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Variation of pollen morphology, and its implications in the phylogeny of Clematis (Ranunculaceae)

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Abstract

Clematis s.l. (including Archiclematis and Naravelia) is a genus of approximately 300 species with cosmopolitan distribution. The diversity of its pollen was surveyed in 162 taxa belonging to all infrageneric groups of Clematis s.l. Pollen morphology was investigated by use of scanning electron microscopy to identify useful characters, test taxonomic and systematic hypotheses, and elucidate pollen character evolution on the basis of the molecular phylogeny. Clematis pollen is small to medium (14.8–32.1 μm × 14.2–28.7 μm), oblate to prolate (P/E = 0.9–1.4) in shape. The apertures may be tricolpate and pantoporate sometimes with 4-zonocolpate and pantocolpate pollen grains as transitional forms. The tricolpate pollen grains are predominant and occur in all the sections of the genus, whereas pantoporate pollen grains can be found in sect. Tubulosae, sect. Viorna, sect. Viticella, and Naravelia only. Phylogenetic mapping of aperture types reveals that the pantoporate pollen type may be the apomorphy in the genus and evolved several times. The surface ornamentation in all taxa studied is similar and characterized by microechinae evenly distributed on the microperforate tectum. The size and density of spinules on the tectum vary greatly but successive in the whole genus. According to the character syndromes of the ornamentation, separating sect. Brachiata from sect. Meclatis is supported. Though pollen morphology may contribute to investigation of problematic taxa, the taxonomic value of pollen morphology is limited at the species level.

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Acknowledgments

The authors thank the herbaria of the Institute of Botany, Chinese Academy of Sciences (PE), Harvard University (GH), the Smithsonian Institute (US), South China Botanical Garden (IBSC), Missouri Botanical Garden (MO), Muséum National d’Histoire Naturelle (P), and the Herbarium of Uppsala University (UPS) for the loans of specimens for examination. We are indebted to Yin-Hou Xiao and Xue-Jian Yang for their assistance with SEM experiments and film development. This study was supported by the Fundamental Research Funds for the Central Universities (grant no. YX2010-31), the State Key Laboratory Program from the State Key Laboratory of Systematic and Evolutionary Botany (grant no. LSEB2011-07), the Main Direction Program of Knowledge Innovation of the Chinese Academy of Sciences (grant no. KSCX2-EW-Z-1), and the National Natural Science Foundation of China (grant nos. 31170201, 81072317, 31110103911).

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Authors and Affiliations

  1. College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083, China

    Lei Xie

  2. State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, The Chinese Academy of Sciences, Beijing, 100093, China

    Liang-Qian Li

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  1. Lei Xie
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Correspondence to Liang-Qian Li.

Appendix

Appendix

Vouchers used for scanning electron microscopy. Species (arranged in alphabetical order), country, collector, collector number, herbarium acronym from index Herbariorum.

