Morphological and genome-wide evidence for natural hybridisation within the genus Stipa (Poaceae).
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
14 08 2020
14 08 2020
Historique:
received:
18
02
2020
accepted:
31
07
2020
entrez:
16
8
2020
pubmed:
17
8
2020
medline:
10
2
2021
Statut:
epublish
Résumé
Hybridisation in the wild between closely related species is a common mechanism of speciation in the plant kingdom and, in particular, in the grass family. Here we explore the potential for natural hybridisation in Stipa (one of the largest genera in Poaceae) between genetically distant species at their distribution edges in Mountains of Central Asia using integrative taxonomy. Our research highlights the applicability of classical morphological and genome reduction approaches in studies on wild plant species. The obtained results revealed a new nothospecies, Stipa × lazkovii, which exhibits intermediate characters to S. krylovii and S. bungeana. A high-density DArTseq assay disclosed that S. × lazkovii is an F1 hybrid, and established that the plastid and mitochondrial DNA was inherited from S. bungeana. In addition, molecular markers detected a hybridisation event between morphologically and genetically distant species S. bungeana and probably S. glareosa. Moreover, our findings demonstrated an uncertainty on the taxonomic status of S. bungeana that currently belongs to the section Leiostipa, but it is genetically closer to S. breviflora from the section Barbatae. Finally, we noticed a discrepancy between the current molecular data with the previous findings on S. capillata and S. sareptana.
Identifiants
pubmed: 32796878
doi: 10.1038/s41598-020-70582-1
pii: 10.1038/s41598-020-70582-1
pmc: PMC7427808
doi:
Substances chimiques
DNA, Mitochondrial
0
DNA, Plant
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
13803Références
Grant, V. Plant Speciation 2nd edn. (Columbia University Press, New York, 1981).
doi: 10.7312/gran92318
Abbott, R. J. Plant invasions, hybridization and the evolution of new plant taxa. Trends Ecol. Evol. 7, 401–405. https://doi.org/10.1016/0169-5347(92)90020-C (1992).
doi: 10.1016/0169-5347(92)90020-C
pubmed: 21236080
Rieseberg, L. H. Hybrid origins of plant species. Annu. Rev. Ecol. Syst. 28, 359–389. https://doi.org/10.1146/annurev.ecolsys.28.1.359 (1997).
doi: 10.1146/annurev.ecolsys.28.1.359
Arnold, M. L. Evolution Through Genetic Exchange (Oxford University Press, Oxford, 2006).
Mallet, J. Hybrid speciation. Nature 446, 279–283. https://doi.org/10.1038/nature05706 (2007).
doi: 10.1038/nature05706
pubmed: 17361174
Abbott, R. J. et al. Hybridization and speciation. J Evol Biol 26, 229–246. https://doi.org/10.1111/j.1420-9101.2012.02599.x (2013).
doi: 10.1111/j.1420-9101.2012.02599.x
pubmed: 23323997
Goulet, B. E., Roda, F. & Hopkins, R. Hybridization in plants: old ideas. New Techniques. Plant Physiol. 173, 65–78. https://doi.org/10.1104/pp.16.01340 (2017).
doi: 10.1104/pp.16.01340
pubmed: 27895205
Rieseberg, L. H. & Wendel, J. F. In Hybrid zones and the evolutionary process (ed. Harrison, R. G.) 70–109 (Oxford University Press, Oxford, 1993).
Mallet, J. Hybridization as an invasion of the genome. Trends Ecol. Evol. 20, 229–237. https://doi.org/10.1016/j.tree.2005.02.010 (2005).
doi: 10.1016/j.tree.2005.02.010
pubmed: 16701374
Hamilton, J. A. & Miller, J. M. Adaptive introgression as a resource for management and genetic conservation in a changing climate. Conserv. Biol. 30, 33–41. https://doi.org/10.1111/cobi.12574 (2015).
doi: 10.1111/cobi.12574
pubmed: 26096581
Suarez-Gonzalez, A., Lexer, C. & Cronk, Q. C. B. Adaptive introgression: a plant perspective. Biol. Lett. 14, 20170688. https://doi.org/10.1098/rsbl.2017.0688 (2018).
