Genome size evolution of the extant lycophytes and ferns

doi:10.1016/j.pld.2021.11.007

Plant Diversity ›› 2022, Vol. 44 ›› Issue (02): 141-152.DOI: 10.1016/j.pld.2021.11.007

• Articles • Previous Articles Next Articles

Genome size evolution of the extant lycophytes and ferns

Fa-Guo Wang^a, Ai-Hua Wang^a,d, Cheng-Ke Bai^b, Dong-Mei Jin^c, Li-Yun Nie^a, AJ Harris^a,e, Le Che^b, Juan-Juan Wang^b, Shi-Yu Li^a, Lei Xu^a, Hui Shen^c, Yu-Feng Gu^c,g,h, Hui Shang^c, Lei Duan^a, Xian-Chun Zhang^f, Hong-Feng Chen^a, Yue-Hong Yan^c,g

a Key Laboratory of Plant Resources Conservation and Sustainable Utilization, Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, 510650, China;
b College of Life Sciences, Shaanxi Normal University, Xi'an, 710062, China;
c Eastern China Conservation Centre for Wild Endangered Plant Resources, Shanghai Chenshan Botanical Garden, Shanghai, 201602, China;
d Key Laboratory of Environment Change and Resources Use in Beibu Gulf, Ministry of Education, Nanning Normal University, Nanning, 530001, China;
e Department of Biology, Oberlin College, Oberlin, OH, 44074, USA;
f State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China;
g Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, the National Orchid Conservation Center of China and the Orchid Conservation & Research Center of Shenzhen, 518114, Shenzhen, China;
h Life Science and Technology College, Harbin Normal University, Harbin, 150025, China

Received:2021-04-11 Revised:2021-11-24 Online:2022-04-25 Published:2022-04-24
Contact: Hong-Feng Chen,E-mail:h.f.chen@scbg.ac.cn;Yue-Hong Yan,E-mail:yhyan@sibs.ac.cn
Supported by:
We thank Yu-Wen Cui for his assistance with data collection and analyses in R. This research was supported by the National Natural Science Foundation of China (grant number 31870188, 31800174, 31700172, 41571056) to Wang, Shen, Wang and Xing, Shanghai Landscaping and City Appearance Administrative Bureau of China, Scientific Research Grants (G182411) to Yan, the Strategic Priority Research Program of the Chinese Academy of Sciences (grant number XDA13020603, XDA13020500) to Chen and Jian, Guangdong Natural Science Foundation (grant number 2015A030308015) to Wang.

Abstract

Abstract: Ferns and lycophytes have remarkably large genomes. However, little is known about how their genome size evolved in fern lineages. To explore the origins and evolution of chromosome numbers and genome size in ferns, we used flow cytometry to measure the genomes of 240 species (255 samples) of extant ferns and lycophytes comprising 27 families and 72 genera, of which 228 species (242 samples) represent new reports. We analyzed correlations among genome size, spore size, chromosomal features, phylogeny, and habitat type preference within a phylogenetic framework. We also applied ANOVA and multinomial logistic regression analysis to preference of habitat type and genome size. Using the phylogeny, we conducted ancestral character reconstruction for habitat types and tested whether genome size changes simultaneously with shifts in habitat preference. We found that 2C values had weak phylogenetic signal, whereas the base number of chromosomes (x) had a strong phylogenetic signal. Furthermore, our analyses revealed a positive correlation between genome size and chromosome traits, indicating that the base number of chromosomes (x), chromosome size, and polyploidization may be primary contributors to genome expansion in ferns and lycophytes. Genome sizes in different habitat types varied significantly and were significantly correlated with habitat types; specifically, multinomial logistic regression indicated that species with larger 2C values were more likely to be epiphytes. Terrestrial habitat is inferred to be ancestral for both extant ferns and lycophytes, whereas transitions to other habitat types occurred as the major clades emerged. Shifts in habitat types appear be followed by periods of genomic stability. Based on these results, we inferred that habitat type changes and multiple whole-genome duplications have contributed to the formation of large genomes of ferns and their allies during their evolutionary history.