Clematis acapulcensis Hook. et Arn.: Costa Rica, A. Smith A656 (GH); C. acerifolia Maxim.: China, Beijing, Shangfangshan, K.J. Guan 75003 (PE); C. acuminata var. longicaudata W. T. Wang: China, Yunnan, Binchuan Xian, T. N. Liou 01776 (PE); C. aethusifolia Turcz.: China, Hebei, Zhuolu Xian, Z. G. Yang 1471 (PE); C. affinis A. St.-Hil.: Brazil, Parana, Koczzcki 53 (P); C. akebioides (Maxim.) Hort. ex Veitch.: China, Gansu, Lanzhou, Y. Q. He 5759 (PE); C. akoensis Hayata: China, Taiwan, Pingbian, T. Y. A. Yang 0271 (PE); C. albicoma Wherry: US, Virginia, Heller 842 (MO); C. alborosea Ulbr.: Peru, C. Vargas 5563 (GH); C. alternata Kitam. et Tamura: China, Tibet, Jilong, Tibet Exped. 6889 (PE); C. apiifolia DC.: China, Zhejiang, Putuoshan, Anonym 1187 (PE); C. aristata R. Br.: Australia, New S. Wales, W. V. Dorrigo s.n. (US); C. armandii Franch.: China, Guizhou, M. Z. Zhang 350 (PE); C. armandii var. hefengensis (G. F. Tao) W. T. Wang: China, Hubei, Hefeng Xian, J.X. Hong 1227 (PE); C. bigelovii Torr.: US, New Mexico, Sandia Mountains, C. C. Ellis 18 (MO); C. bonariensis Juss. ex DC.: Argentina, T. M. Pederson 3658 (US); C. brachyura Maxim.: Korea, Faurie 14 (P); C. buchananiana DC.: China, Yunnan, K. M. Feng 12912 (PE); C. cadmia Buch.-Ham. ex Wall.: China, Jiangxi, Nanchang, Anonym 1688 (PE); C. caleoides Standl. et Steyerm.: Guatemala, A.F. Skutch 105 (US); C. campestris Hil.: Argentina, Tucumán, S. Venturi 686 (US); C. chinensis Osbeck: China, Guangxi, N. K. Liang 2108 (PE); C. chingii W. T. Wang: China, Taiwan, Taizhou, T. Y. A. Yang 02232 (PE); C. chrysocarpa Welw. ex Oliv.: Tanzania, Iringa, Brigood et al. 1306 (UPS); C. chrysocoma Franch.: China, Yunnan, Luquan Xian, Kunming working station 1361 (PE); C. cirrhosa L.: Europe: Anonym s. n. (PE); C. connata DC.: China, Sichuan, Baoxing Xian, G. L. Qu 3835 (PE); C. corniculata W. T. Wang: China, Xinjiang, Yecheng, D. Zheng k102 (PE); C. courtoisii Hand.-Mazz.: China, Henan, Shangcheng Xian, Anonym 276 (PE); C. crassifolia Benth.: China, Guangdong, Anonym 16498 (PE); C. crassipes Chun et How: China, Hainan, Ledong, Z. L. Chen 30349 (PE); C. crispa L.: US, Arkansas, Mississippi valley, Loudewyks, 249 (MO); C. dasyandra Maxim.: China, Hubei, Badong Xian, G. X. Fu and Z. S. Zhang 1066 (PE); C. delavayi Franch.: China, Sichuan, Daocheng Xian, Sichuan Exped. 2095 (PE); C. delavayi var. calvescens Schneid.: China, Sichuan, Derong Xian, Sichuan Exped. 4117 (PE); C. dilatata Péi: China, Zhejiang, M. C. Chang 4933 (PE); C. dioica L.: US, E. L. Ekman H13943 (US); C. dissecta Baker: Madagascar, Fianarantsoa, Malcomber et al. 1390 (UPS); C. drummondii Torr.: US, New Mexico, E. O. Woaton 150 (MO); C. fasciculiflora Franch.: China, Yunnan, Dali Xian, T. N. Liou 017915 (PE); C. finetiana Lévl. et Vant.: China, Guangdong, Pingyuan Xian, L. Deng 4237 (PE); C. flammula L.: France, Corse, P. Aellen 2462 (US); C. foetida Raoul.: New Zealand, H. H. Allai s. n. (IBSC); C. fruticosa