Central Asia revealed as a key area in evolution of Eremurus (Asphodelaceae)

doi:10.1016/j.pld.2023.08.004

Plant Diversity ›› 2024, Vol. 46 ›› Issue (03): 333-343.DOI: 10.1016/j.pld.2023.08.004

• Articles • Previous Articles Next Articles

Central Asia revealed as a key area in evolution of Eremurus (Asphodelaceae)

Dilmurod Makhmudjanov^a,b,c,d, Sergei Volis^c, Ziyoviddin Yusupov^a,b,c, Inom Juramurodov^a,b,c,d, Komiljon Tojibaev^b,c, Tao Deng^a,b, Hang Sun^a,b

a. CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, Yunnan, China;
b. Yunnan International Joint Laboratory for Biodiversity of Central Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, Yunnan, China;
c. Institute of Botany, Academy Sciences of Uzbekistan, Tashkent 100125, Uzbekistan;
d. University of Chinese Academy of Sciences, Beijing 100864, China

Received:2023-06-30 Revised:2023-08-22 Online:2024-05-20 Published:2024-05-25
Contact: Komiljon Tojibaev,E-mail:ktojibaev@mail.ru;Tao Deng,E-mail:dengtao@mail.kib.ac.cn;Hang Sun,E-mail:sunhang@mail.kib.ac.cn
Supported by:
The authors are thankful to Dr. David Boufford from Harvard University Herbaria (USA) for editing the English. We would like to thank Davlatali Abdullaev (Institute of Botany, Academy of Sciences of Uzbekistan) and Isakul Turakulov (Khujand State University, Tajikistan) for their help in identifying the species and for collecting materials used in this study. We are also grateful to Davron Dekhkonov (Namangan State University, Uzbekistan) and Xianhan Huang (Kunming Institute of Botany, China) for their useful comments and suggestions. This study was supported by grants from the Key Projects of the Joint Fund of the National Natural Science Foundation of China (U23A20149), the Second Tibetan Plateau Scientific Expedition and Research (STEP) program (2019QZKK0502), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA20050203), International Partnership Program of the Chinese Academy of Sciences (151853KYSB20180009), the state research project ‘Taxonomic revision of polymorphic plant families of the flora of Uzbekistan' (FZ-20200929321) and the State Programs for the years 2021-2025 ‘Grid mapping of the flora of Uzbekistan' and the ‘Tree of life:monocots of Uzbekistan' of the Institute of Botany of the Academy of Sciences of the Republic of Uzbekistan.

Central Asia revealed as a key area in evolution of Eremurus (Asphodelaceae)

Dilmurod Makhmudjanov^a,b,c,d, Sergei Volis^c, Ziyoviddin Yusupov^a,b,c, Inom Juramurodov^a,b,c,d, Komiljon Tojibaev^b,c, Tao Deng^a,b, Hang Sun^a,b

a. CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, Yunnan, China;
b. Yunnan International Joint Laboratory for Biodiversity of Central Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, Yunnan, China;
c. Institute of Botany, Academy Sciences of Uzbekistan, Tashkent 100125, Uzbekistan;
d. University of Chinese Academy of Sciences, Beijing 100864, China

通讯作者: Komiljon Tojibaev,E-mail:ktojibaev@mail.ru;Tao Deng,E-mail:dengtao@mail.kib.ac.cn;Hang Sun,E-mail:sunhang@mail.kib.ac.cn
基金资助:
The authors are thankful to Dr. David Boufford from Harvard University Herbaria (USA) for editing the English. We would like to thank Davlatali Abdullaev (Institute of Botany, Academy of Sciences of Uzbekistan) and Isakul Turakulov (Khujand State University, Tajikistan) for their help in identifying the species and for collecting materials used in this study. We are also grateful to Davron Dekhkonov (Namangan State University, Uzbekistan) and Xianhan Huang (Kunming Institute of Botany, China) for their useful comments and suggestions. This study was supported by grants from the Key Projects of the Joint Fund of the National Natural Science Foundation of China (U23A20149), the Second Tibetan Plateau Scientific Expedition and Research (STEP) program (2019QZKK0502), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA20050203), International Partnership Program of the Chinese Academy of Sciences (151853KYSB20180009), the state research project ‘Taxonomic revision of polymorphic plant families of the flora of Uzbekistan' (FZ-20200929321) and the State Programs for the years 2021-2025 ‘Grid mapping of the flora of Uzbekistan' and the ‘Tree of life:monocots of Uzbekistan' of the Institute of Botany of the Academy of Sciences of the Republic of Uzbekistan.

