Evolution of Pollen in the Family Berberidaceae

doi:10.3724/SP.J.1143.2012.11105

Abstract

Abstract:

In the APG III, the family Berberidaceae is placed in the Ranunculales within the basal Eudicots. Here, the phylogenetic relationships within Berberidaceae were reconstructed using the Maximum Likelihood method on sequence data from four genomic regions (nuclear ribosomal 26S rDNA and plastid rbcL, matK, and trnLF). Based on previously reported phylogenetic tree and pollen observation, the pollen morphologies of 16 genera of this family were investigated. Pollen plesiomorphy，synapomorphy, and evolutionary pattern were revealed by Fitch Parsimony analysis. Ten pollen characters, including dispersal unit, polarity, shape class, size, aperture number, aperture position, ectoaperture shape, supratectal elements, tectum sculpture, and exine thickness, were evaluated to reassess phylogenetic relationships. Tracing pollen character evolution showed that Berberidaceae possessed a series of plesiomorphies, such as the monad pollen unit, isopolarity, spheroidal shape and medium size. Apolarity, multiple apertures and global aperture state were found to be synapomorphies for the Berberidoideae, strongly supporting the monophyly of this subfamily. Triaperture was a synapomorphy for both Podophylloideae and Nandinoideae, respectively. Berberidoideae and Nandinoideae shared the synapomorphy supratectal elements absent, which distinguished them from Podophylloideae, and supported the sister relationship between Berberidoideae and Nandinoideae. Pollen evolutionary significance of some genera was discussed, and several pollen characters were suggested to be used for defining certain genera, such as Bongardia and Ranzania.

Key words: Basal Eudicots, Berberidaceae, Molecular phylogeny, Pollen morphology, Character evolution

摘要：

以APG III定义的基部真双子叶分支（Basal Eudicots）中毛茛目（Ranunculales）小檗科（Berberidaceae）为研究对象，选取4个DNA片段（rbcL、matK、trnLF和26S rDNA），利用最大似然法构建分子系统树，结合已报道的花粉形态数据，分析了该科16个属的花粉形态。选择花粉分散单位、极性、形状、大小、萌发孔数目、萌发孔位置、外萌发孔形状、覆盖层上元素、覆盖层纹饰和外壁厚度共10个关键性状，采用简约法推断了该科花粉的祖征、共衍征和演化式样。研究表明：单粒、等极、近球形、中等大小是小檗科花粉的祖征。无极、多萌发孔和周面孔是小檗亚科（Berberidoideae）的共衍征，支持其为一个单系。三萌发孔分别为鬼臼亚科（Podophylloideae）、南天竹亚科（Nandinoideae）各自的共衍征；覆盖层上元素不存在是小檗亚科和南天竹亚科的共衍征，将它们与鬼臼亚科区分开来，同时也支持了小檗亚科和南天竹亚科之间的姐妹关系。此外，对一些属花粉形态的演化意义进行了讨论，提出一些特殊的花粉性状可以用来定义某些属，如Bongardia和兰山草属（Ranzania）。

关键词: 基部真双子叶分支, 小檗科, 分子系统学, 花粉形态, 性状演化

CLC Number:

Q 944

ZHANG Ming-Ying-, LU Lu-, LI De-Zhu-, WANG Hong. Evolution of Pollen in the Family Berberidaceae[J]. Plant Diversity, 2012, 34(01): 1-12.

张明英1、2、3, 陆露1、2, 李德铢1、2, 王红1、2. 小檗科的花粉演化[J]. Plant Diversity, 2012, 34(01): 1-12.