Turcz.: China, Hebei, Zhuolu Xian, Z. G. Yang et Z. Q. Zhang 441(PE); C. fusca Turcz.: China, Heilongjiang, X. N. Guan 6 (PE); C. ganpiniana (Lévl. et Vant.) Tamura: China, Guangxi, Hexian, Z. T. Li 604134 (PE); C. ganpiniana var. tenuisepala (Maxim.) C. T. Ting: China, Shanxi, Ruicheng Xian, S. Y. Bao 1536 (PE); C. glabrifolia K. Sun et M. S. Yan: China, Gansu, Wen Xian, K. Sun et al. 0251 (PE); C. glaucophylla Small: US, Florida, Godfrey 84152 (GH); C. glycinoides DC.: Australia, New S. Wales, M. Evans 2659 (GH); C. gouriana Roxb. ex DC.: China, Guizhou, Sichuan and Guizhou Exped. 1602 (PE); C. gracilifolia Rehd. et Wils.: China, Sichuan, Barkam, X. Li 70904 (PE); C. gracilifolia var. dissectifolia W. T. Wang: China, Sichuan, Kangding Xian, Q. Y. Wang 4427 (PE); C. grahami Benth.: US, E. Lyonnet 1315 (US); C. grandidentata (Rehd. et Wils.) W. T. Wang: China, Zhejiang, Changhua, Anonym 28596 (PE); C. graveolens Lindl.: India, B. Khan s. n. (PE); C. grewiiflora DC.: China, Tibet, Jilong Xian, S. Jiang et K. F. Zhao 393 (PE); C. grossa Benth.: Guatemala, A. F. Skutch 2029 (GH); C. haenkeana C. Presl.: Peru, R. Ferreyra 2016 (P); C. hancockiana Maxim.: China, Henan, Xinyang Xian, K. J. Guan 119 (PE); C. henryi Oliv.: China, Chongqing, Nanchuan Xian, P. Tan 2677 (PE); C. heracleifolia DC.: China, Tianjin, Jixian T. N. Liou 4521 (PE); C. hexapetala Pall.: China, Inner Mongolia, Inner Mongolia et Ningxia Exped. 841 (PE); C. hexapetala var. tchefouensis (Debeaux) S. Y. Hu: China, Shandong, Qingdao Laoshan, T. Y. Zhou 1239 (PE); C. hirsuta Guill. et Perr.: Uganda, Albert Nyanza, E. A. Mearns 2550 (US); C. huchouensis Tamura: China, Zhejiang, Haining Xian, L. Yuan 12 (PE); C. ibarensis Baker: Madagascar, Tananarive, Anonym 2520 (P); C. integrifolia L.: China, Xinjiang, Burjin Xian, Anonym 00074 (PE); C. intricata Bunge: China, Hebei, Fuping Xian, K. M. Liu 3279 (PE); C. japonica Thunb.: Japan, K. Hisauti 2729 (PE); C. jialasaensis W. T. Wang: China, Tibet, Nyingchi Xian, W. L. Zheng 1589 (PE); C. jingdungensis W. T. Wang: China, Yunnan, Shunning Xian, C. W. Wang 72020 (PE); C. kirilowii Maxim.: China, Beijing, Zhongde Exped. 583 (PE); C. kockiana Schneider: China, Sichuan, Mabian Xian, D. Y. Hong et al. s. n. (PE); C. kweichowensis Péi: China, Guizhou, Panxian, Anshun Exped. 1245 (PE); C. lancifolia Bur. et Franch.: China, Sichuan, T. T. Yu 1163 (PE); C. lancifolia var. ternata W. T. Wang: China, Sichuan, Miyi Xian, Anonym s. n. (PE); C. lanuginosa Lindl.: China, Zhejiang, Anonym 0737 (PE); C. lasiandra Maxim.: China, Sichuan, Pingwu Xian, L. Xie 2004175 (PE); C. lasiantha Fisch.: Costa Rica, C. F. Baker 499 (GH); C. laxistrigosa (W. T. Wang et M. C. Chang) W. T. Wang: China, Sichuan, T. P. Wang 9614 (PE); C. leschenaultiana DC.: China, Guangxi, Fengshan Xian, L. W. Xu 1411 (PE); C. leschenaultiana var. rubifolia Wight.: China, Guizhou, J. Cavalerie s. n. (PE); C. ligusticifolia Nutt.: Canada, B. Boivin 