Biodiversity Science ›› 2017, Vol. 25 ›› Issue (4): 418-426.doi: 10.17520/biods.2017015

• Bioinventory • Previous Article     Next Article

Comments on the APG’s classification of angiosperms

Wei Wang1, 2, Xiaoxia Zhang1, 2, Zhiduan Chen1, Anming Lu1, *()   

  1. 1 State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093 2 University of the Chinese Academy of Sciences, Beijing 100049
    1 State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093 2 University of the Chinese Academy of Sciences, Beijing 100049
  • Received:2017-01-13 Accepted:2017-03-15 Online:2017-04-20
  • Lu Anming E-mail:anmin@ibcas.ac.cn

With the rise of plant molecular systematics, tremendous progress has been made in understanding phylogenetic relationships within angiosperms. With the basic phylogenetic framework of angiosperms established, a DNA phylogeny-based angiosperm classification system at the order and familial levels was proposed by the Angiosperm Phylogeny Group (APG) in 1998 and has been updated three times. In this paper, we summarize the major achievements of the APG system as follows: (1) testing the repeatability and predictability of the APG system for angiosperms; (2) resolving the systematic positions of some segregate taxa which were not placed based on morphological characters; (3) proving that it is not reasonable to first divide angiosperms based on cotyledon character; (4) demonstrating the importance of tricolpate/tricolporate pollen and derivatives for angiosperm classification; (5) finding that the centrifugal development of stamens in polyandrous groups have evolved independently many times and should not be used to delimit class or subclass of angiosperms; (6) supporting that most of the families delimited by broad morphological characters are natural; and (7) separating some families which are traditionally regarded as natural. We then point out potential problems that need to be resolved in the future, including: (1) how to harmonize the APG system and the morphology-based systems; (2) establishing new morphological evolution theories on the basis of the APG system; (3) determining whether it is enough to only use “monophyly” as a criterion to circumscribe orders and families; (4) determining morphological synapormorphies of those orders in the APG system; and (5) how to best compile a key to distinguish the orders and families of the APG system and to list their diagnostic characters for orders and families. In addition, we propose suggestions for the phylogenetic relationships and taxonomic status of some taxa mainly distributed in Asia, specifically East Asia, including Illiciaceae, Acanthochlamydaceae, Tetracentraceae, Leeaceae, Rhoipteiaceae, Hippocastenaceae, Aceraceae, Bretschneideraceae as familial status, and dividing Cornaceae sensu lato into Cornaceae sensu stricto and Nyssaceae sensu lato.

Key words: angiosperms, molecular systematics, classification, morphology, monophyly, synapormorphy

Fig. 1

Interrelationships of the APG IV (2016) orders of angiosperms. The dotted lines indicate the conflicting placements between nuclear/mitochondrial and chloroplast trees. The orders with the gray contain at least one taxon with multiple centrifugal development stamens. Pollen and cotyledonal characters are labeled on the right."

Fig. 2

Comparison of the circumscription of Malpighiales between the APG IV (2016) and Takhtajan (2009) systems. The numbers in brackets indicate the serial numbers of the orders of Takhtajan (2009)."

Fig. 3

Comparison of the circumscription of Saxifragales between the APG IV (2016) and Takhtajan (2009) systems. The placement of Cynomoriaceae is based on the result of Bellot et al (2016). The numbers in brackets indicate the serial numbers of the orders of Takhtajan (2009)."

