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A review on mechanism of plant geotropism: developing trend in research on

pine root geotropism

Article  in  African journal of agricultural research · November 2006

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African Journal of Agricultural Research Vol. 1 (4), pp. 078-084, November 2006
Available online at http://www.academicjournals.org/AJAR
ISSN 1991- 637X © 2006 Academic Journals

Review

A review on mechanism of plant geotropism:

developing trend in research on pine root geotropism
Dexian He1 and David B South2*
1
College of Agriculture, Henan Agricultural University, 95 Wenhua Rd., Zhengzhou, Henan 450002, China.
2
School of Forestry and Wildlife Sciences and Alabama Agricultural Experiment Station, Auburn University, Auburn,
Alabama 36849-5418, USA.
Accepted 2 November, 2006

Despite the fundamental importance of gravity-driven growth response in plants, the mechanisms that
result in root geotropism are poorly understood and the signaling pathways involved remain elusive.
Therefore, we reviewed root gravisensing structures and theories (or propositions) explaining root
growth geotropism in directions of genetics, physiology, biochemistry, and environmental influence.
The available data show that the mechanism(s) of root geotropism and root-gravisensing sites depends
on the plant species studied. Based upon such a review, key academic controversies on mechanism of
root geotropism were pinpointed, and developing trend of research on root geotropism was addressed.

Key words: developing trend, hypothesis, mechanism, root geotropism.

INTRODUCTION

Root geotropism; the downward curvature of the root tip Gravity-sensitive structures in plant roots
toward the center of gravity is an essential
characteristic for plant survival. Studies in this area can Although there are no convincing conclusions on where the
be traced back to Charles Darwin (1880) who gave a exact gravisensing site is located, scientists are in agree-
description of geotropism and showed that the root cap ment that the gravity sensitive structures are contained
is essential for root geotropism. A plethora of studies within the most distal segment of the plant root. Resear-
that extend throughout the entire 20th century revealed chers refer to this root segment using different terms such
that perception of a change in root orientation as root cap, root apex, and root tip. However, the rootcap
(gravistimulation) by gravity-perceiving cells results in is an anatomical root tissue, whereas the root apex indica-
the formation of a signal that will have to be transmitted tes a root part distinct from the cap. For some authors, the
to a site of that organ where a curvature response can root tip includes a rootcap, the meristematic zone, the
develop (Blancaflor and Masson, 2003). Recent results elongation zone, and the maturation zone (Li, 1984). For
obtained by different plant species raise critical others, it only includes a rootcap, the quiescent center
questions regarding the mechanism of geotropism and (QC), and some meristematic cells (Suzuki et al., 1994).
several hypotheses have been given on (i) which organ The rootcap has widely been regarded as the gravity-
or structure of the root perceives gravity, (ii) how the sensitive site in various plant species. It is reported that
root responds to gravity, and (iii) how environmental during their initial differentiation stages, rootcap cells can
factors affect geotropism. However, no single hypothe- perceive gravity and cause positive orthogeotropic growth
sis has been accepted regarding the whole mechanism of roots (Hensel, 1986). Ablation of the rootcap results in a
of root geotropism (Sievers and Braun, 1996). loss of geotropism (Pilet, 1972; Barlow, 1974; Moore and
McClelen, 1989) but if rootcaps are replaced, a strong
response to gravity is restored (Pilet and Elliott, 1981;
Moore and McClelen, 1989). Half-decapitated maize (Zea
*Corresponding author’s E-mail: [email protected]. Tel: mays L.) roots bent towards the remaining tip. This sugg-
+01 334 844 1022, Fax: +01 334 844 1084. ests that rootcap cells might produce growth inhibitors that
 Dexian and South 079