Key words: Genome size, Ferns, Chromosome numbers, Habitat type, Whole-genome duplications, Evolution

Fa-Guo Wang, Ai-Hua Wang, Cheng-Ke Bai, Dong-Mei Jin, Li-Yun Nie, AJ Harris, Le Che, Juan-Juan Wang, Shi-Yu Li, Lei Xu, Hui Shen, Yu-Feng Gu, Hui Shang, Lei Duan, Xian-Chun Zhang, Hong-Feng Chen, Yue-Hong Yan. Genome size evolution of the extant lycophytes and ferns[J]. Plant Diversity, 2022, 44(02): 141-152.

References

Bai, C.K., Alverson, W.S., Follansbee, A., et al., 2012. New reports of nuclear DNA content for 407 vascular plant taxa from the United States. Ann. Bot. 110, 1623-1629.
Baniaga, A.E., Barker, M.S., 2019. Nuclear genome size is positively correlated with median LTR-RT insertion time in fern and lycophyte genomes. Am. Fern J. 109, 248-266.
Baniaga, A.E., Arrigo, N., Barker, M.S., 2016. The small nuclear genomes of Selaginella are associated with a low rate of genome size evolution. Genome Biol. Evol. 8, 1516-1525.
Banks, J.A., Nishiyama, T., Hasebe, M., et al., 2011. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332, 960-963.
Barker, M.S., Wolf, P.G., 2010. Unfurling fern biology in the genomics age. Bioscience 60, 177-185.
Barrington, D.S., Paris, C.A., Ranker, T.A., 1986. Systematic inferences from spore and stomate size in the ferns. Am. Fern J. 76, 149-159.
Beck, J.B., Windham, M.D., Yatskievych, G., et al., 2010. A diploids-first approach to species delimitation and interpreting polyploid evolution in the fern genus Astrolepis (Pteridaceae). Syst. Bot. 35, 223-234.
Bennett, M.D., Leitch, I.J., 2001. Nuclear DNA amounts in pteridophytes. Ann. Bot. 87, 335-345.
Bennett, M.D., Leitch, I.J., 2012. Plant DNA C-values Database, Release 6.0. [Online]. Royal Botanic Gardens, Kew. Available from http://www.kew.org/cvalues/.
Biderre, C., Canning, E.U., Metenier, G., et al., 1999. Comparison of two isolates of Encephalitozoon hellem and E. intestinalis (Microspora) by pulsed field gel electrophoresis. Eur. J. Protistol. 35, 194-196.
Bonett, R.M., Hess, A.J., Ledbetter, N.M., 2020. Facultative transitions have trouble committing, but stable life cycles predict Salamander genome size evolution. Evol. Biol. 47, 111-122.
Christenhusz, M.J.M., Chase, M.W., Fay, M.F., et al., 2021. Biogeography and genome size evolution of the oldest extant vascular plant genus, Equisetum (Equisetaceae). Ann. Bot. 127, 681-695.
Clark, J., Hidalgo, O., Pellicer, J., et al., 2016. Genome evolution of ferns: evidence for relative stasis of genome size across the fern phylogeny. New Phytol. 210, 1072-1082.
Dai, S.J., Wang, Q.X., Bao, W.M., 2002. Spore morphology of pteridophytes from China III. Thelypteridaceae 1. Cyclosorus Link. Acta Phytotaxon. Sin. 40, 334-344.
Dai, S.J., Wang, Q.X., Bao, W.M., et al., 2005a. Spore morphology of pteridophytes from China IV. Thelypteridaceae 2. Acta Phytotaxon. Sin. 43, 233-245.
Dai, S.J., Wang, Q.X., Bao, W.M., 2005b. Spore morphology of pteridophytes from China V. Aspleniaceae. Acta Phytotaxon. Sin. 43, 246-261.
Dai, S.J., Wang, Q.X., Yu, J., et al., 2005c. Spore morphology of pteridophytes from China VI. Pteridaceae. Acta Bot. Yunnan. 27, 489-500.
David, A., 2009. Conservatism and diversification of plant functional traits: evolutionary rates versus phylogenetic signal. Proc. Natl. Acad. Sci. U.S.A. 106, 19699-19706.