Abstract

Abstract: Eremurus was described at the beginning of the 19th century. However, due to limited sampling and the small number of gene markers to date, its phylogeny and evolution are largely unknown. In this study, we analyzed plastomes from 27 species belonging to 2 subgenera and 3 sections of Eremurus, which are found in Central Asia (its center of diversity) and China. We also analyzed nuclear DNA ITS of 33 species, encompassing all subgenera and sections of the genus in Central Asia, southwest Asia and China. Our findings revealed that the genus was monophyletic, although both subgenera Eremurus and Henningia were found to be paraphyletic. Both plastome and nrDNA-based phylogenetic trees had three clades that did not reflect the current taxonomy of the genus. Our biogeographical and time-calibrated trees suggest that Eremurus originated in the ancient Tethyan area in the second half of the Eocene. Diversification of Eremurus occurred from the early Oligocene to the late Miocene. Paratethys Sea retreat and several orogenetic events, such as the progressive uplift of the Qinghai-Tibet Plateau and surrounding mountain belts (Altai, Pamir, Tian Shan), caused serious topographic and climate (aridification) changes in Central Asia that may have triggered a split of clades and speciation. In this transformed Central Asia, speciation proceeded rapidly driven mainly by vicariance caused by numerous mountain chains and specialization to a variety of climatic, topographic and soil conditions that exist in this region.

Key words: Asphodelaceae, Asphodeloideae, Plastome, Central Asia, Qinghai-Tibet Plateau

摘要： Eremurus was described at the beginning of the 19th century. However, due to limited sampling and the small number of gene markers to date, its phylogeny and evolution are largely unknown. In this study, we analyzed plastomes from 27 species belonging to 2 subgenera and 3 sections of Eremurus, which are found in Central Asia (its center of diversity) and China. We also analyzed nuclear DNA ITS of 33 species, encompassing all subgenera and sections of the genus in Central Asia, southwest Asia and China. Our findings revealed that the genus was monophyletic, although both subgenera Eremurus and Henningia were found to be paraphyletic. Both plastome and nrDNA-based phylogenetic trees had three clades that did not reflect the current taxonomy of the genus. Our biogeographical and time-calibrated trees suggest that Eremurus originated in the ancient Tethyan area in the second half of the Eocene. Diversification of Eremurus occurred from the early Oligocene to the late Miocene. Paratethys Sea retreat and several orogenetic events, such as the progressive uplift of the Qinghai-Tibet Plateau and surrounding mountain belts (Altai, Pamir, Tian Shan), caused serious topographic and climate (aridification) changes in Central Asia that may have triggered a split of clades and speciation. In this transformed Central Asia, speciation proceeded rapidly driven mainly by vicariance caused by numerous mountain chains and specialization to a variety of climatic, topographic and soil conditions that exist in this region.

关键词: Asphodelaceae, Asphodeloideae, Plastome, Central Asia, Qinghai-Tibet Plateau

Dilmurod Makhmudjanov, Sergei Volis, Ziyoviddin Yusupov, Inom Juramurodov, Komiljon Tojibaev, Tao Deng, Hang Sun. Central Asia revealed as a key area in evolution of Eremurus (Asphodelaceae)[J]. Plant Diversity, 2024, 46(03): 333-343.

