A comparison of seed plants’ polyploids between the Qinghai-Tibet Plateau alpine and the Pan-Arctic regions

doi:10.17520/biods.2021146

Abstract

Abstract:

Aims: Polyploidization is an important mechanism for plants to adapt to extreme environments. The Qinghai-Tibet Plateau (QTP) alpine and Pan-Arctic regions have a similar low-temperature environment, and there were closely biotic exchanges between the two regions. However, it is unclear whether the QTP alpine and Pan-Arctic floras have similar polyploid buildup or not. Here, we compared polyploid proportions between these two floras and explored the potential causes for the difference.
Methods: By comprehensive searches in the databases and various literatures, we obtained species lists with chromosome numbers and ploidy of seed plants for the QTP alpine and Pan-Arctic regions, and then calculated polyploid proportion in totality as well as polyploid proportion for different life forms in the two regions.
Results: A total of 1,770 species of seed plants with chromosome numbers were collected, of which 774 occur in the QTP alpine region and 996 occur in the Pan-Arctic. According to the statistical analyses, the proportions of polyploid plants are 20.9% in the QTP alpine region and 61.5% in the Pan-Arctic. The proportions of polyploids of annual herbs, perennial herbs and woody plants in the QTP alpine region are 20.7%, 21.6%, and 12.8%, respectively. The proportions of polyploids of annual herbs, perennial herbs and woody plants in the Pan-Arctic are 60.2%, 65.5%, and 38.3%, respectively.
Conclusions: The polyploid proportions in totality and for different life forms in the Pan-Arctic are higher than those in the QTP alpine region obviously, which is associated with the different evolutionary history of the two floras, as well as their different geological and climatic events. The modernization of the QTP alpine flora took place around the Oligocene-Miocene boundary, and since then the QTP has had a relatively constant low-temperate environment, whereas the Pan-Arctic flora did not develop until 3-4 Ma, and since then the Pan-Arctic flora experienced repeated glacial and interglacial periods and repeated sea-level fluctuations, which might have resulted in the polyploidization of plants. This study contributes to our knowledge on how polyploids adapt to low-temperate environments.

Key words: Qinghai-Tibet Plateau, Pan-Arctic, polyploidization, life form, extreme environments, climate change

Jun Zhang, Huanwen Peng, Fucai Xia, Wei Wang. A comparison of seed plants’ polyploids between the Qinghai-Tibet Plateau alpine and the Pan-Arctic regions[J]. Biodiv Sci, 2021, 29(11): 1470-1480.

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URL: https://www.biodiversity-science.net/EN/10.17520/biods.2021146

https://www.biodiversity-science.net/EN/Y2021/V29/I11/1470

Figures/Tables 3

Fig. 1 Ranges of the Qinghai-Tibet Plateau (QTP) and the Pan-Arctic regions. The range of the QTP refers to Zhang YL et al (2002) and Zhang DC et al (2016); the range of the Pan-Arctic region refers to Elven et al (2011).

Table 1 Statistics of the ploidy and life form of seed plants in the Qinghai-Tibet Plateau (QTP) alpine and Pan-Arctic regions. Percentages indicate polyploid and diploid proportions of different life forms and the total in the two regions.

生活型 Life form	青藏高原高山区物种数 No. of species in the QTP alpine region		泛北极地区物种数 No. of species in the Pan-Arctic region
生活型 Life form	多倍体 Polyploid	二倍体 Diploid	多倍体 Polyploid	二倍体 Diploid
木本植物 Woody plant	6 (12.8%)	41 (87.2%)	49 (38.3%)	79 (61.7%)
草本植物 Herb	156 (21.5%)	571 (78.5%)	564 (65.0%)	304 (35.0%)
一年生草本 Annual herb	18 (20.7%)	69 (79.3%)	53 (60.2%)	35 (39.8%)
多年生草本 Perennial herb	138 (21.6%)	502 (78.4%)	511 (65.5%)	269 (34.5%)
总数 Total	162 (20.9%)	612 (79.1%)	613 (61.5%)	383 (38.5%)

Fig. 2 Possible factors resulting in polyploids in the Qinghai- Tibet Plateau (QTP) alpine and Pan-Arctic (PA) regions. The temperature curve was modified from Westerhold et al (2020). Rises of the QTP alpine and PA floras are based on Ding et al (2020) and Matthews & Ovenden (1990), respectively. The dotted line indicates that the QTP alpine flora started to develop in the early Oligocene, whereas the solid lines indicate the rapid rise of the flora. Pli., Pliocene; Ple., Pleistocene.