doi: 10.1098/rsbl.2017.0688
pubmed: 29540564
pmcid: 5897607
López-Caamal, A. & Tovar-Sánchez, E. Genetic, morphological, and chemical patterns of plant hybridization. Revista Chilena Hist. Nat. 87, 1–14. https://doi.org/10.1186/s40693-014-0016-0 (2014).
doi: 10.1186/s40693-014-0016-0
Abbott, R. J., Barton, N. H. & Good, J. M. Genomics of hybridization and its evolutionary consequences. Mol. Ecol. 25, 2325–2332. https://doi.org/10.1111/mec.13685 (2016).
doi: 10.1111/mec.13685
pubmed: 27145128
Lepais, O. et al. Species relative abundance and direction of introgression in oaks. Mol. Ecol. 18, 2228–2242. https://doi.org/10.1111/j.1365-294X.2009.04137.x (2009).
doi: 10.1111/j.1365-294X.2009.04137.x
pubmed: 19302359
Gómez, J. M., González-Megías, A., Lorite, J., Abdelaziz, M. & Perfectti, F. The silent extinction: climate change and the potential hybridization-mediated extinction of endemic high-mountain plants. Biodivers. Conserv. 24, 1843–1857. https://doi.org/10.1007/s10531-015-0909-5 (2015).
doi: 10.1007/s10531-015-0909-5
Mota, M. R., Pinheiro, F., Leal, B. S. S., Wendt, T. & Palma-Silva, C. The role of hybridization and introgression in maintaining species integrity and cohesion in naturally isolated inselberg bromeliad populations. Plant Biol. 21, 122–132. https://doi.org/10.1111/plb.12909 (2019).
doi: 10.1111/plb.12909
pubmed: 30195257
Parisod, C., Definod, C., Sarr, A., Arrigo, N. & Felber, F. Genome-specific introgression between wheat and its wild relative Aegilops triuncialis. J. Evol. Biol. 26, 223–228. https://doi.org/10.1111/jeb.12040 (2013).
doi: 10.1111/jeb.12040
pubmed: 23205963
Cheng, H. et al. Frequent intra- and inter-species introgression shapes the landscape of genetic variation in bread wheat. Genome Biol. 20, 136. https://doi.org/10.1186/s13059-019-1744-x (2019).
doi: 10.1186/s13059-019-1744-x
pubmed: 31300020
pmcid: 6624984
Hufford, M. B. et al. The genomic signature of crop-wild introgression in maize. PLoS Genet. 9, e1003477. https://doi.org/10.1371/journal.pgen.1003477 (2013).
doi: 10.1371/journal.pgen.1003477
pubmed: 23671421
pmcid: 3649989
Gonzalez-Segovia, E. et al. Characterization of introgression from the teosinte Zea mays ssp. mexicana to Mexican highland maize. PeerJ 7, e6815. https://doi.org/10.7717/peerj.6815 (2019).
doi: 10.7717/peerj.6815
pubmed: 31110920
pmcid: 6501764
Xia, H. B., Wang, W., Xia, H., Zhao, W. & Lu, B. R. Conspecific crop-weed introgression influences evolution of weedy rice (Oryza sativa f. spontanea) across a geographical range. PLoS ONE 6, e16189. https://doi.org/10.1371/journal.pone.0016189 (2011).
doi: 10.1371/journal.pone.0016189
pubmed: 21249201
pmcid: 3020953
Civán, P. & Brown, T. A. Role of genetic introgression during the evolution of cultivated rice (Oryza sativa L.). BMC Evol. Biol. 18, 57. https://doi.org/10.1186/s12862-018-1180-7 (2018).
doi: 10.1186/s12862-018-1180-7
pubmed: 29688851
pmcid: 5913815
Molnár-Láng, M. & Linc, G. Wheat-barley hybrids and introgression lines. In Alien Introgression in Wheat: Cytogenetics, Molecular Biology, and Genomics (eds Molnár-Láng, M. et al.) 315–345 (Springer, Berlin, 2015).