Dolezel, J., Bartos, J., 2005. Plant DNA flow cytometry and estimation of nuclear genome size. Ann. Bot. 95, 99-110.
Dolezel, J., Bartos, J., Voglmayr, H., et al., 2003. Nuclear DNA content and genome size of trout and human. Cytometry 51, 127-128.
Dyer, R.J., Pellicer, J., Savolainen, V., et al., 2013. Genome size expansion and the relationship between nuclear DNA content and spore size in the Asplenium monanthes fern complex (Aspleniaceae). BMC Plant Biol. 13, 219.
Fujiwara, T., Liu, H., Meza-Torres, E.I., et al., 2021. Evolution of genome space occupation in ferns: linking genome diversity and species richness. Ann. Bot. XX, 1-12. https://doi.org/10.1093/aob/mcab094.
Gregory, T.R., 2001. Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biol. Rev. 76, 65-101.
Gregory, T.R., 2004. Insertion-deletion biases and the evolution of genome size. Gene 324, 15-34.
Gregory, T.R., 2005. Synergy between sequence and size in large-scale genomics. Nat. Rev. Genet. 6, 699-708.
Grover, C.E., Wendel, J.F., 2010. Recent insights into mechanisms of genome size change in plants. J. Bot. 2010, 382732. https://doi.org/10.1155/2010/382732.
Hanson, L., Leitch, I.J., 2002. DNA amounts for five pteridophyte species fill phylogenetic gaps in C-value data. Bot. J. Linn. Soc. 140, 169-173.
Haufler, C.H., 2002. Homospory 2002: an odyssey of progress in pteridophyte genetics and evolutionary biology. Bioscience 52, 1081-1093.
Haufler, C.H., 2014. Ever since Klekowski: testing a set of radical hypotheses revives the genetics of ferns and lycophytes. Am. J. Bot. 101, 2036-2042.
Hawkins, J.S., Grover, C.E., Wendel, J.F., 2008. Repeated big bangs and the expanding universe: directionality in plant genome size evolution. Plant Sci. 174, 557-562.
Henry, T.A., Bainard, J.D., Newmaster, S.G., 2014. Genome size evolution in Ontario ferns (Polypodiidae): evolutionary correlations with cell size, spore size, and habitat type and an absence of genome downsizing. Genome 57, 555-566.
Hidalgo, O., Pellicer, J., Christenhusz, M.J.M., et al., 2017a. Is there an upper limit to genome size? Trends Plant Sci. 22, 567-573.
Hidalgo, O., Pellicer, J., Christenhusz, M.J.M., et al., 2017b. Genomic gigantism in the whisk-fern family (Psilotaceae): Tmesipteris obliqua challenges record holder Paris japonica. Bot. J. Linn. Soc. 183, 509-514.
Huang, C.H., Qi, X., Chen, D., et al., 2020. Recurrent genome duplication events likely contributed to both the ancient and recent rise of ferns. J. Integr. Plant Biol. 62, 433-455.
Ji, Y.Q., Qin, Z.Y., Wang, Q.X., et al., 2014. Development of gametophytes of Tectaria decurrens and Tectaria fauriei. Acta Bot. Bor.-Occid. Sin. 34, 689-694.
Jiang, N., Dai, X.L., Cao, J.G., et al., 2010. Spore morphology of pteridophytes from China X. Polypodiaceae. Acta Bot. Bor.-Occid. Sin. 30, 2151-2163.
Kang, M., Tao, J.J., Wang, J., et al., 2014. Adaptive and nonadaptive genome size evolution in Karst endemic flora of China. New Phytol. 202, 1371-1381.
Kassambara, A., Kassambara, M.A., 2020. Package ‘ggpubr’, pp. Klekowski, E.J., Baker, H.G., 1966. Evolutionary significance of polyploidy in pteridophyta. Science 153, 305-307.
Klekowski, E.J., Baker, H.G., 1966. Evolutionary significance of polyploidy in pteridophyta. Science 153, 305-307.
Kott, L.S., Britton, D.M., 1982. A comparative study of sporophyte morphology of three cytotypes of Polypodium virginianum in Ontario. Can. J. Bot. 60, 1360-1370.
