Angiosperm Phylogeny Group Classification

Prof. B. Ravi Prasad Rao

Biodiversity Conservation Division,
Department of Botany, Sri Krishnadevaraya University, Anantapuramu, Andhra Pradesh.
E mail: [email protected]

INTRODUCTION

Andrea Caesalpino (1583), proposed the first methodical arrangement of plants into

15 ‘higher genera’ on the basis of the structure of trunk and fructification. In the mid 18th

century, Linnaeus published ‘Species Plantarum’ with a complete list of 7000 species of

flowering plants known at that time which were classified under 1000 genera and 23 classes.

Contributions of Linnaeus and his immediate successors have formed a strong base for the

current day classification. Linnaeus and other botanists till the end of 20 th century (e.g.

Bentham & Hooker, 1862-83) classified flowering plants for ease of the identification.

Systematic research in the past 150 years and particularly during the last four decades have

greatly influenced our views on the classification of plants especially angiosperms. Cladistic

information strongly points to the fact that simplistic division of angiosperms into monocots

and dicots do not reflect phylogenetic history. During 1990s, reconstruction of flowering

plant phylogeny took a great step forward. Rapidly accumulating DNA sequences,

particularly from the plastid gene rbcL provided new and informative sets of data. Cladistic

analysis of these was also much improved through the development of phylogenetic theory

and application to analyse the large data sets.

To establish a consensus view of the classification of flowering plants, an

international group of flowering plant systematists christened as the Angiosperm Phylogeny

Group (APG), came together to propose a classification based on sound phylogenetic data

sets in 1998. Till 2010, three versions of classifications have been proposed by this group that

was published in 1998, 2003 and 2009, each superseding the previous systems. Peter F.

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Stevens, one of the authors of all three of the APG classifications maintains a web site,

APweb, hosted by the Missouri Botanical Garden, which regularly update the information

regularly since 2001 (Stevens, 2001 onwards). This web site is a prime source of information

for the latest research in angiosperm phylogeny.

APG CLASSIFICATION (APG, 1998)

With the efforts of 29 botanical systematists around the world, a new system of

classification has been proposed under the umbrella of Angiosperm Phylogeny Group

succinctly known as APG 1998. This system is based on sound phylogenetic principle of

arranging taxa on the basis of established monophyly. It relied on the synthesis of

information from the disciplines of morphology, anatomy, embryology, phytochemistry and

more strongly on molecular studies with reference to DNA sequences of two chloroplast

genes (cpDNA; atpB and rbcL) and one gene coding for ribosomes (nuclear ribosomal 18s

DNA).

APG 1998 recognized 462 families, which were grouped into 40 monophyletic orders

classified under few informal monophyletic higher groups: monocots, commelinoids,

eudicots, core eudicots, rosids including eurosids I and eurosids II, asterids including

eausterids I and euasterids II. The focus was on orders and less on families. Many families

were not classified to order because their positions were either uncertain or unknown. In this

classification, there are 81 unplaced families, 11 placed towards the beginning, 25 towards

the end and 45 in the informal groups. Alternative options are provided for some groups, in

which a number of families can either be regarded as separate taxa or can be merged into a

single larger family.

APG 1998 addressed the deficiencies of earlier classifications with respect to

phylogenetic tree of flowering plants and establishment of major groups or clades within. The

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authors chose to adopt a broad approach in defining the limits of orders, resulting in the

recognition of 40 orders, compared to, for example, 232 in Takhtajan's classification

(Takhtajan 1997). In APG 1998 classification, the monocots are recognized as a

monophyletic clade, but the dicots are placed in separate groups, some are basal to monocots

and the remaining is considered as eudicots or 'true dicots'. Various monocot taxa are placed

in between primitive angiosperms and eudicots, thus overcoming the problem of paraphyly.

APG II (2003)

After five years since the publication of APG classification, considering further

advances in flowering plant phylogenetic research, an updated version of the APG

classification (APG II) was proposed in 2003. The APG II classification recognized 457

families (5 less than APG 1998) and 45 orders (5 more than APG 1998). Within 457

families, there are 55 optional segregates (presented in square brackets), thereby considering

minimum number of families as 402. Of the 45 orders, 44 are placed in 11 informal groups

which were considered more or less monophyletic. Contrary to APG 1998 which has 81

unplaced families, in APG II, this number has been reduced to 40. The list of unplaced

families in the beginning has been reduced to 4 and uncertain families towards the end to 9.