9436 (GH); C. loureiriana DC.: China, Fujian, G. S. He 9546 (PE); C. macropetala Ledeb.: China, Shannxi, Taibaiding, J. X. Xiang 1041 (PE); C. mandshurica Rupr.: China, Heilongjiang, Dailing, T. N. Liou 7171 (PE); C. mashanensis W. T. Wang: China, Guangxi, Mashan Xian, X. Z. Zheng 112 (PE); C. menglaensis M. C. Chang: China, Yunnan, Mengla Xian, C. W. Wang 80841 (PE); C. metouensis M. Y. Fang: China, Tibet, Mêdog Xian, W. L. Chen 10876 (PE); C. meyeniana Walp.: China, Guangxi, Longsheng Xian, Guangfu Exped. 0900a (PE); C. microphylla DC.: Austrilia, E. N. S. Jackson 4310 (IBSC); C. millefoliata Eichl.: Peru, F. W. Pennell 13263 (US); C. montana Buch.-Ham. ex DC.: China, Sichuan, Kangding Xian, Anonym s. n. (PE); C. nanophylla Maxim.: China, Gansu, Lanzhou, Y. K. Lian 96912 (PE); C. napaulensis DC.: China, Yunnan, M. G. Li 2897 (PE); C. obscura Maxim.: China, Shanxi, Huanqu Xian, S. Y. Bao 92 (PE); C. orientalis L.: China, Xinjiang, Turpan, Z. M. Zhang 294 (PE); C. otophora Franch. ex Finet. et Gagnep.: China, Hubei, Shennongjia, Shennongjia Exped. 11549 (PE); C. paniculata Gmelin: New Zealand, L. Tibell n220 (IBSC); C. parviloba Gard. et Champ.: China, Jiangxi, Longnan Xian, 263 Mission group 1353 (PE); C. parviloba var. longianthera W. T. Wang: China, Sichuan, Emeishan, T. T. Yu 547 (PE); C. patens var. tientaiensis M. Y. Fang: China, Zhejiang, Tiantaishan, X. Y. He 1 (PE); C. pauciflora Nutt. ex Torr. et A. Gray: US, San Diego, W. Deane s. n. (GH); C. peruviana DC.: Peru, R. Ferreyra 7591 (US); C. peterae Hand-Mazz.: China, Shanxi, Puxian, X. Y. Liu 21057 (PE); C. peterae var. trichocarpa W. T. Wang: China, Gansu, Wenxian, Z. Y. Zhang 14413 (PE); C. pianmaensis W. T. Wang: China, Guizhou, Libo Exped. 81-6-0012 (PE); C. pinchuanensis W. T. Wang et M. Y. Fang: China, Yunnan, Binchuan Xian, T. N. Liou 017699 (PE); C. pinnata Maxim.: China, Beijing, Baihuashan, S. Y. Ho 15037 (PE); C. pitcheri Torr. et A. Gray: US, Kansas, Norton 1 (GH); C. pogonandra Maxim.: China, Gansu, Wenxian, X. L. Chen and Y. F. Wang 911693 (PE); C. populifolia Turcz.: South America, F. J. Breteler 4666 (US); C. potaninii Maxim.: China, Sichuan, Zhegushan, X. Li 74387 (PE); C. pseudootophora Finet et Gagnep.: China, Hunan, Shimen Xian, Hupingshan Exped. A111 (PE); C. pseudopogonandra Finet et Gagnep.: China, Sichuan, Heishui Xian, X. Li 73058 (PE); C. puberula Hook. et Thoms.: China, Yunnan, Gongshan Xian, Anonym 7067 (PE); C. qingchengshanica W. T. Wang: China, Sichuan, Qingchengshan, T. P. Wang 10009 (PE); C. quinquefoliolata Hutch.: China, Guizhou, Jiangko Xian, Z. S. Zhang et al. 401911 (PE); C. ranunculoides Franch.: China, Yunnan, Lijiang Xian, Anonym 22656 (PE); C. recta L.: Austria, D. Y. Hong s. n. (PE); C. rehderiana Craib.: China, Sichuan, Dajin Xian, X. Li 75591 (PE); C. repens Finet et Gagnep.: China, Sichuan, Honghua Xian, Anonym 1476 (PE); C. reticulata Walter: US, Alabama, Palmer 27234 (GH); C. seemanni Kuntze: US, J. Soukup 3578 (US); C. serratifolia Rehd.: China, Jilin, Antu Xian, T. N. Liou 3785 (PE); C. shensiensis W. T. Wang: China, Shanxi, Xiexian, Yellow River Exped. 