Lehtonen, S., Silvestro, D., Karger, D.N., et al., 2017. Environmentally driven extinction and opportunistic origination explain fern diversification patterns. Sci. Rep. 7, 4831.
Leitch, A.R., Leitch, I.J., 2012. Ecological and genetic factors linked to contrasting genome dynamics in seed plants. New Phytol. 194, 629-646.
Leitch, I.J., Leitch, A.R., 2013. Genome size diversity and evolution in land plants. In:Leitch, I.J., Greilhuber, J., Dolezel, J., Wendel, J.F. (Eds.), Plant Genome Diversity, vol. 2. Springer-Verlag, Vienna, pp. 307-322.
Li, Y.Q., Li, Y.J., Li, H., et al., 2010. A comparative study on the leaf blade structure and spore of seven Pyrrosia species in Guangxi. Guihaia 30, 462-470.
Little, D.P., Moran, R.C., Brenner, E.D., Stevenson, D.W., 2007. Nuclear genome size in Selaginella. Genome 50, 351-356.
Liu, J.X., 1997. Studies on the spore morphology of Equisetaceae from China. J. Guizhou Agric. Coll. 16, 31-33.
Liu, H.M., Ekrt, L., Koutecky, P., et al., 2019. Polyploidy does not control all: lineagespecific average chromosome length constrains genome size evolution in ferns. J. Syst. Evol. 57, 418-430.
Loureiro, J., Rodriguez, E., Doležel, J., et al., 2007. Two new nuclear isolation buffers for plant DNA flow cytometry: a test with 37 species. Ann. Bot. 100, 875-888.
Lu, J.M., Li, D.Z., Wu, D., 2007. Spore morphology of the family Dryopteridaceae. Acta Bot. Yunnanica 29, 397-408.
Moran, R.C., 1982. The Asplenium trichomanes complex in the United States and adjacent Canada. Am. Fern J. 72, 5-11.
Nakazato, T., Bogonovich, M., Moyle, L.C., 2008a. Environmental factors predict adaptive phenotypic differentiation within and between two wild Andean tomatoes. Evolution 62, 774-792.
Nakazato, T., Barker, M.S., Rieseberg, L.H., et al., 2008b. In: Ranker, T.A., Haufler, C.H.(Eds.), Biology and Evolution of Ferns and Lycophytes. Cambridge Univ. Press, UK, pp. 175-198.
Obermayer, R., Leitch, I.J., Hanson, L., et al., 2002. Nuclear DNA C-values in 30 species double the familial representation in pteridophytes. Ann. Bot. 90, 209-217.
One Thousand Plant Transcriptomes Initiative, 2019. One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574, 679-685.
Otto, F., 1990. DAPI staining of fixed cells for high-resolution flow cytometry of nuclear DNA. In: Crissman, H.A., Darzynkiewicz, Z. (Eds.), Methods in Cell Biology, vol. 33. Academic Press, New York, pp. 105-110.
Pellicer, J., Fay, M.F., Leitch, I.J., 2010. The largest eukaryotic genome of them all? Bot. J. Linn. Soc. 164, 10-15.
Petrov, D.A., 2002. Mutational equilibrium model of genome size evolution. Theor. Popul. Biol. 61, 531-544.
R Core Team, 2018. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
R Core Team, 2020. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
Rabinowicz, P.D., 2005. Differential methylation of genes and repeats in land plants. Genome Res. 15, 1431-1440.
Revell, L.J., 2012. Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217-223.
Schubert, I., Oud, J.L., 1997. There is an upper limit of chromosome size for normal development of an organism. Cell 88, 515-520.
Schuettpelz, E., Pryer, K.M., 2009. Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. Proc. Natl. Acad. Sci. U.S.A. 106, 11200-11205.