1 APG (1998) An ordinal classification for the families of flowering plants. Annals of the Missouri Botanical Garden, 85, 531-553.
2 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.
3 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.
4 APG IV (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnean Society, 181, 1-20.
5 Bellot S, Cusimano N, Luo S, Sun G, Zarre S, Gröger A, Temsch E, Renner S (2016) Assembled plastid and mitochondrial genomes, as well as nuclear genes, place the parasite family Cynomoriaceae in the Saxifragales. Genome Biology and Evolution, 8, 2214-2230.
6 Cardinal-McTeague WM, Sytsma KJ, Hall JC (2016) Biogeography and diversification of Brassicales: a 103 million year tale. Molecular Phylogenetics and Evolution, 99, 204-224.
7 Carlsward BS, Judd WS, Soltis DE, Manchester S, Soltis PS (2011) Putative morphological synapomorphies of Saxifragales and their major subclades. Journal of the Botanical Research Institute of Texas, 5, 179-196.
8 Chase MW, Fay MF, Savolainen V (2000) Higher-level classification in the angiosperms: new insights from the perspective of DNA sequence data. Taxon, 49, 685-704.
9 Chase MW, Soltis DE, Olmstead RG, Morgan D, Les DH, Mishler BD, Duvall MR, Price R, Hills HG, Qiu Y-L, Kron KA, Retting JH, Conti E, Palmer JD, Manhart JR, Sytsma KJ, Michaels HJ, Kress WJ, Karol KG, Clark WD, Hedren M, Gaut BS, Jansen RK, Kim K-J, Wimpee CF, Smith JF, Furnier GR, Strauss SH, Xiang Q-Y, Plunkett GM, Soltis PS, Williams SE, Gadek PA, Quinn CJ, Eguiarte LE, Golenberg E, Learn GH, Graham S, Barrett SCH, Dayanandan S, Albert VA (1993) Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Annals of the Missouri Botanical Garden, 80, 528-580.
10 Chen ZD, Yang T, Lin L, Lu LM, Li HL, Sun M, Liu B, Chen M, Niu YT, Ye JF, Cao ZY, Liu HM, Wang XM, Wang W, Zhang JB, Meng Z, Cao W, Li JH, Wu SD, Zhao HL, Liu ZJ, Du ZY, Wang QF, Guo J, Tan XX, Su JX, Zhang LJ, Yang LL, Liao YY, Li MH, Zhang GQ, Chung SW, Zhang J, Xiang KL, Li RQ, Soltis DE, Soltis PS, Zhou SL, Ran JH, Wang XQ, Jin XH, Chen YS, Gao TG, Li JH, Zhang SZ, Lu AM, China Phylogeny Consortium (2016) Tree of life for the genera of Chinese vascular plants. Journal of Systematics and Evolution, 54, 277-306.
11 Christenhusz MJM, Vorontsova MS, Fay MF, Chase MW (2015) Results from an online survey of family delimitation in angiosperms and ferns: recommendations to the Angiosperm Phylogeny Group for thorny problems in plant classification. Botanical Journal of the Linnean Society, 178, 501-528.
12 Cronquist A (1981) An Integrated System of Classification of the Flowering Plants. Columbia University Press, New York.
13 Dahlgren R (1983) General aspects of angiosperm evolution and macro-systematics. Nordic Journal of Botany, 3, 119-149.
14 Davis CC, Webb CO, Wurdack KJ, Jaramillo CA, Donoghue MJ (2005) Explosive radiation of Malpighiales supports a Mid-Cretaceous origin of modern tropical rain forests. The American Naturalist, 165, E36-E65.
15 Donoghue MJ, Doyle JA (1989) Phylogenetic analysis of angiosperms and the relationships of Hamamelidae. In: Evolution, Systematics, and Fossil History of the Hamamelidae, vol. 1 (eds Crane PR, Blackmore S), pp. 17-45. Clarendon Press, Oxford, UK.