References

王伏雄, 钱南芬, 张玉龙等, 1995. 中国植物花粉形态［M］. 北京: 科学出版社, 84—86
何顺志, 郭宝林, 1997. 贵州产淫羊藿属药用植物花粉形态的扫描电镜观察［J］. 中国中药杂志, 22 (5): 268—270
苏应娟, 刘启宏, 1994. 湖北产八角莲属植物花粉形态研究［J］. 武汉植物学研究, 12 (3): 217—219
肖培根, 王文采, 王蜀秀, 1979. 毛茛科［A］. 中国植物志［M］. 北京: 科学出版社, 27: 73—591
应俊生, 1979. 小檗科八角莲属和桃儿七属新属的研究［J］. 植物分类学报, 17 (1): 15—25
应俊生, 2001. 小檗科［A］. 中国植物志［M］. 北京: 科学出版社, 29: 50—309
吴征镒, 路安民, 汤彦承等, 2003. 中国被子植物科属综论［M］. 北京: 科学出版社
杨德奎, 杨海, 陈政, 2006. 山东毛茛属植物的花粉形态研究［J］. 山东师范大学学报 (自然科学版), 21 (3): 123—125
张金谈, 王萍莉, 1983. 小檗科Berberidaceae花粉形态研究［J］. 植物分类学报, 21 (2): 130—142
周誉, 郭允珍, 孟宪纾, 1990. 唐松草属五种植物的花粉形态研究［J］. 沈阳药学院学报, 7 (4): 274—276
AiryShaw HK, 1973. A Dictionary of the Flowering Plants and Ferns［M］. Cambridge: Cambridge University Press
APG III, 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III［J］. Botanical Journal of the Linnean Society, 161: 105—121
APSA Members, 2007. The Australasian Pollen and Spore Atlas V1.0. Australian National University, Canberra［OL］. http://apsa.anu.edu.au/
Blackmore S, Heath GLA, 1984. The northwest European pollen flora, 30 Berbreidaceae［J］. Review of Palaeobotany and Palynology, 42 (1): 7—21
Blackmore S, Stafford P, Persson V, 1995. Palynology and systematics of Ranunculiflorae［J］. Plant Systematics and Evolution, 9 ［Suppl.］: 71—82
Cronquist A, 1981. An Integrated System of Classification of Flowering Plants［M］. Cambridge: Cambridge University Press
Clarke GCS, Punt W, Hoen PP, 1991. The northwest European pollen flora, 51 Ranunculaceae［J］. Review of Palaeobotany and Palynology, 69 (6): 117—271
Erdtman G, 1952. Pollen Morphology and Plant Taxonomy. Angiosperms. (An Introduction to PalynologyI) ［M］. Stockholm
Furness CA, 2007. Why does some pollen lack aperture? A review of inaperture pollen in eudicots［J］. Botanical Journal of the Linnean Society, 155 (1): 29—48
Furness CA, 2008. Successive microsporogenesis in eudicots, with particular reference to Berberidaceae (Ranunculales) ［J］. Plant Systemtic and Evolution, 273 (3): 211—223
Ghorbani NM, Azizian D, Sheidai M et al., 2008. Pollen morphology of some Adonis L. species (Ranunculaceae) from Iran［J］. Iran Journal of Botany, 14 (2): 165—170
Guan BC, Fu CX, Qiu YX, 2010. Genetic structure and breeding system of rare understory herb, Dysosma versipellis (Berberidaceae),from temperate deciduous forests in China［J］. American Journal of Botany, 97 (1): 111—122
Guo BL (郭宝林), Xiao PG (肖培根), He SZ (何顺志), 1998. The pollen exine ornamentation of Epimedium and its taxonomic significance［J］. Acta Botanica Yunnanica (云南植物研究), 20 (2): 220—224
Heidemarie H, Michael H, 1995. The convergent evolution of exine shields in angiosperm pollen［J］. Grana, 34 (2): 108—119
Jensen U, 1973. The Interpretation of Comparative Serological Results［M］. New York: Academic Press
Kim YD, Jansen RK, 1994. Characterization and phylogenetic distribution of a chloroplast DNA rearrangement in the Berberidaceae［J］. Plant Systematics and Evolution, 193 (1): 107—114
Kim YD, Jansen RK, 1996. Phylogenetic implications of rbcL and ITS sequence variation in the Berberidaceae［J］. Systematic Botany, 21 (3): 381—396
Kim YD, Jansen RK, 1998. Chloroplast DNA restrition site variation and phylogeny of the Berberidaceae［J］. American Journal of Botany, 85 (12): 1766—1778
Kim YD, Kim SH, Kim CH et al., 2004. Phylogeny of Berberidaceae based on sequences of the chloroplast gene ndhF［J］. Biochemical Systematics and Ecology, 32 (3): 291—301
Lee S, Blackmore S, 1992. A palynotaxonomic study of the genus Trollius (Ranunculaceae) ［J］. Grana, 31 (2): 81—100
Lee CH, Lee S, Suh Y et al., 2004. A palynotaxonomic study of Korean Adonis (Ranunculaceae) ［J］. Journal of Plant Biology, 47 (4): 383—390
Liang HR (梁海锐), Yan WM (阎文玫), 1991. Study on the pollen morphology of Epimedium in China［J］. Bulletin of Botanical Research (植物研究), 11 (4): 81—92
Liao L (廖亮), Xu LL (徐玲玲), 1996. A study on pollen morphology of sect. Ranunculus from China［J］. Acta Botanica BorealiOccidentalia Sinica (西北植物学报), 16 (3): 255—261
