Research Paper

Ecological factors correlate with genome size variation of Acanthocalyx (Caprifoliaceae) in the Hengduan-Himalaya Mountains

Nan Wang, Chih‑Chieh Yu, Yan-Xia Jia, Yao-Wu Xing

Published on: 22 April 2024

Page: 142 - 150

DOI: 10.6165/tai.2024.69.142

Abstract

While the genome sizes of flowering plants vary c. 2400-fold, it remains little known what factors may have driven the variation. In this study, we investigated the spatial pattern of the genome size of 54 populations of Acanthocalyx, which is found in the Hengduan-Himalaya Mountains. Our results showed that the red-flowered lineage of Acanthocalyx had significantly larger genomes (ranging from 1.9 to 2.5 Gb) compared to the white-flowered lineage, which had an average genome size of 1.27 Gb. This difference in genome size can be attributed to particular environmental factors. Within the red-flowered lineage, the genome size was positively correlated with soil nitrogen content and mean diurnal range. On the other hand, the genome size of the white-flowered lineage, Acanthocalyx alba was negatively correlated with latitude which aligns with the population dynamics of this species during the Pleistocene. Overall, our findings highlight the influence of abiotic factors and geography in regulating the genome size of Acanthocalyx species. This study contributes to our understanding of the evolution of alpine plants in the Hengduan-Himalaya Mountains.

Keyword: Acanthocalyx alba, Acanthocalyx delavayi, Acanthocalyx nepalensis, flow cytometry, Pleistocene, speciation

Literature Cited

Basak, S., Wang, G., Sun, X., Yang, Y. 2018 Variations in genome size of Turnip Landraces from two high-altitude environments. J. Am. Soc. Hortic. Sci. 143(2): 136?143.
DOI: 10.21273/JASHS04326-18View Article Google Scholar

Bennett, M.D. 1972 Nuclear DNA content and minimum generation time in herbaceous plants. Proc R Soc Lond B 181(1063): 109?135.
DOI: 10.1098/rspb.1972.0042View Article Google Scholar

Bennett, M.D. 1976 DNA amount, latitude, and crop plant distribution. Environ. Exp. Bot. 16(2-3): 93?108.
DOI: 10.1016/0098-8472(76)90001-0View Article Google Scholar

Bennett, M.D., Smith, J.B. 1976 Nuclear DNA amounts in angiosperms. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 274(933): 227?274.
DOI: 10.1098/rstb.1976.0044View Article Google Scholar

Blackmore, S., Cannon, M.J. 1983 Palynology and systematics of Morinaceae. Rev. Palaeobot. Palynol. 40(3): 207?226.
DOI: 10.1016/0034-6667(83)90037-4View Article Google Scholar

Brown, J.L., Carnaval, A.C. 2019 A tale of two niches: methods, concepts, and evolution. Front. Biogeogr. 11(4): e44158
DOI: 10.21425/F5FBG44158View Article Google Scholar

Bunge, A.v. 1852. Beitrag zur Kenntniss der Flor Russlands und der steppen Central-Asiens. St Petersburg, pp 321?323.
DOI: 10.5962/bhl.title.51048View Article

Bures, P., Wang, Y.F., Horova, L., Suda, J. 2004 Genome size variation in central European species of Cirsium (Compositae) and their natural hybrids. Ann. Bot. 94(3): 353?363.
DOI: 10.1093/aob/mch151View Article Google Scholar

Cannon, M.J., Cannon, J.F.M. 1984 A revision of the Morinaceae (Magnoliophyta – Dipsacales). Bull. Br. Mus. Botany 12(1): 1–15.

Chen, G., Sun, W.-B., Sun, H. 2007 Ploidy variation in Buddleja L. (Buddlejaceae) in the Sino-Himalayan region and its biogeographical implications. Bot. J. Linn. Soc. 154(3): 305?312.
DOI: 10.1111/j.1095-8339.2007.00650.xView Article Google Scholar

Chuckran, P.F., Flagg, C., Propster, J., Rutherford, W.A., Sieradzki, E., Blazewicz, S.J., Hungate, B., Pett-Ridge, J., Schwartz, E., Dijkstra, P. 2023 Edaphic controls on genome size and GC content of bacteria in soil microbial communities. Soil Biol. Biochem. 178: 108935.
DOI: 10.1016/j.soilbio.2022.108935View Article Google Scholar

Ding, W.-N., Ree, R., Spicer, R., Xing, Y. 2020 Ancient orogenic and monsoon-driven assembly of the world’s richest temperate alpine flora. Science 369(6503): 578?581.
DOI: 10.1126/science.abb4484View Article Google Scholar

Dodsworth, S., Leitch, A. R., Leitch, I. J. 2015 Genome size diversity in angiosperms and its influence on gene space. Curr. Opin. Genet. Dev. 35: 73?78.
DOI: 10.1016/j.gde.2015.10.006View Article Google Scholar