References 70

[1]	Bennett MD (2004) Perspectives on polyploidy in plants-Ancient and neo. Biological Journal of the Linnean Society, 82, 411-423. DOI URL
[2]	Botsyun S, Sepulchre P, Donnadieu Y, Risi C, Licht A, Rugenstein JKC (2019) Revised paleoaltimetry data show low Tibetan Plateau elevation during the Eocene. Science, 363, eaaq1436.
[3]	Brochmann C, Brysting AK, Alsos IG, Borgen L, Grundt HH, Scheen AC, Elven R (2004) Polyploidy in arctic plants. Biological Journal of the Linnean Society, 82, 521-536. DOI URL
[4]	Cai LM, Xi ZX, Amorim AM, Sugumaran M, Rest JS, Liu L, Davis CC (2019) Widespread ancient whole-genome duplications in Malpighiales coincide with Eocene global climatic upheaval. New Phytologist, 221, 565-576. DOI URL
[5]	Chen TY, Lou AR (2019) Phylogeography and paleodistribution models of a widespread birch (Betula platyphylla Suk.) across East Asia: Multiple refugia, multidirectional expansion, and heterogeneous genetic pattern. Ecology and Evolution, 9, 7792-7807. DOI URL
[6]	Comes HP, Kadereit JW (2003) Spatial and temporal patterns in the evolution of the flora of the European Alpine System. Taxon, 52, 451-462. DOI URL
[7]	Compagnoni A, Levin S, Childs DZ, Harpole S, Paniw M, Römer G, Burns JH, Che-Castaldo J, Rüger N, Kunstler G, Bennett JM, Archer CR, Jones OR, Salguero-Gómez R, Knight TM (2021) Herbaceous perennial plants with short generation time have stronger responses to climate anomalies than those with longer generation time. Nature Communications, 12, 1824. DOI PMID
[8]	De Storme N, Geelen D (2014) The impact of environmental stress on male reproductive development in plants: Biological processes and molecular mechanisms. Plant, Cell & Environment, 37, 1-18.
[9]	Deng T, Wu FX, Wang SQ, Su T, Zhou ZK (2019) Significant shift in the terrestrial ecosystem at the Paleogene/Neogene boundary in the Tibetan Plateau. Chinese Science Bulletin, 64, 2894-2906. (in Chinese with English abstract)
	[ 邓涛, 吴飞翔, 王世骐, 苏涛, 周浙昆 (2019) 古近纪/新近纪之交青藏高原陆地生态系统的重大转折. 科学通报, 64, 2894-2906.]
[10]	Despres L, Loriot S, Gaudeul M (2002) Geographic pattern of genetic variation in the European globeflower Trollius europaeus L. (Ranunculaceae) inferred from amplified fragment length polymorphism markers. Molecular Ecology, 11, 2337-2347. DOI URL
[11]	Ding L, Spicer RA, Yang J, Xu Q, Cai F, Li S, Lai Q, Wang H, Spicer TEV, Yue Y, Shukla A, Srivastava G, Khan MA, Bera S, Mehrotra R (2017) Quantifying the rise of the Himalaya orogen and implications for the South Asian monsoon. Geology, 45, 215-218. DOI URL
[12]	Ding WN, Ree RH, Spicer RA, Xing YW (2020) Ancient orogenic and monsoon-driven assembly of the world’s richest temperate alpine flora. Science, 369, 578-581. DOI URL
[13]	Drummond CS, Eastwood RJ, Miotto STS, Hughes CE (2012) Multiple continental radiations and correlates of diversification in Lupinus (Leguminosae): Testing for key innovation with incomplete taxon sampling. Systematic Biology, 61, 443-460. DOI URL