Loconte H, Estes JR, 1989. Phylogenetic systematics of Berberidaceae and Ranunculales (Magnoliidae) ［J］. Systematic Botany, 14 (4): 565—579
Ma SB (马绍宾), Hu ZH (胡志浩), 1997. A contribution to the geographical distribution and phylogeny of Podophylloideae (Berberidaceae) ［J］. Acta Botanica Yunnanica (云南植物研究), 1 (1): 48—56
Maddison W, Maddison D, 2009. Mesquite: a modular system for evolutionary analysis. Version 2.6. Computer program and documentation distributed by the author［OL］. http://mesquiteproject.org/mesquite/mesquite.html
Meacham CA, 1980. Phylogeny of the Berberidaceae with an evaluation of classifications［J］. Systematic Botany, 5 (2): 149—172
Mitter V, Sharma BD, 1963. Study of Indian pollen grains 2. Ranunculaceae［J］. Pollen et Spores, 5 (2): 285—296
Nair PKK, 1965. Pollen Grains of Western Himalayan Plants［M］. London: Asia Publishing House
Nickol MG, 1995. Phylogeny and inflorescences of Berberidaceae-a morphological survey［J］. Plant Systematic and Evolution, 9 (suppl.): 327—340
Nowicke JW, Skvarla JJ, 1979. Pollen Morphology: The potential influence in higher order systematics［J］. Annals of the Missouri Botanical Garden, 66 (4): 633—700
Nowicke JW, Skvarla JJ, 1981. Pollen morphology and Phylogenetic Relationships of the Berberidaceae［M］. Smithsonian Contributions to Botany, 50: 1—83
Peng Y (彭勇), Chen SB (陈四宝), Liu Y (刘勇) et al., 2006. A pharmacophylogenetic study of the Berberidaceae (s.l.)［J］. Acta Phytotaxonomica Sinica (植物分类学报), 44 (3): 241—257
Perveen A, Qaiser M, 2006. Pollen flora of PakistanL. Ranunculaceae［J］. Pakistan Journal of Botany, 38 (3): 499—509
Perveen A, Qaiser M, 2010. Pollen flora of PakistanLXV. Berberidaceae［J］. Pakistan Journal of Botany, 42 (1): 1—6
Pladat. Palynological database［OL］.http://www.paldat.org/
Punt W, Hoen PP, Blackmore S et al., 2007. Glossary of pollen and spore terminology［J］. Review of Palaeobotany and Palynology, 143 (1-2): 1—81
Robert E, Woodson J, 1928. Dysosma: A new genus of Berberidaceae［J］. Annals of the Missouri Botanical Garden, 15 (4): 335—340
Tatlidil S, Bicakci A, Malyer H et al., 2005. Pollen morphology of Thalictrum L. species (Ranunculaceae) in Turkey［J］. Pakistan Journal of Botany, 37 (2): 203—212
Terabayashi S, 1981. Study in the morphology and systematics of Berberidaceae［J］. Botanical Magazine (Tokyo), 94 (2): 141—157
Terabayashi S, 1985a. The comparative floral anatomy and systematics of the Berberidaceae. II. Systematic considerations［J］. Acta Phytotaxnomica Geobotanica, 36 (1): 1—13
Terabayashi S, 1985b. The comparative floral anatomy and systematics of the Berberidaceae. I. Morphology［J］. Memoirs of the Faculty of Science, Kyoto University, 10: 73—90
Walker JW, 1974. Aperture evolution in the pollen of primitive angiosperms［J］. American Journal of Botany, 61 (10): 1112—1137
Walker JW, Dolye JA, 1975. The base of angiosperm phylogeny: Palynology［J］. Annals of the Missouri Botanical Garden, 62 (3): 664—723
Wang WT (王文采), Xie L (谢磊), 2007. A revision of Clematis sect. Tubulosae (Ranunculaceae)［J］. Acta Phytotaxonomica Sinica (植物分类学报), 45 (4): 425—457
Wang W, Chen ZD, Liu Y et al., 2007. Phylogenetic and biogeographic diversification of Berberidaceae in the Northern Hemisphere［J］. Systemtic Botany, 32 (4): 731—742
Wang W, Chen ZD, Ren Y et al., 2009. Phylogeny and classification of Ranunculales: Evidence from four molecular loci and morphological data［J］. Perspectives in Plant Ecology, Evolution and Systematics, 11 (2): 81—110
Wu ZY (吴征镒), Zhou ZK (周浙昆), Li DZ (李德铢) et al., 2003. The arealtype of the world family of seed plant［J］. Acta Botanica Yunnanica (云南植物研究), 25 (3): 245—257
Xu L (许腊), Lu L (陆露), Li DZ (李德铢) et al., 2011. Evolution of pollen in the Dipsacales［J］. Plant Diversity and Resources (植物分类与资源学报), 33 (3): 249—259
Yuan Q, Yang QE, 2006. Cytology, palynology, and taxonomy of Asteropyrum and four other genera of Ranunculaceae［J］. Botanical Journal of the Linnean Society, 152 (1): 15—26
Yu XS (余旭升), Liu QH (刘启宏), 1991. A study on the pollen morphlogy of Epimedium in Hubei province［J］. Journal of Wuhan Botanical Research (武汉植物学研究), 9 (3): 295—299