References

[1] APG IV. 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants:APG IV. Bot. J. Linn. Soc. 181, 1-20.
[2] Baker, J.G., 1877. Revision of the genera and species of Anthericeae and Eriospermeae. J. Linn. Soc. 15, 253-363.
[3] Ballato, P., Cifelli, F., Heidarzadeh, G., et al., 2017. Tectono-sedimentary evolution of the northern Iranian Plateau:insights from middle-late Miocene foreland-basin deposits. Basin Res. 29, 417-446.
[4] Bialik, O.M., Frank, M., Betzler, C., et al., 2019. Two-step closure of the Miocene Indian Ocean Gateway to the Mediterranean. Sci. Rep. 9, 8842.
[5] Bieberstein, F.A.M.v. 1819. Flora Taurico-Caucasica. Typis Academicis. Charkouiae (Kharkov), pp. 269-270.
[6] Boissier, E. 1884. Eremurus. in:Boissier, E.(Eds.), Flora Orientalis. Georg, H. Geneve, pp. 321-328.
[7] Brandham, P., 1971. The chromosomes of the Liliaceae:II:Polyploidy and karyotype variation in the Aloineae. Kew Bull. 25, 381-399.
[8] Chase, M.W., De Bruijn, A.Y., Cox, A.V., et al., 2000. Phylogenetics of Asphodelaceae (Asparagales):an analysis of plastid rbcL and trnL-F DNA sequences. Ann. Bot. 86, 935-951.
[9] Cheng, L., Zhang, Y.J., 1993. Chromosome number and karyotype of Eremurus chinensis Fedtsch. Wuhan. Bot. Res. 11, 281-282.
[10] Clift, P.D., Hodges, K.V., Heslop, D., et al., 2008. Correlation of Himalayan exhumation rates and Asian monsoon intensity. Nat. Geosci. 1, 875-880.
[11] Copeland, P., Harrison, T.M., Pan, Y., et al., 1995. Thermal evolution of the Gangdese batholith, southern Tibet:a history of episodic unroofing. Tectonics 14, 223-236.
[12] Darriba, D., Taboada, G.L., Doallo, R., et al., 2012. jModelTest 2:more models, new heuristics and parallel computing. Nat. Methods 9, 772-772.
[13] Deng, T., Nie, Z.-L., Drew, B.T., et al., 2015. Does the Arcto-Tertiary biogeographic hypothesis explain the disjunct distribution of Northern Hemisphere herbaceous plants?The case of Meehania(Lamiaceae). PLoS One 10, e0117171.
[14] Deng, T., Zhang, J.-W., Meng, Y., et al., 2017. Role of the Qinghai-Tibetan Plateau uplift in the Northern Hemisphere disjunction:evidence from two herbaceous genera of Rubiaceae. Sci. Rep. 7, 13411.
[15] Devey, D.S., Leitch, I., Pires, J.C., et al., 2006. Systematics of Xanthorrhoeaceae sensu lato, with an emphasis on Bulbine. Aliso:A Journal of Systematic and Floristic Botany 22, 345-351.
[16] Dierckxsens, N., Mardulyn, P., Smits, G., 2017. NOVOPlasty:de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res. 45, e18-e18.
[17] Ding, H., Zhang, Z., Dong, X., et al., 2016. Early Eocene (c. 50 Ma) collision of the Indian and Asian continents:Constraints from the North Himalayan metamorphic rocks, southeastern Tibet. Earth Planet Sci. Lett. 435, 64-73.
[18] Doyle, J.J., Doyle, J.L., 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19, 11-15.
[19] Drummond, A.J., Rambaut, A., 2007. BEAST:Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 1-8.
[20] Eker, I. 2020. Eremurus M.Bieb. in:Guner, A., Kandemir, A., Menemen, Y., et al. eds., The Illustrated Flora of Turkey web version. ANG Foundation Nezahat Gokyigit Botanik Bahcesi Publications. Istanbul, pp. 1-9.
[21] Fedtschenko, B. 1935. Eremurus M.Bieb. in:Komarov, V.(Eds.), Flora of the USSR. USSR Acad. Sci. Leningrad, pp. 37-52.
[22] Fehrer, J., Gemeinholzer, B., Chrtek Jr, J., et al., 2007. Incongruent plastid and nuclear DNA phylogenies reveal ancient intergeneric hybridization in Pilosella hawkweeds (Hieracium, Cichorieae, Asteraceae). Mol. Phylogenet. Evol. 42, 347-361.