APG III (2009)

To fill further gaps in APG II and to develop a much more stabilized classification,

with recommendations of different scientist groups around the world, a revised and updated

version of APG was published in October, 2009 by a team of 8 scientists in the name of APG

III. This classification followed Backlund & Bremer (1998) principles of rank-based

phylogenetic classification that is applicable at all levels.

APG III recognizes 413 families. Except ten families, viz., Dasypogonaceae,

Ceratophyllaceae, Sabiaceae, Dilleniaceae, Boraginaceae, Vahliaceae, Icacinaceae,

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Metteniusaceae, Oncothecaceae, Cynomoriaceae and Apodanthaceae, rest of the 403 families

are assigned to 59 orders. Of these 59 orders, Amborellales, Nymphaeales, Austrobaileyales

and Chloranthales (covering 8 families) are unplaced, i.e. not included under any clade, and

kept in the begining. The remaining 55 orders are assigned to 11 clades or groups:

magnoliids, monocots, commelinids, eudicots, core eudicots, rosids, fabids, malvids, asterids,

lamiids and campanulids. Order Ceratophyllales is considered as probable sister of eudicots.

Cynomoriaceae, Apodanthaceae and the genera Gumillea Ruiz & Pav., Petenaea Lundell and

Nicobariodendron Vasudeva and Chakrab. were considered as taxa of uncertain position. An

abstract of APG III classification with respect to groups, orders and families is presented in

Table 1 and the complete list of 413 families as per LAPG III sequence and along with

number of genera and species for each family, world distribution and representative genera

(including type genus) can be consulted through Rao and Prasanna (2010).

New orders viz., Amborellales, Berberidopsidales, Bruniales, Buxales, Chloranthales,

Escalloniales, Huerteales, Nymphaeales, Paracryphiales, Petrosaviales, Picramniales,

Trochodendrales, Vitales and Zygophyllales are recognized in APG III. Many genera and

families which were unplaced in APG and APG II classifications are now included in

respective orders; this includes Hydatellaceae (Nymphaeales), Huaceae (Oxalidales),

Rafflesiaceae (Malpighiales), Aphloiaceae, Geissolomataceae and Strasburgeriaceae (all

Crossosomatales), Picramniaceae (Picramniales), Cytinaceae (Malvales), Balanophoraceae

(Santalales), and Mitrastemonaceae (Ericales).

Newly segregated families of APG III for genera previously treated under other APG-

recognized families includes Calophyllaceae (Malpighiales), Capparaceae and Cleomaceae

(both Brassicales), Linderniaceae and Thomandersiaceae (both Lamiales). Many families that

were in square brackets in APG II are now treated clearly: Brassicaceae s.l. have been split

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into 3 families viz., Brassicaceae s.s., Capparaceae and Cleomaceae. However, in some cases,

the broader circumscriptions are retained, e.g., Amaryllidaceae, Asparagaceace and

Passifloraceae. The positions of Ceratophyllaceae, Chloranthaceae and Picramniaceae have

been clarified, for which additional orders have been proposed that were not previously

recognized.

Of the 413 families of APG III, 121 are monotypic, represented by a single genus and

28 of them are represented by single species. As per the current update information given in

the APG website (Stevens, 2001 onwards), the largest family is Orchidaceae (27,800

species/880 genera). Other dominant families are: Asteraceae (23,600 species / 1620 genera),

Fabaceae (19,560/745), Rubiaceae (13,150 /611) and Poaceae (11,337/ 707).

Perusal of the literature has revealed that of the 413 families, 259 are represented in

India. The distribution pattern of the families indicate that 5 families are endemic to

Madagascar, 4 to Cape Province of South Africa and Chile each, 3 to New Caledonia, one

family each for Somalia, Tasmania, China, Fiji islands and Mexico. It is interesting to note

that 24 families are endemic to Australian continent and surrounding islands. African

continent with Madagascar is an exclusive home for 17 families.

A formal classification of the land plants that is compatible with the APG III

classification was proposed by Chase & Reveal (2009). For detailed information on orders

and family delimitations, readers are advised to consult APWeb (Stevens, 2001 onwards) and

for molecular and allied datasets used for separation of different clades, orders and families in

APG, consult APG II (APG II, 2003).