16 Doyle JA, Hotton CL (1991) Diversification of early angiosperm pollen in a cladistic context. In: Pollen and Spores: Patterns of Diversification (eds Blackmore S, Barnes SH), pp. 165-195. Clarendon Press, Oxford, UK.
17 Feng M, Fu DZ, Liang HX, Lu AM (1995) Floral morphogenesis of Aquilegia L. (Ranunculaceae). Acta Botanica Sinica, 37, 791-794. (in Chinese with English abstract)
[冯旻, 傅德志, 梁汉兴, 路安民 (1995) 耧斗菜属花部形态发生. 植物学报, 37, 791-794.]
18 Friis EM, Crane PR, Pedersen KR (2011) Early Flowers and Angiosperm Evolution. Cambridge University Press, Cambridge, UK.
19 Handel-Mazzetti H (1932) Rhoipteaceae, eine nenu Familie der Monochlamydeen. Feddes Repertorium, 30, 75-80.
20 Harrington MG, Edwards KJ, Johnson SA, Chase MW, Gadek PA (2005) Phylogenetic inference in Sapindaceae sensu lato using plastid matK and rbcL DNA sequences. Systematic Botany, 30, 366-382.
21 Judd WS, Olmstead RG (2004) A survey of tricolpate (eudicot) phylogenetic relationships. American Journal of Botany, 91, 1627-1644.
22 Judd WS, Sanders RW, Donoghue MJ (1994) Angiosperm family pairs: preliminary phylogenetic analyses. Harvard Papers in Botany, 5, 1-51.
23 Lu AM (1989) Explanatory notes on R. Dahlgren’s system of classification of the angiosperms. Cathaya, 1, 149-160.
24 Lu AM, Zhang ZY (1990) The differentiation, evolution and systematic relationship of Juglandales. Acta Phytotaxonomica Sinica, 28, 96-102. (in Chinese with English abstract)
[路安民, 张志耘 (1990) 胡桃目的分化、进化和系统关系. 植物分类学报, 28, 96-102.]
25 Melchior H (1964) A. Engler’s Syllabus der Pflanzenfamilien Band II. Gebrüder Borntraeger, Berlin-Nikolassee.
26 Moore MJ, Bell CD, Soltis PS, Soltis DE (2007) Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proceedings of the National Academy of Sciences, USA, 104, 19363-19368.
27 Rudall PJ, Remizowa MV, Prenner G, Prychid CJ, Tuckett RE, Sokoloff DD (2009) Nonflowers near the base of extant angiosperms? Spatiotemporal arrangement of organs in reproductive units of Hydatellaceae and its bearing on the origin of the flower. American Journal of Botany, 96, 67-82.
28 Saarela JM, Rai HS, Doyle JA, Endress PK, Mathews S, Marchant AD, Briggs BG, Graham SW (2007) Hydatellaceae identified as a new branch near the base of the angiosperm. Nature, 446, 312-315.
29 Soltis DE, Moore MJ, Burleigh G, Soltis PS (2009) Molecular markers and concepts of plant evolutionary relationships: Progress, promise and future prospects. Critical Reviews in Plant Sciences, 28, 1-15.
30 Stevens PF (2001 onwards) Angiosperm Phylogeny Website. Version 12, July2012.
31 Stuessy TF (2010) Paraphyly and the origin and classification of angiosperms. Taxon, 59, 689-693.
32 Sun G, Ji Q, Dilcher DL, Zheng S, Nixon KC, Wang X (2002) Archaefructaceae, a new basal angiosperm family. Science, 296, 899-904.
33 Takhtajan A (2009) Flowering Plants, 2nd edn. Springer, Heidelberg.
34 Thorne RF (1992) Classification and geography of the flowering plants. Botantical Review, 58, 225-348.