influence root gravicurvature (Pilet, 1983). Furthermore, of amyloplasts in geotropic roots of either maize (Moore,
Pilet (1982) propose that maize root geotropism is 1985b) or barley (Hordeum vulgare L.) (Moore, 1985a).
dependent upon rootcap length. Downward curvature Also, in oil palm (Elaeis guin-eensis Jacq.), the direction of
was the least when the rootcap was the smallest, and amyloplast movement could not be used to predict the
the fewer the cell number, the less the geotropic direction of root growth (Jourdan et al., 2000).
response (Pilet, 1982). However, the role of the rootcap Endoplasmic reticulum; The endoplasmmic reticulum
is still unproven as the sole site of graviperception. For (ER) of columellar cells in the rootcap may play a role in
example, Wolverton and others (2002) reported that gravisensing (Zheng and Staehelin, 2001). When maize
maize root geotropism responded to a signal originating roots were positioned horizontally, there was a change in
outside of the cap. In addition, Sack and others (1994) the normal nuclear membrane-parallel distribution pattern
indicated the gravisensing site of frogbit (Limnobium of ER. After resuming their original position, the ER resto-
spongia Bosc Richard) roots was located in the red its normal distribution (Juniper and French, 1973).
elongation zone. Membranes of the nodal ER might modulate the
If the rootcap is the gravity perceiving root segment, gravisensing signals produced by amyloplasts in tobacco
then what tissue of the rootcap perceives gravity? The (Nicotiana tabacum L.) roots (Zheng and Staehelin, 2001).
central columellar cells possess their own specific struc- In cress (Lepidium sativum L.), the distal ER complex was
ture in geotropic roots and are thought by some to con- necessary for root graviperception (Sievers and Heyder-
tain gravity perception sites (Moore and Miller, 1993). Caspers, 1983). However, differences were not observed
Tissue volume and cell number were greater in the either in distribution or surface area of ER between hori-
columella of graviresponsive primary roots, compared zontally placed graviresponsive and non-gravire- sponsive
with those of less graviresponsive roots in castor bean barley roots (Moore, 1985a).
(Ricinus communis L.) (Moore, 1985d) and garden Golgi apparatus; Golgi bodies, or dictyosomes, may also
onion (Allium cepa L.) (Moore, 1985c). While ablation of play a role in geotropism development. Compared with
the peripheral rootcap cells did not alter root curvature, those in nonresponding maize, more Golgi bodies were in
ablation of the innermost columellar cells resulted in the the top of cells (versus the bottom of cells) in geotropically
strongest inhibitory effect on root curvature (Blancaflor responding roots (McNitt and Shen-Miller, 1978).
et al., 1998). However, not all researchers agree with Microtubule and microfilament; Cortical microtubules play
these propositions. On the other hand, it has been a role during morphogenesis of roots and some believe
suggested that the differential graviresponsiveness of they are involved with gravity perception (Staves et al.,
roots is due to other root tissues. The outer cell layers 1997). However, other researchers believe that microtubu-
(especially the epidermis), for example, were reported les and microfilaments are not involved in the gravires-
to play a key role in primary root gravicurvature in ponse of maize roots (Baluska and Hasenstein, 1997;
maize (Maimon and Moore, 1991). Hasenstein et al., 1999). Blocking actin microfilament did
The exact cell organelle that responds to gravity not affect geotropism in rice (Oryza sativa L.), maize, and
remains in doubt. Each of the following reported hypo- cress (Staves et al., 1997). The depletion of endoplasmic
theses on cell organelles-based gravity sensing network microtubule networks and actin microfilament bundles
system is followed by its antithesis: Amyloplast; Amylo- might be related to the sedimentation of large amyloplasts
plasts are widely considered to act as statoliths, and are in cress, tomato (Lycopersicon esculentum Mill.), timothy
thought to settle within the rootcap cell under the (Phleum (pretense L.), and maize (Baluska et al., 1997)
influence of gravity. In roots of mouse-ear cress
(Arabidopsis thaliana (L.) Heynh.) (Kiss et al., 2002), Theories (or propositions) on signal transduction
tea (Camellia sinensis (L.) Kuntze) (Yamashita et al., mechanism of root geotropism
1997), and other species (Moore, 1986a), there was a
close relationship between geotropism and presence of Little is known about the mechanisms involved in gravity
amyloplasts. Geotropic response returned in the decap- signal perception and transduction. The reported theories
ped primary roots after amyloplasts developed in root- (or propositions) on signal transduction pathways of root
cap cells in maize (Barlow, 1974). In contrast, others geotropism fall into the following categories: physiological
studies revealed that amyloplasts are not necessary for and biochemical control, genetic programming, and envi-
roots to respond to gravity (Shen-Miller and Hinchman, ronmental influence.
1974) and that other gravity perception systems exist in
plant cells (MacCleery and Kiss, 1999; Kodera and
Physiological and biochemical control
Sato, 2001). For example, some researchers report no
difference in the size or density of amyloplasts in hori- Starch-statolith model
zontally oriented roots between maize cultivars having
different graviresponsiveness (Moore, 1986b). The As emphasized earlier in this review, the starch-statolith
appearance of root curvature was not followed by a model is the most widely reported hypothesis for explaining
change in the volume, number, and sedimentation rate root graviperception. Statolith sedimentation is considered
080 Afr. J. Agric. Res.

