1991)
hormone production and improved plant mineral reported that dicotyledons (with large diameters)
nutrition (Gamalero et al. 2002, 2004; Lemanceau et penetrated strong soils more than graminaceous
al. 2005). In turn, these changes to the root system monocotyledons (with smaller diameters), and from
architecture likely impact upon microbial dynamics in this suggested that dicotyledonous species may exert
the rhizosphere through altered rhizodeposition in- greater axial growth pressures than monocotyledon-
cluding changes in signalling molecules released ous species. However, in studies where maximum
(Bais et al. 2006; Jones et al. 2004) axial root growth pressure (σmax) has been directly
To summarise, the information presented in this measured, no relation between the σmax and the
section supports the idea of root systems as very ability to penetrate strong soil has been found
plastic structures, influenced by the soil micro- (Whalley and Dexter 1993), including in studies
organisms, yet also able to influence them. For where monocotyledons and dicotyledonous species
example, in coralloid roots, Cycas are able to regulate have been directly compared (Clark and Barraclough
the growth of cyanobacteria outside the root by 1999). Thus, the ability to penetrate strong soils may
inducing hormogonia, and also inside the root to instead be directly related to root diameter (see
promote conditions for maximum nitrogen fixation Materechera et al. 1992; Clark et al. 2003). Changes
(Grilli Caiola 2002); plants control the extent of AM in root elongation and diameter due to mechanical
colonization (Vierheilig 2004) while hyphal density impedance are likely controlled by ethylene produc-
and anastomosis rate also show a plant species effect tion (He et al. 1996; Sarquis et al. 1991). Sarquis et al.
(Giovannetti et al. 2004). On the other hand, plants (1991) demonstrated that evolution of ethylene
with different root system structure and physiology, increased within 1 h following application of me-
are differently dependent upon mycorrhization chanical impedance to roots. Furthermore, addition of
(Azcón and Ocampo 1981; Fitter 2004) while, in various inhibitors of ethylene action and synthesis
turn, colonisation by mycorrhizal fungi may impact helped restore root elongation rates in these mechan-
upon root system structure (Berta et al. 2005). ically impeded roots, highlighting the importance of
ethylene in control of the root response to mechanical
impedance (Sarquis et al. 1991).
Root response to abiotic stress
Water stress
Soil is the most complex of all environments
containing liquid, gaseous and solid phases, the ratios Generally, water is believed to be available for plant
of which can change depending on the prevailing uptake at matric potentials greater than -1.5 MPa (the
conditions. Thus, this complexity presents several wilting point of many mesophytic plants), but root
challenges to the growing root and in this section growth can be severely slowed by potentials greater
some of the abiotic stresses that impact upon the root than this value (Bengough 2003). Schenk and Jackson
and the roots response to these stresses will be (2002a) surveyed the literature on root system sizes
discussed. In particular, we will focus upon mechan- for individual plants from deserts, scrublands, grass-
174 Plant Soil (2009) 321:153–187