[1]	Jun-Yi Zhang, Yue-Hong Cheng, Min Liao, Yu Feng, Sen-Long Jin, Ting-Mei He, Hai He, Bo Xu. A new infrageneric classification of Gastrochilus (Orchidaceae: Epidendroideae) based on molecular and morphological data [J]. Plant Diversity, 2024, 46(04): 435-447.
[2]	Hai-Su Hu, Jiu-Yang Mao, Xue Wang, Yu-Ze Liang, Bei Jiang, De-Quan Zhang. Plastid phylogenomics and species discrimination in the “Chinese” clade of Roscoea (Zingiberaceae) [J]. Plant Diversity, 2023, 45(05): 523-534.
[3]	Yao-Ke Li, Julian Harber, Chuan Peng, Zhi-Qiang Du, Yao-Wu Xing, Chih-Chieh Yu. Taxonomic synopsis of Berberis (Berberidaceae) from the northern Hengduan mountains region in China, with descriptions of seven new species [J]. Plant Diversity, 2022, 44(05): 505-517.
[4]	Zheng-Yu Zuo, Ting Zhao, Xin-Yu Du, Yun Xiong, Jin-Mei Lu, De-Zhu Li. A revision of Dryopteris sect. Diclisodon (Dryopteridaceae) based on morphological and molecular evidence with description of a new species [J]. Plant Diversity, 2022, 44(02): 181-190.
[5]	Gang Yao, Bine Xue, Kun Liu, Yuling Li, Jiuxiang Huang, Junwen Zhai. Phylogenetic estimation and morphological evolution of Alsineae (Caryophyllaceae) shed new insight into the taxonomic status of the genus Pseudocerastium [J]. Plant Diversity, 2021, 43(04): 299-307.
[6]	Santosh Kumar Rana, Dong Luo, Hum Kala Rana, Shaotian Chen, Hang Sun. Molecular phylogeny, biogeography and character evolution of the montane genus Incarvillea Juss. (Bignoniaceae) [J]. Plant Diversity, 2021, 43(01): 1-14.
[7]	Xiangqin Yu, Chunlei Xiang, Hua Peng. Taxonomy in the Kunming Institute of Botany (KIB): Progress during the past decade (2008-2018) and perspectives on future development [J]. Plant Diversity, 2018, 40(04): 147-157.
[8]	Robert A. Spicer. Tibet, the Himalaya, Asian monsoons and biodiversity-In what ways are they related? [J]. Plant Diversity, 2017, 39(05): 233-244.
[9]	ZHENG Xin-, MIN Yun-Jiang-, XU Bo-, SUN Hang-, ZHOU Zhong-Ze. Pollen Morphology of Plants from the Hengduan Mountains and Their Ecological Significance [J]. Plant Diversity, 2015, 37(06): 657-682.
[10]	LIU Dong, WANG Xin-Yu, LI Jian-Wen, QIAN Zi-Gang, WANG Li-Song. Contributions to the Lichen Flora of the Hengduan Mountains, China (6): Revisional Study of the Genus Canoparmelia (Lichenized Ascomycota, Parmeliacaea) [J]. Plant Diversity, 2014, 36(06): 781-787.
[11]	YANG Chen-Xuan, CHEN Li, WANG Juan, YANG Yu-Ming, LI Lu. Pollen Morphology of the Chinese Endemic Clematoclethra (Actinidiaceae) and Its Taxonomic Implications [J]. Plant Diversity, 2014, 36(05): 569-577.
[12]	DONG Hong-Jin, PENG Hua. Relationships within the Lonicera macrantha Complex Based on Morphological and Molecular Data [J]. Plant Diversity, 2014, 36(02): 133-141.
[13]	YU Wen-Bin. Nomenclatural Clarifications of Sinopodophyllum (Berberidaceae) [J]. Plant Diversity, 2014, 36(01): 37-40.
[14]	ZHANG Yu-Xiao-, HU Yu-Xing-, MA Peng-Fei-, ZHANG Li-Na-, LI De-Zhu. Selection of Potential Plastid DNA Barcodes for Bambusoideae (Poaceae) [J]. Plant Diversity, 2013, 35(6): 743-750.
[15]	MAO Feng-Juan-, LI Shuang-Zhi-, XU Qiong-Hua-, MA Shi-Zhu-, ZHANG Dian-Xiang. Pollen Morphology of Glycosmis (Rutaceae) and Its Systematic Implications [J]. Plant Diversity, 2013, 35(2): 109-118.