[14]	Ebersbach J, Muellner-Riehl AN, Michalak I, Tkach N, Hoffmann MH, Röser M, Sun H, Favre A (2017) In and out of the Qinghai-Tibet Plateau: Divergence time estimation and historical biogeography of the large arctic-alpine genus Saxifraga L. Journal of Biogeography, 44, 900-910. DOI URL
[15]	Elven R, Murray DF, Razzhivin VY, Yurtsev BA (2011) Annotated Checklist of the Panarctic Flora (PAF), Vascular Plants. http://Panarcticflora.org/. (accessed on 2020-10-20)
[16]	Fang XM, Dupont-Nivet G, Wang CS, Song CH, Meng QQ, Zhang WL, Nie JS, Zhang T, Mao ZQ, Chen Y (2020) Revised chronology of central Tibet uplift (Lunpola Basin). Science Advances, 6, eaba7298.
[17]	Farnsworth A, Lunt DJ, Robinson SA, Valdes PJ, Roberts WHG, Clift PD, Markwick P, Su T, Wrobel N, Bragg F, Kelland SJ, Pancost RD (2019) Past East Asian monsoon evolution controlled by paleogeography, not CO₂. Science Advances, 5, eaax1697.
[18]	Favre A, Michalak I, Chen CH, Wang JC, Pringle JS, Matuszak S, Sun H, Yuan YM, Struwe L, Muellner-Riehl AN (2016) Out-of-Tibet: The spatio-temporal evolution of Gentiana (Gentianaceae). Journal of Biogeography, 43, 1967-1978. DOI URL
[19]	Gamberg M (2020) Threats to arctic ecosystems. In: Encyclopedia of the World’s Biomes (eds Goldstein MI, DellaSala DA), pp. 532-538. Elsevier, Oxford.
[20]	Gao QZ, Guo YQ, Xu HM, Ganjurjav H, Li Y, Wan YF, Qin XB, Ma X, Liu S (2016) Climate change and its impacts on vegetation distribution and net primary productivity of the alpine ecosystem in the Qinghai-Tibetan Plateau. Science of the Total Environment, 554/555, 34-41.
[21]	Goldblatt P (1980) Polyploidy in angiosperms:Monocotyledons. In: Polyploidy: Biological Relevance (ed. Lewis WH), pp. 219-239. Springer, New York.
[22]	Grant JK, De DC, Biochimie SBD (1963) Methods of Separation of Subcellular Structural Components. Cambridge University Press, Cambridge.
[23]	Hoffmann MH, von Hagen KB, Hörandl E, Röser M, Tkach NV (2010) Sources of the arctic flora: Origins of arctic species in Ranunculus and related genera. International Journal of Plant Sciences, 171, 90-106. DOI URL
[24]	Hou Y, Nowak MD, Mirré V, Bjorå CS, Brochmann C, Popp M (2016) RAD-seq data point to a northern origin of the arctic-alpine genus Cassiope (Ericaceae). Molecular Phylogenetics and Evolution, 95, 152-160. DOI URL
[25]	Khatoon S, Ali SI (1993) Chromosome Atlas of the Angiosperms of Pakistan. BCC & T Press, Karachi.
[26]	Körner C (2003) The alpine life zone. In:Alpine Plant Life: Functional Plant Ecology of High Mountain Ecosystems (ed.ed. Körner C), pp. 9-20. Springer-Verlag, New York.
[27]	Lasabuda APE, Johansen NS, Laberg JS, Faleide JI, Senger K, Rydningen TA, Patton H, Knutsen S-M, Hanssen A (2021) Cenozoic uplift and erosion of the Norwegian Barents Shelf -A review. Earth-Science Reviews, 217, 103609. DOI URL
[28]	Levin DA (2002) The Role of Chromosomal Change in Plant Evolution (Oxford Series in Ecology and Evolution). Oxford University Press, New York.
[29]	Li GD, Kim C, Zha HG, Zhou Z, Nie ZL, Sun H (2014) Molecular phylogeny and biogeography of the arctic-alpine genus Lagotis (Plantaginaceae). Taxon, 63, 103-115. DOI URL