[23] Goloskokov, V. 1958. Eremurus. in:Pavlov, N.(Eds.), Flora of Kazakhstan. Acad. Sci. KazSSR. Almaty, pp. 109-117.
[24] Gupta, A.K., Yuvaraja, A., Prakasam, M., et al., 2015. Evolution of the South Asian monsoon wind system since the late Middle Miocene. Palaeogeogr. Palaeoclimatol. Palaeoecol. 438, 160-167.
[25] Harrison, T.M., Copeland, P., Kidd, W., et al., 1992. Raising tibet. Science 255, 1663-1670.
[26] Hedge, I., Wendelbo, P., 1963. Notes on the giant Asphodels of Afghanistan. J. R. Hortic. 88, 402-406.
[27] Jansen, R.K., Cai, Z., Raubeson, L.A., et al., 2007. Analysis of 81 genes from 64 plastid genomes resolves relationships in angiosperms and identifies genome-scale evolutionary patterns. PNAS 104, 19369-19374.
[28] Jin, J.J., Yu, W.B., Yang, J.B., et al., 2020. GetOrganelle:a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol. 21, 1-31.
[29] Kashenko, L. 1951. Eremurus. in:Vvedensky, A.(Eds.), Flora of Kirgizii. Kirgiztan USSR. Frunze, pp. 29-36.
[30] Katoh, K., Standley, D.M., 2013. MAFFT multiple sequence alignment software version 7:improvements in performance and usability. Mol. Biol. Evol. 30, 772-780.
[31] Kearse, M., Moir, R., Wilson, A., et al., 2012. Geneious Basic:an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 28, 1647-1649.
[32] Khokhryakov, А., 1965. Eremuruses and its Culture. Nauka. Moskow.
[33] Kumar, S., Stecher, G., Tamura, K., 2016. MEGA7:molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870-1874.
[34] Lee, S.Y., Xu, K.W., Huang, C.Y., et al., 2022. Molecular phylogenetic analyses based on the complete plastid genomes and nuclear sequences reveal Daphne(Thymelaeaceae) to be non-monophyletic as current circumscription. Plant Divers. 44, 279-289.
[35] Lifante, Z.D., 1996. A karyological study of Asphodelus L.(Asphodelaceae) from the Western Mediterranean. Bot. J. Linn. Soc. 121, 285-344.
[36] Ling, W., Lingji, W., Miao, M., et al., 2004. Karyotype analysis of Eremurus anisopterus. J. Shihezi Univ. 22, 417-418.
[37] Liu, C., Chen, H.H., Tang, L.Z., et al., 2022. Plastid genome evolution of a monophyletic group in the subtribe Lauriineae (Laureae, Lauraceae). Plant Divers. 44, 377-388.
[38] Liu, X., Sun, H., Miao, Y., et al., 2015. Impacts of uplift of northern Tibetan Plateau and formation of Asian inland deserts on regional climate and environment. Quat. Sci. Rev. 116, 1-14.
[39] Lu, H., Wang, X., Li, L., 2010. Aeolian sediment evidence that global cooling has driven late Cenozoic stepwise aridification in central Asia. Geol. Soc. Spec. Publ. 342, 29-44.
[40] Maddison, W.P., 2007. Mesquite:a modular system for evolutionary analysis. Version 2.0. http://mesquiteproject.org.
[41] Makhmudjanov, D., Juramurodov, I., Kurbonalieva, M., et al., 2022. Genus Eremurus(Asphodelaceae) in the flora of Uzbekistan. Plant Divers. Cen. As. 2, 82-127.
[42] Makhmudjanov, D., Yusupov, Z., Abdullaev, D., et al., 2019. The complete chloroplast genome of Eremurus robustus(Asphodelaceae). Mitochondrial DNA B Resour. 4, 3366-3367.
[43] Male, P.J.G., Bardon, L., Besnard, G., et al., 2014. Genome skimming by shotgun sequencing helps resolve the phylogeny of a pantropical tree family. Mol. Ecol. Resour. 14, 966-975.
[44] Manafzadeh, S., Salvo, G., Conti, E., 2014. A tale of migrations from east to west:the Irano-Turanian floristic region as a source of Mediterranean xerophytes. J. Biogeogr. 41, 366-379.
[45] McKain, M.R., McNeal, J.R., Kellar, P.R., et al., 2016. Timing of rapid diversification and convergent origins of active pollination within Agavoideae (Asparagaceae). Am. J. Bot. 103, 1717-1729.