Dole?el, J., ??hal?kov?, J., and Lucretti, S. 1992 A high-yield procedure for isolation of metaphase chromosomes from root tips of Vicia faba L. Planta. 188(1): 93?98.
DOI: 10.1007/BF00198944View Article Google Scholar

Dole?el, J., Greilhuber, J., Suda, J. 2007 Estimation of nuclear DNA content in plants using flow cytometry. Nat. Protoc. 2(9): 2233?2244.
DOI: 10.1038/nprot.2007.310View Article Google Scholar

Du, Y.P., Bi, Y., Zhang, M.F., Yang, F.P., Jia, G. X., Zhang, X.H. 2017 Genome size diversity in Lilium (Liliaceae) is correlated with karyotype and environmental Traits. Front. Plant Sci. 8: 1303.
DOI: 10.3389/fpls.2017.01303View Article Google Scholar

Fick, S.E., Hijmans, R.J. 2017 WorldClim 2: new 1?km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37(12): 4302?4315.
DOI: 10.1002/joc.5086View Article Google Scholar

Galbraith, D.W., Harkins, K.R., Maddox, J.M., Ayres, N. M., Sharma, D.P., Firoozabady, E. 1983 Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220(4601): 1049?1051.
DOI: 10.1126/science.220.4601.1049View Article Google Scholar

Giovannoni, S.J., Cameron Thrash, J., Temperton, B. 2014 Implications of streamlining theory for microbial ecology. ISME J, 8(8): 1553?1565.
DOI: 10.1038/ismej.2014.60View Article Google Scholar

Grotkopp, E., Rejmanek, M., Sanderson, M.J., Rost, T.L. 2004 Evolution of genome size in pines (Pinus) and its life-history correlates: supertree analyses. Evolution, 58(8): 1705?1729.
DOI: 10.1554/03-545View Article Google Scholar

Guignard, M.S., Nichols R.A., Knell R.J., Macdonald A., Romila C.-A., Trimmer M., Leitch I.J. Leitch A.R. 2016 Genome size and ploidy influence angiosperm species' biomass under nitrogen and phosphorus limitation. New Phytol. 210(4): 1195?1206.
DOI: 10.1111/nph.13881View Article Google Scholar

Han, T.S., Zheng, Q.J., Onstein, R.E., Rojas-Andres, B.M., Hauenschild, F., Muellner-Riehl, A.N., Xing, Y.W. 2020 Polyploidy promotes species diversification of Allium through ecological shifts. New Phytol. 225(1): 571?583.
DOI: 10.1111/nph.16098View Article Google Scholar

Hutang, G.R., Tong, Y., Zhu, X.G., Gao, L.Z. 2023 Genome size variation and polyploidy prevalence in the genus Eragrostis are associated with the global dispersal in arid area. Front Plant Sci. 14: 1066925.
DOI: 10.3389/fpls.2023.1066925View Article Google Scholar

Knight, C.A., Molinari, N.A., Petrov, D.A. 2005 The large genome constraint hypothesis: evolution, ecology and phenotype. Ann. Bot. 95(1): 177?190.
DOI: 10.1093/aob/mci011View Article Google Scholar

Laurie, D.A., Bennett, M.D. 1985 Nuclear DNA content in the genera Zea and Sorghum. Intergeneric, interspecific and intraspecific variation. Heredity. 55(3): 307?313.
DOI: 10.1038/hdy.1985.112View Article Google Scholar

Leitch, I.J., Chase, M. W., and Bennett, M.D. J.A.o.b. 1998 Phylogenetic analysis of DNA C-values provides evidence for a small ancestral genome size in flowering plants. Ann. Bot. 82: 85–94.
DOI: 10.1006/anbo.1998.0783View Article Google Scholar

Leong-Skornickova, J., Sida, O., Jarolimova, V., Sabu, M., Fer, T., Travnicek, P., Suda, J. 2007 Chromosome numbers and genome size variation in Indian species of Curcuma (Zingiberaceae). Ann. Bot. 100(3): 505?526.
DOI: 10.1093/aob/mcm144View Article Google Scholar

Li, X.-H., Zhu, X.-X., Niu, Y., Sun, H. 2014 Phylogenetic clustering and overdispersion for alpine plants along elevational gradient in the Hengduan Mountains Region, southwest China. J. Syst. Evol. 52(3): 280?288.
DOI: 10.1111/jse.12027View Article Google Scholar

Liu, F., Wu, H., Zhao, Y., Li, D., Yang, J.L., Song, X., Shi, Z., Zhu, A.X., Zhang, G.L. 2022 Mapping high resolution National Soil Information Grids of China. Sci. Bull. 67(3): 328?340.
DOI: 10.1016/j.scib.2021.10.013View Article Google Scholar

Loureiro, J., Castro, M., Cerca de Oliveira, J., Mota, L., Torices, R. 2013 Genome size variation and polyploidy incidence in the alpine flora from Spain. Anales Jard. Bot. Madrid. 70(1): 39?47.
DOI: 10.3989/ajbm.2350View Article Google Scholar