lands and savannas all with ≤ 1,000 mm mean annual promotive effects of these two stresses as while
precipitation. They found that maximum rooting hypoxia and mechanical impedance had strong syn-
depth showed a strong positive relationship with ergistic effects on ethylene production actual aeren-
mean annual precipitation for all plant growth forms, chyma formation did not show a synergistic effect
except shrubs and trees. Moreover, maximum rooting (He et al. 1996). Aerenchyma allow gas (notably
depth for all growth forms tended to be shallowest in oxygen) to be transported from the shoot to the root
arid regions and deepest in subhumid regions, which either via simple diffusion, or possibly under pressure
was thought to be the result of more restricted water flow (Jackson and Armstrong 1999). Aerenchyma are
infiltration depths in areas with lower precipitation. therefore essential for the internal ventilation of roots
These results appear to contradict the widely held in an anaerobic environment. However, there may be
view that rooting depth increases in drier environ- a trade-off between root mechanical strength and
ments. However, as Schenk and Jackson (2002a) aerenchyma formation particularly in plant species
state, the distinction between relative and absolute that lack a multiseriate ring of tissue for mechanical
rooting depths is critical. Thus, for a given canopy protection in the outer cortex (Striker et al. 2007).
size herbaceous plants do have deeper maximum The movement of oxygen from the shoots to the
rooting depths in drier environments, but as canopy roots also has important consequences for rhizosphere
size increases so too does the absolute rooting depth. micro-organisms, as some oxygen is released from the
However, the relationship is not simply due to root (termed radical oxygen loss (ROL)) into the zone
increased plant size as above– and below–ground immediately surrounding the root. The resulting
allometrics also change with climate. Moreover, “oxidation zone” (Fig. 6) has been estimated to
depths at which plants have 50% or 95% of their extend 1– 3 mm from the root (Van Bodegom et al.
total root biomass are significantly deeper in drier 2001) although its size will depend upon oxygen
than in humid environments (Schenk and Jackson supply versus consumption and the redox buffering
2002b). Water availability is not the only abiotic capacity of the soil. The plant species present is also a
factor that influences rooting depth, soil texture, factor as many wetland plant species are capable of
organic horizon size (Schenk and Jackson 2002b) forming a barrier to ROL in root basal areas, thus
and plant species composition will also dictate the ensuring oxygen reaches the root apex allowing
rooting depth achieved. continued root growth (Armstrong et al. 1991;
McDonald et al. 2002). In contrast, in non-wetland
Soil aeration and aerenchyma formation species oxygen may be more readily lost from the
root, as shown for wheat (Thomson et al. 1992) and
Excess water leading to waterlogging is also prob- barley (McDonald et al. 2001). Even in wetland
lematic for the root as this can lead to hypoxia (low species, however, this barrier to ROL may be more
oxygen). In response to such stress many plants (but ‘leaky’ in some species than others, and monocotyle-
not all i.e. Brassica napus; Voesenek et al. 1999) can dons may produce a tighter barrier to oxygen loss
form aerenchyma, enlarged gas spaces in tissues than dicotyledonous species (Laan et al. 1989; Visser
which exceed those found as intracellular spaces. et al. 2000). The type of aerenchyma that form may
Aerenchyma form either by cell separation (‘schizo- be important in determining how effective the barrier
genous’ aerenchyma) or by cell death and removal to ROL has to be in order to ensure the root tip
(‘lysigenous’ aerenchyma); more is known about receives adequate oxygen. Visser et al. (2000)
formation of the latter as it occurs in many crop suggested that the barrier to ROL needs to be more
species including barley, rice and wheat (Drew et al. effective in species with lysigenous aerenchyma
2000; Evans 2003; Justin and Armstrong 1991). because porosity increases for a considerable length
Aerenchyma formation may be induced by elevated behind the tip (2–6 cm), whereas in species with
ethylene concentrations (Fig. 6; Colmer et al. 2006; schizogenous aerenchyma high porosity is achieved
Drew et al. 2000; but see also Visser and Bögemann much nearer the tip (i.e. within 0.5–1 cm). In addition,
2006). As noted above ethylene also is important in ROL barrier formation may be related to sediment
the roots response to mechanical impedance. Howev- type, redox conditions and microbial oxygen demand
er different mechanisms may be involved in the in the plants habitat (Smits et al. 1990; Laskov et al.
Plant Soil (2009) 321:153–187 175

Fig. 6 Some responses of the plant to oxygen stress caused by Plants can also increase production of adventitious roots near
waterlogging in the soil. Aerenchyma (enlarged gas spaces in the surface of the soil where O2 concentrations may be less
plant tissues) are formed by cell separation or death and limiting. Some O2 will also leaked to the soil resulting in an
subsequent removal of cellular material. Oxygen (O2) is oxidation zone around the root. The size of this oxidation zone
transported from above ground organs to the roots while depends on the extent and effectiveness of any radical oxygen
ethylene (C2H2), carbon dioxide (CO2) and methane (CH4) barrier produced in the roots which may prevent oxygen loss in
from the soil-root environment flow in the opposite direction. the root basal zones but not at the root tips

2006), and upon the type and age of the root; ROL in uptake ability (Garthwaite et al. 2006; Ranathunge et
young adventitious and fine lateral roots can be rapid al. 2003) except when plants are also under P stress
whereas in older parts of adventitious roots and (Fan et al. 2007). Thus, in O2-deficient environments
rhizomes no ROL occurs (Armstrong and Armstrong there may be a trade-off between root morphology
1988). The ROL barrier may be constitutively and physiology to balance the need for nutrient and
produced in some plant species (Visser et al. 2000) water capture and retain adequate oxygen supply to
but induced under stagnant, deoxygenated conditions the root system for root function. Using modelling
in others (Colmer 2003; Insalud et al. 2006; but see approaches Kirk (2003) showed that a system of
McDonald et al. 2002). How the barrier to ROL coarse, aerenchmymatous primary roots with gas-
actually forms is not known but in rice plants a layer impermeable walls allowing oxygen flow to short,
of sclerenchymatous fibres with thick secondary walls fine, gas-permeable lateral roots was the best com-
on the external side of the cortex forms (Clark and promise between the need for internal aeration and
Harris 1981), which may, together with adjacent cell maximum absorbing surface per unit root mass,
layers, become impregnated with phenolic com- which, in fact is, the basic architecture of many
pounds or lipid complexes to form a barrier to ROL wetland root systems.
(Insalud et al. 2006). Some oxygen loss to the rhizosphere may actually
be beneficial to the plant as it may stimulate oxygen
Consequences for nutrient uptake in oxygen-deficient requiring nitrifying bacteria and prevent reduction of
environments toxic ions (e.g. Fe3+ to Fe2+) in the immediate vicinity
of the root. Kirk (2003) estimated that the oxygen lost
The formation of a barrier to ROL may also be to the rhizosphere via fine lateral roots was enough to
expected to interfere with nutrient uptake and trans- allow sufficient nitrification to satisfy half the plant’s
location of water and ions (Clark and Harris 1981). N demand as absorbed NO3-. More studies have been
Evidence suggests however, that the barrier to ROL conducted investigating the influence of low oxygen
does not affect root hydraulic conductivity i.e. water concentrations on P uptake but the results of these
176 Plant Soil (2009) 321:153–187