[46] McLay, T.G., Bayly, M., 2016. A new family placement for Australian blue squill, Chamaescilla:Xanthorrhoeaceae (Hemerocallidoideae), not Asparagaceae. Phytotaxa 275, 97-111.
[47] McQuarrie, N., van Hinsbergen, D.J., 2013. Retrodeforming the Arabia-Eurasia collision zone:age of collision versus magnitude of continental subduction. Geology 41, 315-318.
[48] Molnar, P., Boos, W.R., Battisti, D.S., et al., 2010. Orographic controls on climate and paleoclimate of Asia:thermal and mechanical roles for the Tibetan Plateau. Annu. Rev. Earth Planet Sci. 38, 77-102.
[49] Molnar, P., England, P., Martinod, J., 1993. Mantle dynamics, uplift of the Tibetan Plateau, and the Indian monsoon. Rev. Geophys. 31, 357-396.
[50] Moore, M.J., Soltis, P.S., Bell, C.D., et al., 2010. Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots. PNAS 107, 4623-4628.
[51] Mouthereau, F., 2011. Timing of uplift in the Zagros belt/Iranian plateau and accommodation of late Cenozoic Arabia-Eurasia convergence. Geol. Mag. 148, 726-738.
[52] Naderi, S.K., Kazempour, O.S., Zareei, M., 2009. Phylogeny of the genus Eremurus(Asphodelaceae) based on morphological characters in the Flora Iranica area. Iran. J. Bot. 15, 7-35.
[53] Patel, R.K., Jain, M., 2012. NGS QC Toolkit:a toolkit for quality control of next generation sequencing data. PLoS One 7, e30619.
[54] Popov, M.G., 1927. Geographical and morphological methods in systematics and processes of hybridization in nature. Tr. Prik. Bot. Sel. 17, 221-229.
[55] Popov, M.G., 1941. Geographic and genetic elements of the flora of the Alma-Ata Reserve. Vegetation of Kazakhstan. Publishing House of the Academy of Sciences of the USSR. Moscow.
[56] Popov, M.G., 1963. Basic Florogenetics. Academy of Sciences of the USSR. Moscow-Leningrad.
[57] Rambaut, A., 2018. FigTree-Tree Figure Drawing Tool Version v. 1.4.4. http://tree.bio.ed.ac.uk/software/figtree/.
[58] Ramstein, G., Fluteau, F., Besse, J., et al., 1997. Effect of orogeny, plate motion and land-sea distribution on Eurasian climate change over the past 30 million years. Nature 386, 788-795.
[59] Raza, J., Ahmad, M., Zafar, M., et al., 2022. Systematic significance of seed morphology and foliar anatomy among Acanthaceous taxa. Biologia 77, 3125-3142.
[60] Richter, F., Pearson, J., Vilkas, M., et al., 2022. Growth of the southern Tian Shan-Pamir and its impact on central Asian climate. GSA Bull. 135, 1859-1878.
[61] Rieseberg, L.H., Soltis, D., 1991. Phylogenetic consequences of cytoplasmic gene flow in plants. Evol. Trends Plants 5, 65-84.
[62] Ronquist, F., Huelsenbeck, J.P., 2003. MrBayes 3:Bayesian phylogenetic inference under mixed models. Bioinformatics. 19, 1572-1574.
[63] Safar, K.N., Osaloo, S.K., Assadi, M., et al., 2014. Phylogenetic analysis of Eremurus, Asphodelus, and Asphodeline(Xanthorrhoeaceae-Asphodeloideae) inferred from plastid trnL-F and nrDNA ITS sequences. Biochem. Syst. Ecol. 56, 32-39.
[64] Sato, T., Kimura, F., 2005. Impact of diabatic heating over the Tibetan Plateau on subsidence over northeast Asian arid region. Geophys. Res. Lett. 32, L05809.
[65] Soltis, D.E., Kuzoff, R.K., 1995. Discordance between nuclear and chloroplast phylogenies in the Heuchera group (Saxifragaceae). Evolution 49, 727-742.
[66] Song, Y.-X., Peng, S., Mutie, F.M., et al., 2022. Evolution and taxonomic significance of seed micromorphology in Impatiens(Balsaminaceae). Front. Plant Sci. 13, 215.