35 Wang W, Lu AM, Ren Y, Chen ZD (2009) Phylogeny and classification of Ranunculales: evidence from four molecular loci and morphological data. Perspectives in Plant Ecology, Evolution and Systematics, 11, 81-110.
36 Wu ZY, Lu AM, Tang YC, Chen ZD, Li DZ (2003) The families and genera of angiosperms in China: a comprehensive analysis. Science Press, Beijing. (in Chinese)
[吴征镒, 路安民, 汤彦承, 陈之端, 李德铢 (2003) 中国被子植物科属综论. 科学出版社, 北京.]
37 Xiang XG, Wang W, Li RQ, Lin L, Liu Y, Zhou ZK, Li ZY, Chen ZD (2014) Large-scale phylogenetic analyses reveal fagalean diversification promoted by the interplay of diaspores and environments in the Paleogene. Perspectives in Plant Ecology, Evolution and Systematics, 16, 101-110.
38 Zhang ZY, Lu AM, Wen J (1994) Embryology of Ehoiptelea chiliantha (Rhoipteaceae) and its systematic relationship. Cathaya, 6, 57-66.
[1] Tang Kang,Yang Ruolin. Origin and Evolution of Soybean Protein-coding Genes [J]. Chin Bull Bot, 2019, 54(3): 316-327.
[2] ZHU Wei, YU Li-Xuan, ZHAO De-Hai, JIA Li-Ming. Architectural analysis of root systems of mature trees in sandy loam soils using the root development classification [J]. Chin J Plant Ecol, 2019, 43(2): 119-130.
[3] ZOU Xian-Hua, HU Ya-Nan, WEI Dan, CHEN Si-Tong, WU Peng-Fei, MA Xiang-Qing. Correlation between endogenous hormone and the adaptability of Chinese fir with high phosphorus-use efficiency to low phosphorus stress [J]. Chin J Plant Ecol, 2019, 43(2): 139-151.
[4] Chen Zuoyi, Xu Xiaojing, Zhu Suying, Zhai Mengyi, Li Yang. Species diversity and geographical distribution of the Chaetoceros lorenzianus complex along the coast of China [J]. Biodiv Sci, 2019, 27(2): 149-158.
[5] Tu Weifeng,Zhang Yang,Tang Jie,Tu Yuqin,Xin Jiajia,Ji Hongli,Zhang Nanfeng,Zhang Tao. Comparison of taxonomic morphological characteristics between Rorippa indica and R. dubia [J]. Biodiv Sci, 2019, 27(2): 168-176.
[6] GAO Chen-Guang, QIAO Xian-Guo, WANG Zi, LU Shuai-Zhi, HOU Dong-Jie, LIU Chang-Cheng, ZHAO Li-Qing, GUO Ke. Distribution, community characteristics and classification of Thymus mongolicus steppe in China [J]. Chin J Plan Ecolo, 2018, 42(9): 971-976.
[7] Le Wang, Chen Shi, Jinyan Tian, Xiaonan Song, Mingming Jia, Xiaojuan Li, Xiaomeng Liu, Ruofei Zhong, Dameng Yin, Shanshan Yang, Xianxian Guo. Researches on mangrove forest monitoring methods based on multi-source remote sensing [J]. Biodiv Sci, 2018, 26(8): 838-849.
[8] Zeng Yinwei, Cao Yuman, Sha Xuyang, Li Shuxia, Yang Peizhi, Hu Tianming, Liu Jinlong. An Observation Method of Nodule and Root Morphology without Damage in Real-time [J]. Chin Bull Bot, 2018, 53(5): 661-670.
[9] SUN Xiao-Wei,YANG Qing-Song,LIU He-Ming,WANG Xi-Hua. Classification of plant associations based on a 20 hm2 dynamics plot of evergreen broad- leaved forest in Mt. Tiantong, Zhejiang, China [J]. Chin J Plan Ecolo, 2018, 42(5): 550-561.
[10] Chu Kelin, Ma Xiaoping, Zhang Zewei, Wang Pengfei, Lü Linna, Zhao Qiang, Sun Hongying. A checklist for the classification and distribution of China’s freshwater crabs [J]. Biodiv Sci, 2018, 26(3): 274-282.