Meng, Y., Yang, Y.-P., Sun, H., Deng, T., Nie, Z.-L. 2014 Chromosome numbers, karyotypes, and polyploidy evolution of Anaphalis species (Asteraceae: Gnaphalieae) from the Hengduan Mountains, SW China. Caryologia 67(3): 238?249.
DOI: 10.1080/0144235X.2014.974352View Article Google Scholar

Mu, Q.-Y., Yu, C.-C., Wang, Y., Han, T.-S., Wang, H., Ding, W.-N., Zhang, Q.-Y., Low, S. L., Zheng, Q.-J., Peng, C., Hu, Z.-Y., Xing, Y.-W. 2021 Comparative phylogeography of Acanthocalyx (Caprifoliaceae) reveals distinct genetic structures in the Himalaya-Hengduan Mountains. Alp. Bot. 132(1): 153?168.
DOI: 10.1007/s00035-021-00262-xView Article Google Scholar

Mu, Q.-Y., Yu, C.-C., Xing, Y.-W. 2020 Notes on the type specimen of Acanthocalyx delavayi (Caprifoliaceae) at Herbarium of the National Museum of Natural History in Paris (P). Phytotaxa 451: 90–92.
DOI: 10.11646/phytotaxa.451.1.8View Article Google Scholar

Pellicer, J., Hidalgo, O., Dodsworth, S., Leitch, I.J. 2018 Genome size diversity and its impact on the evolution of land plants. Genes (Basel) 9(2): 88
DOI: 10.3390/genes9020088View Article Google Scholar

Pellicer, J., Leitch, I.J. 2020 The Plant DNA C-values database (release 7.1): an updated online repository of plant genome size data for comparative studies. New Phytol. 226(2): 301?305.
DOI: 10.1111/nph.16261View Article Google Scholar

Puttick, M.N., Clark, J., Donoghue, P.C. 2015 Size is not everything: rates of genome size evolution, not C-value, correlate with speciation in angiosperms. Proc. Royal Soc. B Biol Sci. 282(1820): 20152289.
DOI: 10.1098/rspb.2015.2289View Article Google Scholar

Qiu, F., Baack, E.J., Whitney, K. D., Bock, D.G., Tetreault, H.M., Rieseberg, L.H., Ungerer, M.C. 2019 Phylogenetic trends and environmental correlates of nuclear genome size variation in Helianthus sunflowers. New Phytol. 221(3): 1609?1618.
DOI: 10.1111/nph.15465View Article Google Scholar

R Core Team (Version 2.6-6) 2018 Retrieved from https://cran.r-project.org/package=RASTER

Reeves, G., Francis, D., Davies, M.S., Rogers, H.J., Hodkinson, T.R. 1998 Genome size is negatively correlated with altitude in natural populations of Dactylis glomerata. Ann. Bot. 82(suppl_1): 99?105.
DOI: 10.1006/anbo.1998.0751View Article Google Scholar

Rieseberg, L.H. 2001 Chromosomal rearrangements and speciation. Trends Ecol. Evol. 16(7): 351?358.
DOI: 10.1016/S0169-5347(01)02187-5View Article Google Scholar

Sedel’nikova, T.S. 2016 Variability of genome size in conifers under extreme environmental conditions. Biol. Bull. 6(2): 177?188.
DOI: 10.1134/S2079086416020079View Article Google Scholar

Terlevic, A., Bogdanovic, S., Frajman, B., Resetnik, I. 2022 Genome size variation in Dianthus sylvestris Wulfen sensu lato (Caryophyllaceae). Plants 11(11): 1481.
DOI: 10.3390/plants11111481View Article Google Scholar

Tito, C.M., Poggio, L., and Naranjo, C.A. 1991 Cytogenetic studies in the genus Zea: 3. DNA content and heterochromatin in species and hybrids. Theor. Appl. Genet. 83(1): 58?64.
DOI: 10.1007/BF00229226View Article Google Scholar

Waters, C., Murray, B.G., Melville, G., Coates, D., Young, A., Virgona, J. 2010. Polyploidy and possible implications for the evolutionary history of some Australian Danthonieae. Aust. J. Bot. 58(1): 23?34.
DOI: 10.1071/BT09138View Article Google Scholar

WFO 2023 Morina longifolia Wall. ex DC. In: World Flora Online. Retrieved from http://www.worldfloraonline.org/taxon/wfo-0001046451

Wu, Z.-Y. 1988. Hengduan mountain flora and her significance. J. Jap. Bot. 63(9): 297?311.

Yang, Q.-E., Landrein, S. 2011 Caprifoliaceae In: Wu Z, Hong D, Raven PH (eds.) Flora of China, vol 19 Beijing and St. Louis: Science Press and Missouri Botanical Garden Press.