Shi, X., Yang, L.H., Chen, Q., 2017. Spore morphology of genus Pyrrosia from China. Guihaia 37, 1455-1462.
Slijepcevic, P., 2018. Genome dynamics over evolutionary time: "C-value enigma" in light of chromosome structure. Mutat. Res-Gen. Tox. En. 836, 22-27.
Smith, A.R.., Pryer, K.M., Schuettpelz, E., et al., 2006. A classification for extant ferns. Taxon 55, 705-731.
Szövényi, P., Gunadi, A., Li, F.W., 2021. Charting the genomic landscape of seed-free plants. Nat. Plants 7, 554-565. https://doi.org/10.1038/s41477-021-00888-z.
The Pteridophyte Phylogeny Group, 2016. A community-derived classification for extant lycophytes and ferns. J. Syst. Evol. 54, 563-603.
Thomas, C.A., 1971. The genetic organization of chromosomes. Annu. Rev. Genet. 5, 237-256.
Tryon, A.F., Lugardon, B., 1991. Spores of the Pteridophyta. Springer, New York.
Wagner, W.H.J., Wagner, F.S., 1979. Polyploidy in pteridophytes. Basic Life Sci. 13, 199-214.
Wakamiya, I., Newton, R.J., Johnston, J.S., et al., 1993. Genome size and environmental-factors in the genus Pinus. Am. J. Bot. 80, 1235-1241.
Wang, Q.X., Yu, J., Zhang, X.C., 2001. Spore morphology of pteridophytes from China I. Lygodiaceae. Acta Phytotaxon. Sin. 39, 38-44.
Wang, R.X., Lu, S.G., Deng, X.C., et al., 2006a. Spore morphology of three species of Adiantum L. from Guangxi, China. J. Guangxi Normal Univ. Nat. Sci. Ed.: J. Nat. Resour. Life Sci. Educ. 24, 79-81.
Wang, R.X., Lu, S.G., Deng, X.C., et al., 2006b. Spore morphology of pteridophytes from Guangxi I. Polypodiaceae. Guihaia 26, 565-569.
Wang, F.G., Liu, H.M., He, C.M., et al., 2015. Taxonomic and evolutionary implications of spore ornamentation in Davalliaceae. J. Syst. Evol. 53, 72-81.
Wang, J., Yu, J., Sun, P., et al., 2020. Paleo-polyploidization in lycophytes. Dev. Reprod. Biol. 18, 333-340.
Webb, C.O., Ackerly, D.D., Kembel, S.W., 2008. Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24, 2098-2100.
Wendel, J.F., Cronn, R.C., Johnston, J.S., et al., 2002. Feast and famine in plant genomes. Genetica 115, 37-47.
Wendel, J.F., Jackson, S.A., Meyers, B.C., et al., 2016. Evolution of plant genome architecture. Genome Biol. 17, 37.
Wood, T.E., Takebayashi, N., Barker, M.S., et al., 2009. The frequency of polyploid speciation in vascular plants. Proc. Natl. Acad. Sci. U.S.A. 106, 13875-13879.
Xu, Y., Dai, X.L., Cao, J.G., 2012. Spore morphology of pteridophytes from China XI. Huperziaceae. Acta Bot. Bor.-Occid. Sin. 32, 1140-1147.
Yang, D.M., He, R.R., Xing, F.W., et al., 2013. Study on spore and leaf epidermis morphology of Pteris (Pteridaceae) from China. Guihaia 33, 1-19.
Zanne, A.E., Tank, D.C., Cornwell, W.K., et al., 2013. Three keys to the radiation of angiosperms into freezing environments. Nature 506, 89-92.
Zhang, Y.L., Xi, Y.Z., Zhang, C.T., et al., 1976. Sporae Pteridophytorum Sinicorum. Science Press, Beijing.
Zhang, J.M., Liu, Y.F., Dong, K., et al., 2002. Studies on the spores morphology of Psilotaceae. J. Cap. Normal Univ. 23, 49-51.
Zhang, Y.J., Liu, Y.J., Zhou, X.M., et al., 2012. Spore morphology of Arachniodes(Dryopteridaceae) from Yunnan. Acta Bot. Bor.-Occid. Sin. 32, 2215-2223.
Zhou, K., Liu, B.B., Wang, Y.L., et al., 2019. Evolutionary mechanism of genome duplication enhancing natural autotetraploid sea barley adaptability to drought stress. Environ. Exp. Bot. 159, 44-54.