344 (PE); C. siamensis Drummond et Craib.: China, Yunnan, China-Russia Exped. s. n. (PE); C. sibirica (L.) Mill.: China, Xinjiang, Xinjiang Exped. 10544 (PE); C. simensis Fresen: Ethiopia, Addis Ababa, F. G. Meyer 7533 (US); C. smilacifolia Wall.: China, Yunnan, Puer Xian, Y. Jiang 12935 (PE); C. songarica Bunge: China, Xinjiang, Wenquan, Xinjiang and Tibet Exped. 3553 (PE); C. songarica var. aspleniifolia (Schrenk) Trautv.: China, Xinjiang, L. Yang 88-085 (PE); C. stanleyi Hook.: Africa, Bayliss 2002 (GH); C. stans Sieb. et Zucc.: Japan, Shizuoka, F. Chikata 15778 (PE); C. subumbellata Kurz.: China, Yunnan, Fengqing Xian, T. T. Yu 18254 (PE); C. tangutica (Maxim.) Korsh.: China, Tibet, Gêrzê Xian, F. Z. Li 23 (PE); C. tangutica var. obtusiuscula Rehd.et Wils.: China, Qinghai, Tibet Exped. 177 (PE); C. tashiroi Maxim.: China, Taiwan, Taibei, W. F. He, 648 (PE); C. tenuipes W. T. Wang: China, Yunnan, C. W. Wang et al. 87086 (PE); C. terniflora DC.: China, Anhui, Xiaoxian, M. Chen and Zhang 19 (PE); C. tomentella (Maxim.) W. T. Wang: China, Shanxi, Yulin Xian, P. Licent 7078 (PE); C. tosaensis Makino: Japan, Miyoshi Furuse 27217 (PE); C. trifida Hook.: Madagascar, Fortyth-Major 714 (US); C. tsaii W. T. Wang: China, Yunnan, B. Y. Qiu 52651 (PE); C. uncinata Champ.: China, Chongqing, Nanchuan Xian, Z. Y. Liu 4519 (PE); C. urophylla Franch.: China, Hubei, Hefeng Xian, H. J. Li 8437 (PE); C. venusta M. C. Chang: China, Yunnan, Yulongshan, SW Exped. 164 (PE); C. versicolor Small: US, Texas, Correll 37401 (GH); C. villosa DC.: Tanzania, Hemit, P. J. Greenway 7741 (US); C. virginiana L.: US, Texas, San Augustine, E. J. Palmer 10622 (MO); C. viridiflora Bert.: Mozambique, Delagoa Bay, H. Junod 370 (US); C. viridis (W. T. Wang et M. C. Chang) W. T. Wang: China, Sichuan, Sêrtar Xian, Lu 06565 (PE); C. viticella L.: Slovenija, Tauno Ulvinen s. n. (UPS); C. wenshanensis W. T. Wang: China, Yunnan, Wenshan Xian, Y. M. Shui 002714 (PE); C. wightiana Wall.: India, Kodaikanal Region, Anglade s. n. (GH); C. williamsii A. Gray ex Perry: Japan, Kyshu Fukuoka, Sadao Tsutsui 29574 (IBSC); C. yuanjiangensis W. T. Wang: China, Yunnan, Yan-shan Lung-tang-tzai-shan, C. W. Wang 83560 (PE); C. yunnanensis Franch.: China, Yunnan, Binchuan Xian, T. N. Liou 017847 (PE); Naravelia laurifolia Wall.: Thailand, Kow Kiee Se Buhn Beung District, J. F. Maxwell 76-691 (PE); N. pilurifera Hance: China, Yunnan, Mengkuan, C. W. Wang 79972 (PE); N. zylanica (L.) DC. China, Anonym s. n. (PE).

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Xie, L., Li, LQ. Variation of pollen morphology, and its implications in the phylogeny of Clematis (Ranunculaceae). Plant Syst Evol 298, 1437–1453 (2012). https://doi.org/10.1007/s00606-012-0648-y

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