[30]	Li SF, Valdes PJ, Farnsworth A, Davies-Barnard T, Su T, Lunt DJ, Spicer RA, Liu J, Deng WYD, Huang J, Tang H, Ridgwell A, Chen LL, Zhou ZK (2021) Orographic evolution of northern Tibet shaped vegetation and plant diversity in eastern Asia. Science Advances, 7, eabc7741.
[31]	Liu XD, Chen BD (2000) Climatic warming in the Tibetan Plateau during recent decades. International Journal of Climatology, 20, 1729-1742. DOI URL
[32]	Ma PF, Wang LC, Wang CS, Wu XH, Wei YS (2015) Organic-matter accumulation of the lacustrine Lunpola oil shale, central Tibetan Plateau: Controlled by the paleoclimate, provenance, and drainage system. International Journal of Coal Geology, 147/148, 58-70.
[33]	Masterson J (1994) Stomatal size in fossil plants: Evidence for polyploidy in majority of angiosperms. Science, 264, 421- 424. PMID
[34]	Matthews JV, Ovenden LE (1990) Late Tertiary plant macrofossils from localities in arctic/subarctic North America: A review of the data. ARCTIC, 43, 364-392.
[35]	Michl T, Huck S, Schmitt T, Liebrich A, Haase P, Büdel B (2010) The molecular population structure of the tall forb Cicerbita alpina (Asteraceae) supports the idea of cryptic glacial refugia in central Europe. Botanical Journal of the Linnean Society, 164,142-154. DOI URL
[36]	Miller KG, Kominz MA, Browning JV, Wright JD, Mountain GS, Katz ME, Sugarman PJ, Cramer BS, Christie-Blick N, Pekar SF (2005) The Phanerozoic record of global sea-level change. Science, 310, 1293-1298. DOI URL
[37]	Murray DF (1995) Causes of arctic plant diversity:Origin and evolution. In: Arctic and Alpine Biodiversity: Patterns, Causes and Ecosystem Consequences (eds Chapin FS, Korner C), pp. 21-32. Springer, Heidelberg, Germany.
[38]	Myers-Smith IH, Elmendorf SC, Beck PSA, Wilmking M, Hallinger M, Blok D, Tape KD, Rayback SA, Macias-Fauria M, Forbes BC (2015) Climate sensitivity of shrub growth across the tundra biome. Nature Climate Change, 5, 887-891. DOI
[39]	Nie ZL, Wen J, Gu ZJ, Boufford DE, Sun H (2005) Polyploidy in the flora of the Hengduan Mountains hotspot, Southwestern China. Annals of the Missouri Botanical Garden, 92, 275- 306.
[40]	Pan BT, Gao HS, Li BY, Li JJ (2004) Step-like landforms and uplift of the Qinghai-Xizang Plateau. Quaternary Sciences, 24, 50-57, 133. (in Chinese with English abstract)
	[ 潘保田, 高红山, 李炳元, 李吉均 (2004) 青藏高原层状地貌与高原隆升. 第四纪研究, 24, 50-57, 133.]
[41]	Rice A, Šmarda P, Novosolov M, Drori M, Glick L, Sabath N, Meiri S, Belmaker J, Mayrose I (2019) The global biogeography of polyploid plants. Nature Ecology & Evolution, 3, 265-273.
[42]	Roquet C, Boucher FC, Thuiller W, Lavergne S (2013) Replicated radiations of the alpine genus Androsace (Primulaceae) driven by range expansion and convergent key innovations. Journal of Biogeography, 40, 1874-1886. DOI URL
[43]	Serreze MC, Barry RG (2011) Processes and impacts of Arctic amplification: A research synthesis. Global and Planetary Change, 77, 85-96. DOI URL