by some to contribute to gravisensitivity (Kiss and Sack, Studies on cytokinin (CTK) are by far fewer than auxin in
1990; MacCleery and Kiss, 1999). Starch-filled roots the field of root geotropism. According to Tan and others
responded to gravistimulus whereas starch- deficient (1989), zeatin may play a role in the root-geotropic respon-
roots did not (Kiss and Sack, 1990). Results from ses of maize and peanut (Arachis hypogaea L.). More
spacecraft experiments provided support for the starch- recently, Aloni and others (2004) postulated that a cyto-
statolith model (Kiss et al., 1998; Smith et al., 1999). kinin gradient across the root cap upon gravistimulation
However, this hypothesis has been challenged since a might contribute to the initial phase of the geotropic
maize mutant lacking amyloplasts expressed geotro- response.
pism (Evans et al., 1986) as did a starchless Arabido- Nitric oxide (NO) is a widespread gaseous signaling
psis mutant (MacCleery and Kiss, 1999). molecule both in animal and plants. There is evidence
showing that NO serves as a signal in root geotropism. Hu
and others (2005) reported that gravistimulation of soybean
Hormone propositions (Glycine max) roots induced asymmetric NO accumulation,
Auxin gradient plays a key role in root geotropism either and direct NO application to the lower side of horizontal
as a geotropic controller or signal transduction mediator roots enhanced gravitropic curvature, whereas application
(Legue et al., 1996). The Cholodny-Went hypothesis to the upper side suppressed it.
suggested that geotropism is controlled by auxin distri-
bution (Hasenstein et al., 1999). A signal originating in Calcium hypothesis
the rootcap might affect auxin distribution in tissues
2
behind the cap. An asymmetry of auxin concentration in Ca + has long been postulated to function as a second
the elongation region of horizontal roots might cause messenger in a wide range of cellular processes. Similarly,
2
differential growth rates. Subsequently, a growth incre- Ca + plays an essential role in the development of root
ase in the upper half and growth inhibition in the lower geotropism. Gravity-induced downward movement of endo-
2
half would result in root curvature. This might explain genous Ca + triggered the redistribution of growth factors
why root curvature was delayed or inhibited after indole- inducing gravicurvature response (Moore and Fondren,
acetic acid (IAA) was applied to the upper side of the 1988). When receiver blocks contained CaCl2, asymmetric
horizontal maize root (Schurzmann and Hild, 1980). distribution of labeled IAA soon appeared within the tissue
Likewise, synthetic auxin 1-naphthale-neacetic acid (Lee and Evans, 1985a) and root curvature developed
2
(NAA) restored root ageotropism after it was added to towards the Ca + source (Lee et al., 1983). Others found
2
an auxin-resistant Arabidopsis mutant (Yamamoto and that polar movement of Ca + from the upper to the lower
Yamamoto, 1998). However, the cellular mechanism of side of a horizontal root tip was characteristic of gravires-
auxin redistribution has not been identified (Hasenstein ponsive roots (Moore, 1985c; 1985e; Moore and Fondren,
2
et al., 1999; Friml et al. 2002) and a recent finding sug- 1988). A delay or decrease in the polar transport of Ca +
gest that some early phases of geotropism might be could result in decreased graviresponsiveness (Moore,
2
independent of auxin gradient (Chen et al., 2002). In 1986b). When gravity induced polar movement of Ca +
addition to auxin, several other hormones are involved across the root tip was retarded, root geotropism was
in the geotropism response. For instance, Pilet and prevented (Lee et al., 1984).
Elliott (1981) reported an increase in abscisic acid
(ABA) content in the lower half and a decrease in the
upper half of horizontally oriented roots. To date, how- Other Factors
ever, there has not been evidence to support the hypo- Other factors also contribute to geotropism signal trans-
thesis that root geotropism depends upon the asymme- duction within the root cell Proteins and enzymes are
trical distribution of ABA. In fact, Moore (1990) reported believed to affect root geotropism. Calmodulin (CaM) might
that ABA is not necessary for geotropism in maize pri- be involved in geotropic sensing and signal transduction.
mary roots. Westberg and others (1994) reported that lateral roots of
Another plant hormone suspected in root geotropism common bean (Phaseolus vulgaris L.) had less CaM than
is gibberellin (GA). When geotropically stimulated, a did primary roots and this might contribute to the difference
redistribution of GA3 was found in the upper and lower in geotropism expressed by those roots. Inhibitors of CaM
half of horizontally positioned roots in horse bean (Vicia activity can block or delay root curvature in maize (Stine-
faba L.) (El-Antably and Larsen, 1974a; 1974b). How- metze, 1990). Other proteins and enzymes, such as acetyl-
ever, others reported that gravicurvature in GA-treated cholinesterase (AChE) (Momonoki et al., 2000), AUX1 pro-
primary roots did not differ from that in untreated roots tein (Marchant et al., 1999), calmodulin kinases (Lu and
in maize (Moore and Dickey, 1985). Feldman, 1997), EIR1 (Luschnig et al., 1998), IAA-inositol
Ethylene is also considered to play a role in root geo- synthase (Momonoki et al., 2000), plasma membrane
tropism (Bucher and Pilet, 1982). For example, Lee and NAD(P)H-like oxidase (Garcia et al., 1999), inositol-1,4,5-
others (1990) suggested that ethylene affected lateral trisphosphate (IP3) (Perera et al., 1999), and J-domain
transport of IAA. proteins (Guan et al., 2003) might also be involved in geo-
 Dexian and South 081