[11] Yangjing Peng,Jian Fan,Shaohua Xing,Guofa Cui. Overview and classification outlook of natural protected areas in mainland China [J]. Biodiv Sci, 2018, 26(3): 315-325.
[12] Feng-Jiao SHEN, Qian-Qian REN, Qi DONG, Li ZHU, Jian-Fang ZHANG, Jing YANG, Ran ZHANG, Hong-Zhu LIANG, Jian-Cheng ZHAO, Shuo SHI. A new angiosperms molecular specimen treatment method for field use [J]. Chin J Plan Ecolo, 2017, 41(7): 787-794.
[13] Haining Qin, Lina Zhao, Shengxiang Yu, Huiyuan Liu, Bo Liu, Nianhe Xia, Hua Peng, Zhenyu Li, Zhixiang Zhang, Xingjin He, Linke Yin, Yulin Lin, Quanru Liu, Yuantong Hou, Yan Liu, Qixin Liu, Wei Cao, Jianqiang Li, Shilong Chen, Xiaohua Jin, Tiangang Gao, Wenli Chen, Haiying Ma, Yuying Geng, Xiaofeng Jin, Chaoyang Chang, Hong Jiang, Lei Cai, Chunxin Zang, Jianyong Wu, Jianfei Ye, Yangjun Lai, Bing Liu, Qinwen Lin, Naxin Xue. Evaluating the endangerment status of China’s angiosperms through the red list assessment [J]. Biodiv Sci, 2017, 25(7): 745-757.
[14] Xue Zhang, Yurui Wang, Yangbo Fan, Xiaotian Luo, Xiaozhong Hu, Feng Gao. Morphology, ontogeny and molecular phylogeny of Euplotes aediculatus Pierson, 1943 (Ciliophora, Euplotida) [J]. Biodiv Sci, 2017, 25(5): 549-560.
[15] Xile Zhou, Dongmei Jin, Yicheng Liu, Hui Shang, Yuehong Yan. Sporangia Morphology of Ferns I. Lindsaeaceae [J]. Chin Bull Bot, 2017, 52(3): 322-330.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] Cao Jiashu, Miao Ying. Evolutionary principle and conservation strategies of biodiversity[J]. Biodiv Sci, 1997, 05(3): 220 -223 .
[2] Pengtao Wang, Jing Zhao, Huanhuan Yu. Reactive Oxygen Species Signaling in Stomata[J]. Chin Bull Bot, 2014, 49(4): 490 -503 .
[3] You Wen-hui, Song Yong-chang. A Study on Energy in Vascular Aquatic Macrophyte Communities in Dianshan Lake[J]. Chin J Plan Ecolo, 1995, 19(3): 208 -216 .
[4] Quanying Du, Zhi Li, Shurun Liu, Hongyan Liu. Dynamics of species diversity and characteristics of halophytic plant communities around saline lakes in arid and semi-arid regions of Inner Mongolia[J]. Biodiv Sci, 2007, 15(3): 271 -281 .
[5] Yefei Shang, Ming Li, Bo Ding, Hao Niu, Zhenning Yang, Xiaoqiang Chen, Gaoyi Cao, Xiaodong Xie. Advances in Auxin Regulation of Plant Stomatal Development[J]. Chin Bull Bot, 2017, 52(2): 235 -240 .
[6] Kao Tso-Ching, Cheng Ching-Yung. New Taxa of the Chinese Celastraceae (1)[J]. J Syst Evol, 1988, 26(4): 310 -314 .
[7] Wei Zhou,Xu Li,Kaiyuan Li,Minghui Li. Fish faunal presence value in three first level tributaries of the Salween River in Yunnan, China and its meaning for aquatic nature reserve plan- ning[J]. Biodiv Sci, 2016, 24(10): 1146 -1153 .
[8] CHEN Jin, LI Yang, HUANG Jian-Hui. Decomposition of mixed litter of four dominant species in an Inner Mongolia steppe[J]. Chin J Plan Ecolo, 2011, 35(1): 9 -16 .
[9] Ke-Fu Zhao, Jie Song, Hai Fan, San Zhou, and Meng Zhao. Growth Response to Ionic and Osmotic Stress of NaCl in Salt-tolerant and Salt-sensitive Maize[J]. J Integr Plant Biol, 2010, 52(5): 468 -475 .
[10] WANG Guan-Lin, YANG Huai-Yi, XIA Ran, FANG Hong-Jun, JING Shi-Xi. Cloning and Sequencing the Full-length cDNA of Annexin from Strawberry Fruit[J]. J Integr Plant Biol, 2001, 43(8): 874 -876 .