[67] Stamatakis, A., 2014. RAxML version 8:a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 30, 1312-1313.
[68] Su, N., Hodel, R.G., Wang, X., et al., 2023. Molecular phylogeny and inflorescence evolution of Prunus(Rosaceae) based on RAD-seq and genome skimming analyses. Plant Divers.
[69] Suchard, M.A., Rambaut, A., 2009. Many-core algorithms for statistical phylogenetics. Bioinformatics. 25, 1370-1376.
[70] Sun, H., Zhang, J., Deng, T., et al., 2017. Origins and evolution of plant diversity in the Hengduan Mountains, China. Plant Divers. 39, 161.
[71] Swofford, D.L., 2002. PAUP^*, Phylogenetic Analysis Using Parsimony (^* and Other Methods). Version 4.10. Sinauer Associates. Sunderland.
[72] Thorsen, M.J., Dickinson, K.J., Seddon, P.J., et al., 2009. Seed dispersal systems in the New Zealand flora. Perspect. Plant Ecol. Evol. Syst. 11, 285-309.
[73] Tuzlaci, E., 1986. Chromosome numbers of some Asphodeline species. MARMARA Pharm. J. 2, 113-117.
[74] Vaidya, G., Lohman, D.J., Meier, R., 2011. SequenceMatrix:concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27, 171-180.
[75] Vvedensky, A. 1932. Eremurus. in:Fedtschenko, B.A., Popov, M.G. eds., Flora of Turkmenii. USSR Acad. Sci. and Bot. Ins. Turkm. USSR. Leningrad, pp. 250-257.
[76] Vvedensky, A. 1941. Eremurus. in:Kudryashev, S.(Eds.), Flora of Uzbekistan. Uzb. Sec. USSR Acad. Sci. Tashkent, pp. 398-410.
[77] Vvedensky, A. 1963. Eremurus. in:Ovchinnikov, P.(Eds.), Flora of Tadjikistan. USSR Acad. Sci. Moscow-Leningrad, pp. 186-212.
[78] Vvedensky, A., Kovalevskaya, S. 1971. Eremurus. in:Kovalevskaya, S.(Eds.), Conspectus Florae Asiae Mediae. Fan UzSSR Tashkent, pp. 14-27.
[79] Wang, X., Carrapa, B., Chapman, J.B., et al., 2019. Parathethys last gasp in central Asia and late Oligocene accelerated uplift of the Pamirs. Geophys. Res. Lett. 46, 11773-11781.
[80] Wendel, J.F., Doyle, J.J. 1998. Phylogenetic Incongruence:Window into Genome History and Molecular Evolution. Molecular Systematics of Plants II:DNA Sequencing. Springer. Boston, pp. 265-296.
[81] Wendelbo, P. 1958. Eremurus. in:Koeie, M., Rechinger, K.H. eds., Symbolae Afghanicae, pp. 150-191.
[82] Wendelbo, P. 1982. Asphodeloideae: Asphodelus, Asphodeline& Eremerus. in:Rechinger, K.(Eds.), Flora Iranica, pp. 3-31.
[83] Wendelbo, P., Furse, P. 1969. Eremurus of South West Asia. Lily Year Book, pp. 56-69.
[84] Xinqi, C., Turland, N. 2000. Eremurus. in:Wu, Z., Raven, P. eds., Flora of China. Science Press and Missouri Botanical Garden Press. Beijing and St. Louis (MO), pp. 159-160.
[85] Yu, Y., Blair, C., He, X., 2020. RASP 4:ancestral state reconstruction tool for multiple genes and characters. Mol. Biol. Evol. 37, 604-606.
[86] Yusupov, Z., Deng, T., Volis, S., et al., 2020. Phylogenomics of Allium section Cepa(Amaryllidaceae) provides new insights on domestication of onion. Plant Divers. 43, 102-110.
[87] Yusupov, Z., Ergashov, I., Volis, S., et al., 2022. Seed macro-and micromorphology in Allium (Amaryllidaceae) and its phylogenetic significance. Ann. Bot. 129, 869-911.
[88] Zhang, Z., Flatoey, F., Wang, H., et al., 2012. Early Eocene Asian climate dominated by desert and steppe with limited monsoons. J. Asian Earth Sci. 44, 24-35.
[89] Zhuang, G., Pagani, M., Zhang, Y.G., 2017. Monsoonal upwelling in the western Arabian Sea since the middle Miocene. Geology 45, 655-658.
[90] Zonneveld, B.J., 2002. Genome size analysis of selected species of Aloe(Aloaceae) reveals the most primitive species and results in some new combinations. Bradleya 2002, 5-12.