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APG III vis-a-vis BENTHAM AND HOOKER CLASSIFICATION

An attempt has been made to compare the positions of families as treated in Bentham

and Hooker’s classification with that of 413 families of APG III. Thirty five families, (mostly

monotypic) have been described after the publication of Genera Plantarum (Bentham and

Hooker, 1862-83). Significant changes in APG III treatment of families vis-à-vis Bentham

and Hookers’s system include the following. Liliaceae s.l. is split into 14 families and many

of them are transferred to Asparagaceae. Molluginaceae and Gisekiaceae are recognized

separately from Aizoaceae. Euphorbiaceae s.l. is split into Euphorbiaceae s.s.,

Phyllanthaceae, Picrodendraceae and Putranjivaceae. Genera Sopubia and Striga

(Scrophulariaceae) are included in Orobanchaceae; Hydrocotyle (Apiaceae) is included in

Araliaceae. Bombacaceae, Sterculiaceae and Tiliaceae are merged with Malvaceae;

Asclepiadaceae with Apocynaceae; Avicenniaceae with Acanthaceae; Barringtoniaceae with

Lecythidaceae; Chenopodiaceae with Amaranthaceae; Cochlospermaceae with Bixaceae;

Cotylaceae with Betulaceae; Cuscutaceae with Convolvulaceae; Viscaceae with Santalaceae;

Myrsinaceae with Primulaceae; Rhododendraceae and Vacciniaceae with Ericaceae;

Lobeliaceae with Campanulaceae; Valerianaceae with Caprifoliaceae. Many genera of

Scrophulariaceae and Verbenaceae are merged with Plantaginaceae and Lamiaceae

respectively (Refer to Table 2 for details). It is interesting to note that APG like that of

Bentham and Hooker’s system considered Papilionaceae, Caesalpiniaceae and Mimosaceae

as subfamilies of Fabaceae viz., Faboideae, Ceasalpinioideae and Mimosoideae.

LAPG & LAPG III

Haston et al. (2007), developed a linear sequence of families (called as LAPG) based

on APG II classification and provided a list of 479 families. Haston et al. (2009) revised

LAPG for the new APG III classification as LAPG III and considered 413 families. Although

the methodology followed has been questioned by Hawthorne et al. (2008), it is concluded

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that in the absence of any obviously better way of generating a linear sequence from a

phylogenetic tree, APG III can be considered a viable system with options open to modify the

methodology to ensure stability. It is pertinent to note that many European herbaria have

agreed to adopt LAPG. The LAPG sequence has been accepted by RBG Kew, RBG

Edinburgh, the Natural History Museum (London), the Musée National d’Histoire Naturelle

(Paris), Conservatoire et Jardin Botaniques (Geneva) and the National Herbarium Nederland

(Leiden, Utrecht and Wageningen) to re-arrange their herbarium collections.

In APG III, families are alphabetically arranged in clades. In LAPG, families within

the clades are reorganized. With respect to unplaced orders and families at the beginning,

orders sequence in LAPG is similar to that of APG III, but families are re-organised. In

Magnoliid clade, Magnoliales are followed by Laurales, vice-versa in APG III. In the clade

Monocots, orders are in the same sequence as that of APG III. In Commelinids, Zingiberales

are followed by Poales, vice-versa in APG III. Unplaced Dasypogonaceae is retained in the

same clade, but kept in between Zingiberales and Poales, which were kept at the beginning in

APG III. Ceratophyllales and Ceratophyllaceae position as probable sister of eudicots is

unchanged. In Eudicots, orders are in the same sequence like that of APG III. Even unplaced

Sabiaceae is retained in the same position between Ranunculales and Proteales. In Core

Eudicots, orders are in the same sequence like that of APG III. Dilleniaceae, the unplaced

family is retained in the same position after Gunnerales. Cynomoriaceae considered as taxa of

uncertain position and kept at the end in APG III is included in core eudicots in LAPG. There

is no change in Rosids taxa. In Fabids and Malvids, sequence of orders is changed. In

Asterids, sequence of orders is unchanged. In Lamiiids, sequence of orders is changed. Of the

5 unplaced families kept at the beginning in APG III, 3 families are kept at the beginning and

other two placed between Gentianales and Solanales in LAPG.

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 Currently some of the problems of placement of families and genera have been

resolved in the latest update of APG which can consulted on http://www.mobot.org/MOBOT/

research/APweb.