[1]	Na Su, Richard G.J. Hodel, Xi Wang, Jun-Ru Wang, Si-Yu Xie, Chao-Xia Gui, Ling Zhang, Zhao-Yang Chang, Liang Zhao, Daniel Potter, Jun Wen. Molecular phylogeny and inflorescence evolution of Prunus (Rosaceae) based on RAD-seq and genome skimming analyses [J]. Plant Diversity, 2023, 45(04): 397-408.
[2]	Yu-Feng Gu, Jiang-Ping Shu, Yi-Jun Lu, Hui Shen, Wen Shao, Yan Zhou, Qi-Meng Sun, Jian-Bing Chen, Bao-Dong Liu, Yue-Hong Yan. Insights into cryptic speciation of quillworts in China [J]. Plant Diversity, 2023, 45(03): 284-301.
[3]	Mei-Zhen Wang, Xiao-Kai Fan, Yong-Hua Zhang, Jing Wu, Li-Mi Mao, Sheng-Lu Zhang, Min-Qi Cai, Ming-Hong Li, Zhang-Shi-Chang Zhu, Ming-Shui Zhao, Lu-Xian Liu, Kenneth M. Cameron, Pan Li. Phylogenomics and integrative taxonomy reveal two new species of Amana (Liliaceae) [J]. Plant Diversity, 2023, 45(01): 54-68.
[4]	Romina Vidal-Russell, Mariana Tadey, Romana Urfusová, Tomáš Urfus, Cintia Paola Souto. Evolutionary importance of the relationship between cytogeography and climate: New insights on creosote bushes from North and South America [J]. Plant Diversity, 2022, 44(05): 492-498.
[5]	Chao Liu, Huan-Huan Chen, Li-Zhou Tang, Phyo Kay Khine, Li-Hong Han, Yu Song, Yun-Hong Tan. Plastid genome evolution of a monophyletic group in the subtribe Lauriineae (Laureae, Lauraceae) [J]. Plant Diversity, 2022, 44(04): 377-388.
[6]	Zhi-Jian Yin, Ze-Huan Wang, Norbert Kilian, Ying Liu, Hua Peng, Ming-Xu Zhao. Mojiangia oreophila (Crepidinae, Cichorieae, Asteraceae), a new species and genus from Mojiang County, SW Yunnan, China, and putative successor of the maternal Faberia ancestor [J]. Plant Diversity, 2022, 44(01): 83-93.
[7]	Guo-Qiang Zhang, Gui-Zhen Chen, Li-Jun Chen, Jun-Wen Zhai, Jie Huang, Xin-Yi Wu, Ming-He Li, Dong-Hui Peng, Wen-Hui Rao, Zhong-Jian Liu, Si-Ren Lan. Phylogenetic incongruence in Cymbidium orchids [J]. Plant Diversity, 2021, 43(06): 452-461.
[8]	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.
[9]	Jun-Chu Peng, Xiang-Guang Ma, Yue-Hua Wang, Hang Sun. New insights into the evolutionary history of Megacodon: Evidence from a newly discovered species [J]. Plant Diversity, 2020, 42(03): 198-208.
[10]	Yujin Li, Qingqing Ye, De He, Huixian Bai, Jianfan Wen. The ubiquity and coexistence of two FBPases in chloroplasts of photosynthetic eukaryotes and its evolutionary and functional implications [J]. Plant Diversity, 2020, 42(02): 120-125.
[11]	Rong Li, Lishen Qian, Hang Sun. Current progress and future prospects in phylofloristics [J]. Plant Diversity, 2018, 40(04): 141-146.
[12]	Bang Feng, Zhuliang Yang. Studies on diversity of higher fungi in Yunnan, southwestern China: A review [J]. Plant Diversity, 2018, 40(04): 165-171.
[13]	Frank Hauenschild, Adrien Favre, Jan Schnitzler, Ingo Michalak, Martin Freiberg, Alexandra N. Muellner-Riehl. Spatio-temporal evolution of Allium L. in the Qinghai-Tibet-Plateau region:Immigration and in situ radiation [J]. Plant Diversity, 2017, 39(04): 167-179.
[14]	Xinmin Zhang, Darong Yang. Occurrence of internally ovipositing non-agaonid wasps and pollination mode of the associated agaonid wasps [J]. Plant Diversity, 2017, 39(03): 130-134.
[15]	Rong Li. Using a mega-phylogeny of seed plants to test for non-random patterns of areal-types across the Chinese tree of life [J]. Plant Diversity, 2016, 38(06): 283-288.

Genome size evolution of the extant lycophytes and ferns

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 15

Recommended Articles

Metrics