tropism. Environmental Influence

Mucilage or mucilage-like materials might be essen-
2 In addition to gravity, root geotropism can be influenced by
tial for the transport of either calcium (Ca +) (Moore and
various environmental factors, which include light, soil
Fondren, 1986) or substances that mediate root respon-
conditions, chemicals and nutrients.
se to gravity (Moore and McClelen, 1989). When mucil-
age was applied asymmetrically to vertically oriented
root tips, maize primary roots curved towards the mucil- Light
age (Marcum and Moore, 1990). In the presence of
mucilage, root tips of a maize cultivar that was non-res- The expression of root geotropism is light dependent
ponsive to gravity became strongly responsive to gra- (MacDonald and Gordon, 1978). In many species, roots
vity (Moore et al., 1990). grow downward only when the foliage is illuminated (Lu
Organic compounds such as brassinosteroids (BRs) and Feldman, 1997). Roots of a certain maize cultivar
are also believed to be involved in auxin-mediated proc- failed to respond to gravity when seeds germinated in dark-
esses in maize primary roots. Exogenously applied cas- ness or dim green light (Feldman, 1985). Roots of another
tasterone (as an endogenous BR) increased the gravir- maize cultivar lost their geotropic response after being
esponse in an IAA-dependent manner (Kim et al., transferred from light to darkness (Lee and Evans, 1985b).
2000). Suzuki and others (1981) suggest that light affects two
Recent work indicates that reactive oxygen species physiological processes of root geotropism. The first invol-
(ROS) may function as a downstream component in ves photochemical transformation and the second involve
auxin-mediated signal transduction in root gravitropism. a drop in the NADP level in the tissue.
Gravity induced the asymmetric generation of hydrogen With regards to the effectiveness of wavelength, 660 nm
peroxide (H2O2) in maize roots, as did asymmetrically was optimum for geotropism while 460 nm and 560 nm
applied auxin. Moreover, asymmetric application of were less effective (Shen-Miller, 1978). Red light can
H2O2 or antioxidants promoted or inhibited geotropism, induce root geotropism if applied after a gravity stimulus
respectively (Joo et.al., 2001). (Kelly and Leopold, 1992), but if it is applied before the
gravity stimulus there is little effect on curvature (Kelly and
Leopold, 1992).