Central Asia revealed as a key area in evolution of Eremurus (Asphodelaceae)

Central Asia revealed as a key area in evolution of Eremurus (Asphodelaceae)

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	Kai Chen, Yan-Chun Liu, Yue Huang, Xu-Kun Wu, Hai-Ying Ma, Hua Peng, De-Zhu Li, Peng-Fei Ma. Reassessing the phylogenetic relationships of Pseudosorghum and Saccharinae (Poaceae) using plastome and nuclear ribosomal sequences [J]. Plant Diversity, 2025, 47(03): 382-393.
[2]	Amos Kipkoech, Ke Li, Richard I. Milne, Oyetola Olusegun Oyebanji, Moses C. Wambulwa, Xiao-Gang Fu, Dennis A. Wakhungu, Zeng-Yuan Wu, Jie Liu. An integrative approach clarifies species delimitation and biogeographic history of Debregeasia (Urticaceae) [J]. Plant Diversity, 2025, 47(02): 229-243.
[3]	Linjiang Ye, Robabeh Shahi Shavvon, Hailing Qi, Hongyu Wu, Pengzhen Fan, Mohammad Nasir Shalizi, Safiullah Khurram, Mamadzhanov Davletbek, Yerlan Turuspekov, Jie Liu. Population genetic insights into the conservation of common walnut (Juglans regia) in Central Asia [J]. Plant Diversity, 2024, 46(05): 600-610.
[4]	Peng-Cheng Fu, Qiao-Qiao Guo, Di Chang, Qing-Bo Gao, Shan-Shan Sun. Cryptic diversity and rampant hybridization in annual gentians on the Qinghai-Tibet Plateau revealed by population genomic analysis [J]. Plant Diversity, 2024, 46(02): 194-205.
[5]	Nian Zhou, Ke Miao, Changkun Liu, Linbo Jia, Jinjin Hu, Yongjiang Huang, Yunheng Ji. Historical biogeography and evolutionary diversification of Lilium (Liliaceae): New insights from plastome phylogenomics [J]. Plant Diversity, 2024, 46(02): 219-228.
[6]	Haibin Yu, Man Yang, Zixin Lu, Weitao Wang, Fangyuan Yu, Yonghua Zhang, Xue Yin, Hongjun Yu, Junjie Hu, David C. Deane. A phylogenetic approach identifies patterns of beta diversity and floristic subregions of the Qinghai-Tibet Plateau [J]. Plant Diversity, 2024, 46(01): 59-69.
[7]	Yue-Wen Xu, Lu Sun, Rong Ma, Yong-Qian Gao, Hang Sun, Bo Song. Does pollinator dependence decrease along elevational gradients? [J]. Plant Diversity, 2023, 45(04): 446-455.
[8]	Rivontsoa A. Rakotonasolo, Soejatmi Dransfield, Thomas Haevermans, Helene Ralimanana, Maria S. Vorontsova, Meng-Yuan Zhou, De-Zhu Li. New insights into intergeneric relationships of Hickeliinae (Poaceae: Bambusoideae) revealed by complete plastid genomes [J]. Plant Diversity, 2023, 45(02): 125-132.
[9]	Shi-Yu Lv, Xia-Ying Ye, Zhong-Hu Li, Peng-Fei Ma, De-Zhu Li. Testing complete plastomes and nuclear ribosomal DNA sequences for species identification in a taxonomically difficult bamboo genus Fargesia [J]. Plant Diversity, 2023, 45(02): 147-155.
[10]	Yan-Ling Xu, Hao-Hua Shen, Xin-Yu Du, Lu Lu. Plastome characteristics and species identification of Chinese medicinal wintergreens (Gaultheria, Ericaceae) [J]. Plant Diversity, 2022, 44(06): 519-529.
[11]	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.
[12]	Shiou Yih Lee, Ke-Wang Xu, Cui-Ying Huang, Jung-Hyun Lee, Wen-Bo Liao, Yong-Hong Zhang, Qiang Fan. Molecular phylogenetic analyses based on the complete plastid genomes and nuclear sequences reveal Daphne (Thymelaeaceae) to be non-monophyletic as current circumscription [J]. Plant Diversity, 2022, 44(03): 279-289.
[13]	Mengqing Zhe, Le Zhang, Fang Liu, Yiwei Huang, Weishu Fan, Junbo Yang, Andan Zhu. Plastid RNA editing reduction accompanied with genetic variations in Cymbidium, a genus with diverse lifestyle modes [J]. Plant Diversity, 2022, 44(03): 316-321.
[14]	Jia-Xin Yang, Shuai Peng, Jun-Jie Wang, Shi-Xiong Ding, Yan Wang, Jing Tian, Han Yang, Guang-Wan Hu, Qing-Feng Wang. Morphological and genomic evidence for a new species of Corallorhiza (Orchidaceae: Epidendroideae) from SW China [J]. Plant Diversity, 2021, 43(05): 409-419.
[15]	Xinhui Li, Tao Yang, Dandan Wang. Phylogenetic and functional structures of succession in plant communities on mounds of Marmota himalayana in alpine regions on the northeast edge of the Qinghai-Tibet Plateau [J]. Plant Diversity, 2021, 43(04): 275-280.