[44]	Shi Z, Bai DZ, Lei JP, Li MH, Xiao WF (2011) Advance on physioecological adaptation of alpine plants to mountainous environment. Acta Botanica Boreali-Occidentalia Sinica, 31, 1711-1718. (in Chinese with English abstract)
	[ 施征, 白登忠, 雷静品, 李迈和, 肖文发 (2011) 高山植物对其环境的生理生态适应性研究进展. 西北植物学报, 31, 1711- 1718.]
[45]	Souto CP, Kitzberger T, Arbetman MP, Premoli AC (2015) How do cold-sensitive species endure ice ages? Phylogeographic and paleodistribution models of postglacial range expansion of the mesothermic drought-tolerant conifer Austrocedrus chilensis. New Phytologist, 208, 960-972. DOI URL
[46]	Spicer RA, Su T, Valdes PJ, Farnsworth A, Wu FX, Shi GL, Spicer TEV, Zhou ZK (2021) Why ‘the uplift of the Tibetan Plateau’ is a myth. National Science Review, 8, nwaa091.
[47]	Stebbins GL (1938) Cytological characteristics associated with the different growth habits in the dicotyledons. American Journal of Botany, 25, 189-198. DOI URL
[48]	Stebbins GL (1950) Variation and Evolution in Plants. Columbia University Press, New York.
[49]	Stebbins GL (1984) Polyploidy and the distribution of the arctic-alpine flora: New evidence and a new approach. Botanica Helvetica, 94, 1-13.
[50]	Su T, Farnsworth A, Spicer RA, Huang J, Wu FX, Liu J, Li SF, Xing YW, Huang YJ, Deng WYD, Tang H, Xu CL, Zhao F, Srivastava G, Valdes PJ, Deng T, Zhou ZK (2019) No high Tibetan Plateau until the Neogene. Science Advances, 5, eaav2189.
[51]	Su T, Spicer RA, Li SH, Xu H, Huang J, Sherlock S, Huang YJ, Li SF, Wang L, Jia LB, Deng WYD, Liu J, Deng CL, Zhang ST, Valdes PJ, Zhou ZK (2019) Uplift, climate and biotic changes at the Eocene-Oligocene transition in south-eastern Tibet. National Science Review, 6, 495-504. DOI URL
[52]	Sun JM, Xu QH, Liu WM, Zhang ZQ, Xue L, Zhao P (2014) Palynological evidence for the latest Oligocene-Early Miocene paleoelevation estimate in the Lunpola Basin, central Tibet. Palaeogeography, Palaeoclimatology, Palaeoecology, 399, 21-30. DOI URL
[53]	Sun YS, Wang AL, Wan DS, Wang Q, Liu JQ (2012) Rapid radiation of Rheum (Polygonaceae) and parallel evolution of morphological traits. Molecular Phylogenetics and Evolution, 63, 150-158. DOI URL
[54]	Tkach NV, Hoffmann MH, Röser M, von Hagen KB (2008) Temporal patterns of evolution in the Arctic explored in Artemisia L. (Asteraceae) lineages of different age. Plant Ecology & Diversity, 1, 161-169.
[55]	Tsuneo F, Katsuhiko K, Hong DY, Zhou SL, Takuko S (1998) A karyomorphological comparison of four Saxifraga species collected in the western part of Sichuan Province, China. Chromosome Science, 2, 103-109.
[56]	Van de Peer Y, Ashman TL, Soltis PS, Soltis DE (2021) Polyploidy: An evolutionary and ecological force in stressful times. The Plant Cell, 33, 11-26. DOI URL
[57]	Wang EQ (2013) Evolution of the Tibetan Plateau: As constrained by major tectonic-thermo events and a discussion on their origin. Chinese Journal of Geology, 48, 334-353. (in Chinese with English abstract)
	[ 王二七 (2013) 青藏高原大地构造演化--主要构造-热事件的制约及其成因探讨. 地质科学, 48, 334-353.]