investigations are conflicting. Lorenzen et al. (2001) aerenchyma facilitating the release of the denitrified
found that under low oxygen concentration plants gases into the atmosphere (Reddy et al. 1989).
adjusted root length less in response to low P than Moreover, some wetland species such as rice have
plants in aerated solution but that this did not been shown to preferentially uptake NH4+ rather than
adversely impact upon nutrient capture. Insalud et NO3- (see Reddy et al. 1989), which may further
al. (2006) found although numbers of adventitious exasperate the loss of N from the plant-soil system via
roots, root dry mass and root-to-shoot ratios increased the denitrification pathway. Many wetland plant
in rice plants 4 d after transferral to stagnant species are also AM (Cooke and Lefor 1998; Bauer
conditions, maximum root length and shoot growth et al. 2003), although colonisation levels and arbus-
declined as did relative P uptake, at least initially, cule frequency may be more depressed than in non-
under low P conditions. In contrast, Rubio et al. waterlogged conditions (Mendoza et al. 2005). The
(1997) found that while waterlogging (thus reduced benefit, in terms of enhanced P capture may also vary
O2 supply) did reduce root-to-shoot ratios of Paspa- with plant-fungal combination (see previous sections,
lum dilatatum, P concentrations were not reduced. and elsewhere in this volume). In a study on AM
Thus, P uptake per unit of root biomass must have colonisation of fens Cornwell et al. (2001) found that
increased under waterlogging conditions which was nine out of ten dicotyledonous species examined
due to production of finer roots with higher physio- formed AMs while the six monocotyledonous species
logical capacity to absorb P as well as an increase in studied were generally non-mycorrhizal. Cornwell et
the availability of P in the waterlogged soil (Rubio et al. (2001) attributed these differences to the extent of
al. 1997). The study by Rubio et al. (1997) was the aerenchyma formation in these plants. In the mono-
only study of the three discussed above which used cotyledonous species well developed aerenchyma
soil. Studies in stagnant solution culture enable the formed which would be able to oxidise the rhizo-
responses of roots to be easily studied but they do not sphere promoting phosphorus mineralisation and its
reflect the complex nutrient dynamics that occur in subsequent availability to the plant, thus rendering
the soil matrix. Saleque and Kirk (1995) proposed O2 these species less reliant on AM fungi to enhance P
release from roots results in Fe2+ oxidation which, capture. However, Šraj-Kržič et al. (2006) found no
due to the release of H+, acidifies the rhizosphere relationship between AM colonisation and aerenchy-
sufficiently to increase the pool of available P. Under ma ratio in their study on various emerged and
P deficiency, plant release of H+ also increased due to submerged plant species, but did find positive
uptake of NH4+ rather than NO3- in O2-stressed plants correlations between AM colonisation frequency and
resulting in an additional mechanism to acidify the intensity and plant available phosphorous. As AM
rhizosphere and potentially increase P solubilization fungi are known to be multi-functional (Newsham et
(Kirk and Du Le Van 1997). Thus, studies which do al. 1995), AM colonisation may confer benefits to
not use soil as the growth medium will not have the their host other than simply enhanced P capture under
same spatial-temporal P release dynamics and conse- waterlogged conditions.
quently may underestimate the capture of P under
oxygen deficient conditions. Aerenchyma formation and methane emissions

Aerenchyma and soil micro-organisms In addition to allowing the flow of oxygen from
shoots to roots and the surrounding soil, aerenchyma
Oxygen release by aerenchymatous plants also has also act as important conduits of gases such as carbon
important impacts on nutrient cycling in flooded soils dioxide, ethylene and methane in the opposite
(Fig. 6) via impacts on the bacterial community direction (Fig. 6). Methane (CH4) emission in
(Bodelier and Frenzel 1999; Reddy et al. 1989). The particular has important consequences for global
stimulation of nitrifying bacteria in the oxidation zone carbon cycle and global warming. The International
may positively impact on the plant’s nutrition by Panel on Climate Change (IPCC) report that CH4 is c.
releasing NO3- from the soil/sediment for root uptake, 21 times more effective at trapping heat in the earth’s
although some of the converted NO3- may diffuse into atmosphere than CO2 over a 100 year period. Natural
anaerobic areas and be lost via denitrification with the and agricultural wetlands contribute c. 40–50% of the
Plant Soil (2009) 321:153–187 177

total methane emitted to the atmosphere on a global Acknowledgements AH thanks Alastair Fitter, Anna Armstrong
basis and a positive correlation between CH4 emis- and Deirdre Rooney for comments on the ‘Root Function’ and
‘Root Response to Abiotic Stress’ sections. We also thank three
sion and net ecosystem production for a range of anonymous referees for their comments which helped greatly
global wetlands has been found (Whiting and Chan- improve the manuscript.
ton 1993). Moreover, c. 3% of daily net ecosystem
productivity can be emitted directly back to the
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