Genetic control
Soil conditions
Root geotropism is genetically programmed and varies Various soil factors can affect the downward growth of
with species and genotypes. In cereal crops root, geo- roots. Soil with high mechanical resistance can affect
tropism is at least partially gene-controlled (Oyanagi et taproot curvature (Nakamoto, 1994), in part, because inad-
al., 1993). The geotropic response of seminal roots equate soil aeration affects root geotropism (Nantawisa-
might be controlled by a single dominant gene in wheat rakul and Newman, 1992). In addition, low soil water
(Triticum aestivum L.)(Oyanagi et al., 1991). Geotropic content can cause a decrease in the root angle from
characteristics also differ with root types or orders vertical (Nakamoto, 1994). Root geotropic curvature can
within a genotype. For example, tap roots of para decrease with increases in soil temperature (Perbal, 1973).
rubbertree (Hevea brasiliensis (Willd.) Muell.-Arg.] were The optimum pH for geotropism of maize roots was bet-
strongly orthogeotropic, secondary roots either exhibit- ween 5-6 (Nantawisarakul and Newman, 1992).
ted reduced orthogeotropism or were semiplagiotropic,
tertiary and quaternary roots were ageotropic (Roux
and Pages, 1996). In longleaf pine (Pinus palustris Other exogenous factors
Mill.), some lateral roots exhibited positive geotropism
Residues of herbicides and other chemicals applied to
after geotropism in the taproot ceases (South et al.,
commercial seeds (i.e. seed surface sterilants) affect root
2001).
growth and geotropism. Chlorsulfuron and metsulfuron-
So far, the molecular mechanisms underlying plant
methyl caused severe ultrastructural alterations in the root
geotropism are not known (Muller et al., 1998). How-
caps of pea (Pisum sativum L.) and maize, and thus
ever, recent molecular studies have allowed the identi-
influenced root geotropism (Fayez et al., 1995). Tetrazo-
fication of genes that play roles in root geotropism for
lium altered root geotropism of barley, oat (Avena sativa
some species. For example, genes ARG1 and AUX1
L.), rape (Brassica napus L.), sheep fescue (Festuca ovina
(Rosen et al., 1999), AtPIN2 (Muller et al., 1998), PIN3
L.), and wheat (Steiner and Fuchs, 1987). With regards to
(Friml et al., 2002), and RHG (Fukaki et al., 1997) were
widely used sterilants, while no negative effects of H2O2 on
involved in geotropism in Arabidopsis. The CS-IAA1
root geotropism are reported, mercuric chloride (HgCl2) is
gene might be related to the graviresponse during early
said to result in a loss in geotropism in loblolly pine radicles
seedling stages of cucumber (Cucumis sativus L.)(Fujii
(personal communication with Walt Kelley, 1999).
et al., 2000).
Chemicals such as EDTA (ethylene diamine tetraacetic
082 Afr. J. Agric. Res. •
•
•
•
acid), EGTA [ethylene glycolbis (beta- aminoethyl • is the importance of mycorrhizae in pine geotropism
ether)-N,N,N',N'-tetra- acetic acid], HFCA (9-hydroxy- development? What is the relationship between geotropism
fluorene-9-carboxylic acid), NPA (naphthyl-phthalamic and mucilage? Do pine roots express geotropism under
acid), and TIBA (2,3,5-triiodobenzoic acid) can exert sterile conditions, and in the dark? Does pine geotropism
2
influences on root geotropism. In maize, Ca + chelators vary with varied temperatures and nutrient supplies? How
EDTA and EGTA had inhibiting effects on geotropism do chemicals used in forestry affect pine root geotropism?
(Lee et al., 1983; Marcum and Moore, 1990). NPA inhi-
bited root graviresponse in pea (Gaither and Abeles, Completion of the propositions mentioned above could aid
1975), tomato (Muday and Haworth, 1994), and Arabi- our understanding of plant root geotropism, and might also
dopsis (Rashotte et al., 2000), or reduced root geotropic help explain why certain pine seedlings lose natural
curvature in maize (Lee et al., 1990). TIBA retarded geotropism (South et al., 2001).
2
gravity-induced polar movement of Ca + across the root
tip, which prevented root geotropism both in pea and
maize (Lee et al., 1984). Acknowledgement
Other exogenous compounds of Li, B, Na, Mg, P, S,
Zn, and Ag also influence root geotropism. For exam- This paper is part of the Auburn University (AU) Ph.D.
ple, NaCl stimulated while NaF inhibited root geotro- dissertation “Geotropism in pine radicles.” The authors
pism in soybean (Glycine max L.) Merr.) (Bejaoui, 1980) wish to express their great appreciation to AU Professors
and maize (Baehler and Pilet, 1979). Increases in Zn Dean Gjerstad, Scott Enebak, Roland Dute, Glenn Wehtje,
concentration affected geotropism in horse bean (Bo- and Michael Miller for their suggestions and support.
bak and Blanarik, 1987).
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