[58]	Wang JJ, Peng ZB, Sun H, Nie ZL, Meng Y (2017) Cytogeographic patterns of angiosperms flora of the Qinghai- Tibet Plateau and Hengduan Mountains. Biodiversity Science, 25, 218-225. (in Chinese with English abstract)
	[ 王家坚, 彭智邦, 孙航, 聂泽龙, 孟盈 (2017) 青藏高原与横断山被子植物区系演化的细胞地理学特征. 生物多样性, 25, 218-225.] DOI
[59]	Wang Q, Liu JQ, Allen GA, Ma YZ, Yue W, Marr KL, Abbott RJ (2016) Arctic plant origins and early formation of circumarctic distributions: A case study of the mountain sorrel, Oxyria digyna. New Phytologist, 209, 343-353. DOI URL
[60]	Wang YF, Sylvester SP, Lu XM, Dawadi B, Sigdel SR, Liang EY, Julio Camarero J (2019) The stability of spruce treelines on the eastern Tibetan Plateau over the last century is explained by pastoral disturbance. Forest Ecology and Management, 442, 34-45. DOI URL
[61]	Wen J, Zhang JQ, Nie ZL, Zhong Y, Sun H (2014) Evolutionary diversifications of plants on the Qinghai- Tibetan Plateau. Frontiers in Genetics, 5, 4.
[62]	Westerhold T, Marwan N, Drury AJ, Liebrand D, Agnini C, Anagnostou E, Barnet JSK, Bohaty SM, De Vleeschouwer D, Florindo F, Frederichs T, Hodell DA, Holbourn AE, Kroon D, Lauretano V, Littler K, Lourens LJ, Lyle M, Pälike H, Röhl U, Tian J, Wilkens RH, Wilson PA, Zachos JC (2020) An astronomically dated record of Earth’s climate and its predictability over the last 66 million years. Science, 369, 1383-1387. DOI PMID
[63]	Woodruff DS, Turner LM (2009) The Indochinese-Sundaic zoogeographic transition: A description and analysis of terrestrial mammal species distributions. Journal of Biogeography, 36, 803-821. DOI URL
[64]	Wu SD, Han BC, Jiao YN (2020) Genetic contribution of paleopolyploidy to adaptive evolution in angiosperms. Molecular Plant, 13, 59-71. DOI URL
[65]	Yang Y, Sun H (2006) Advances in the functional ecology of alpine and arctic plants. Acta Botanica Yunnanica, 28, 43-53. (in Chinese with English abstract)
	[ 杨扬, 孙航 (2006) 高山和极地植物功能生态学研究进展. 云南植物研究, 28, 43-53.]
[66]	Yuan J, Yang ZY, Deng CL, Krijgsman W, Hu XM, Li SH, Shen ZS, Qin HF, An W, He HY, Ding L, Guo ZT, Zhu RX (2021) Rapid drift of the Tethyan Himalaya terrane before two-stage India-Asia collision. National Science Review, 8, nwaa173.
[67]	Zenil-Ferguson R, Ponciano JM, Burleigh JG (2017) Testing the association of phenotypes with polyploidy: An example using herbaceous and woody eudicots. Evolution, 71, 1138- 1148. DOI PMID
[68]	Zhang DC, Ye JX, Sun H (2016) Quantitative approaches to identify floristic units and centres of species endemism in the Qinghai-Tibetan Plateau, south-western China. Journal of Biogeography, 43, 2465-2476. DOI URL
[69]	Zhang JQ, Meng SY, Allen GA, Wen J, Rao GY (2014) Rapid radiation and dispersal out of the Qinghai-Tibetan Plateau of an alpine plant lineage Rhodiola (Crassulaceae). Molecular Phylogenetics and Evolution, 77, 147-158. DOI URL
[70]	Zhang YL, Li BY, Zheng D (2002) A discussion on the boundary and area of the Tibetan Plateau in China. Geographical Research, 21, 1-8. (in Chinese with English abstract)
	[ 张镱锂, 李炳元, 郑度 (2002) 论青藏高原范围与面积. 地理研究, 21, 1-8.]