Table1 : ABSTRACT OF APG CLASSIFICATION

Clade/ Group Orders

(No. of orders/families) (No. of. families)
- Unplaced Orders
Amborellales (1) ; Nymphaeales (3)
Austrobaileyales (3); Chloranthales (1)
MAGNOLIIDS (4/20 ) Canellales (2) ; Piperales (5); Laurales (7)
Magnoliales (6)
MONOCOTS (7/47) Acorales (1) ; Alismatales (13); Petrosaviales (1);
Dioscoreales (3); Pandanales (5)
Liliales (10) ; Asparagales (14)
COMMELINIDS (4/31) Unplaced family-Dasypogonaceae
Arecales (1) ; Commelinales (5); Poales (16)
Zingiberales (8)
PROBABLE SISTER OF Ceratophyllales (1)
EUDICOTS (1/1)
EUDICOTS (4/14) Ranunculales (7) ; Unplaced family- Sabiaceae
Proteales (3) ; Trochodendrales (1); Buxales (2)
CORE EUDICOTS (2/17) Gunnerales (2) ; Unplaced family- Dilleniaceae
Saxifragales (14)
ROSIDS (1/1) Vitales (1)
FABIDS (8/73) Zygophyllales (2); Celastrales (2); Oxalidales (7);
Malphigiales (35); Cucurbitales (7); Fabales (4); Fagales
(7); Rosales (9)
MALVIDS (11/ 102) Geraniales (3); Myrtales (9); Crossosomatales (7);
Picramniales (1); Huerteales (3); Brassicales (17)
Malvales (10); Sapindales (9); Berberidopsidales (2);
Santalales (7); Caryophyllales (34)
ASTERIDS (2/28) Cornales (6); Ericales (22)
LAMIIDS (4/40) Unplaced families: Boraginaceae, Vahliaceae,
Icacinaceae, Metteniusaceae, Oncothecaceae
Garryales (2); Gentianales (5); Lamiales (23)
Solanales(5)
CAMPANULIDS (7/29) Aquifoliales (5); Asterales (11); Escalloniales (1);
Bruniales (2); Paracryphiales (1); Dipsacales (2); Apiales
(7)
TAXA OF UNCERTAIN 2 families: Apodanthaceae and Cynomoriaceae
POSITION 3 genera : Gumillea, Petenaea (possibly Malvales) and
Nicobariodendron

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 REFERENCES

Andrea Caesalpino (1583). De plantis libri XVI (1583).

APG (1998). An ordinal classification for the families of flowering plants. Annals of the
Missouri Botanical Garden 85: 531–553.
APG II (2003). An update of the Angiosperm Phylogeny Group classification for the
orders and families of flowering plants: APG II. Botanical Journal of the Linnean
Society 141: 399–436.
APG III (2009). An update of the Angiosperm Phylogeny Group classification for the
orders and families of flowering plants: APG III. Botanical Journal of the Linnean
Society 161: 105–121.
Backlund, A. and Bremer K. (1998). To be or not to be–principles of classification and
monotypic plant families. Taxon 47: 391–401.
Bentham, George and Hooker, J.D. (1862-1883). Genera plantarum: ad exemplaria
imprimis in Herberiis Kewensibus servata definita. London, (3 vols.).
Chase, M. W. and Reveal, James L. (2009). A phylogenetic classification of the land
plants to accompany APG III. Botanical Journal of the Linnean Society: 122–
127.
Haston, E., Richardson, J.E., Stevens, P.F., Chase, M.W., Harris D.J. (2007). A linear
sequence of Angiosperm Phylogeny Group II families. Taxon 56: 7–12.
Haston, E., Richardson, J.E., Stevens, P.F., Chase, M.W., Harris D.J. (2009). LAPG III:
a linear sequence of the families in APG III. Botanical Journal of the Linnean
Society 161: 128–131.
Hawthorne, W.D. and Hughes, C.E. (2008). Optimising linear taxon sequences derived
from phylogenetic trees- a reply to Haston et al. Taxon 57: 1–7.
Rao, B. Ravi Prasad and P.V. Prasanna (2010) Conspectus of Angiosperm Phylogeny
Group Classification and its application to flowering plants of India. Ind. J. Forestry
33 (4): 569-584.
Stevens P. F. (2001 onwards). Angiosperm phylogeny website. Available at
http://www.mobot.org/MOBOT/research/APweb/. Latest retrieved 15-3-16.
Takhtajan A. (1997). Diversity and classification of flowering plants. New York:
Columbia University Press.