Pankin, A. & von Korff, M. Co-evolution of methods and thoughts in cereal domestication studies: a tale of barley (Hordeum vulgare). Curr. Opin. Plant Biol. 36, 15–21. https://doi.org/10.1016/j.pbi.2016.12.001 (2017).
doi: 10.1016/j.pbi.2016.12.001
pubmed: 28011443
Yan, H. et al. High-density marker profiling confirms ancestral genomes of Avena species and identifies D-genome chromosomes of hexaploid oat. Theor. Appl. Genet. 129, 2133. https://doi.org/10.1007/s00122-016-2762-7 (2016).
doi: 10.1007/s00122-016-2762-7
pubmed: 27522358
pmcid: 5069325
Liu, Q., Lin, L., Zhou, X., Peterson, P. M. & Wen, J. Unraveling the evolutionary dynamics of ancient and recent polyploidization events in Avena (Poaceae). Sci. Rep. 7, 41944. https://doi.org/10.1038/srep41944 (2017).
doi: 10.1038/srep41944
pubmed: 28157193
pmcid: 5291219
Martis, M. M. et al. Reticulate evolution of the rye genome. Plant Cell 25, 3685–3698. https://doi.org/10.1105/tpc.113.114553 (2013).
doi: 10.1105/tpc.113.114553
pubmed: 24104565
pmcid: 3877785
Hagenblad, J., Oliveira, H. R., Forsberg, N. E. G. & Leino, M. W. Geographical distribution of genetic diversity in Secale landrace and wild accessions. BMC Plant Biol. 16, 23. https://doi.org/10.1186/s12870-016-0710-y (2016).
doi: 10.1186/s12870-016-0710-y
pubmed: 26786820
pmcid: 4719562
Almaraj, V. A. & Balasundaram, N. On the taxonomy of the members of 'Saccharum complex’. Genet. Resour. Crop. Evol. 53, 35–41. https://doi.org/10.1007/s10722-004-0581-1 (2006).
doi: 10.1007/s10722-004-0581-1
Pachakkil, B. et al. Cytogenetic and agronomic characterization of intergeneric hybrids between Saccharum spp. hybrid and Erianthus arundinaceus. Sci. Rep. 9, 1748. https://doi.org/10.1038/s41598-018-38316-6 (2019).
doi: 10.1038/s41598-018-38316-6
pubmed: 30742000
pmcid: 6370852
Barnaud, A. et al. A weed-crop complex in sorghum: the dynamics of genetic diversity in a traditional farming system. Am. J. Bot. 96, 1869–1879. https://doi.org/10.3732/ajb.0800284 (2009).
doi: 10.3732/ajb.0800284
pubmed: 21622308
Ohadi, S., Hodnett, G., Rooney, W. & Bagavathiannan, M. Gene flow and its consequences in Sorghum spp. Crit. Rev. Plant Sci. 36, 367–385. https://doi.org/10.1080/07352689.2018.1446813 (2018).
doi: 10.1080/07352689.2018.1446813
Elshire, R. J. et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6, e19379. https://doi.org/10.1371/journal.pone.0019379 (2011).
doi: 10.1371/journal.pone.0019379
pubmed: 3087801
pmcid: 3087801
Hamlin, J. A. & Arnold, M. L. Determining population structure and hybridization for two iris species. Ecol. Evol. 4, 743–755. https://doi.org/10.1002/ece3.964 (2014).
doi: 10.1002/ece3.964
pubmed: 24683457
pmcid: 3967900
Qi, L. et al. Genotyping-by-sequencing uncovers the introgression alien segments associated with sclerotinia basal stalk rot resistance from wild species-I. Helianthus argophyllus and H. petiolaris. Frontiers in genetics 7, 219. https://doi.org/10.3389/fgene.2016.00219 (2016).
doi: 10.3389/fgene.2016.00219
pubmed: 28083014
pmcid: 5183654
Schilling, M. P., Gompert, Z., Li, F. W., Windham, M. D. & Wolf, P. G. Admixture, evolution, and variation in reproductive isolation in the Boechera puberula clade. BMC Evol. Biol. 18, 61. https://doi.org/10.1186/s12862-018-1173-6 (2018).
doi: 10.1186/s12862-018-1173-6
pubmed: 29699502
pmcid: 5921550
Edet, O. U., Gorafi, Y. S. A., Nasuda, S. & Tsujimoto, H. DArTseq-based analysis of genomic relationships among species of tribe Triticeae. Sci. Rep. 8, 16397. https://doi.org/10.1038/s41598-018-34811-y (2018).
doi: 10.1038/s41598-018-34811-y
pubmed: 30401925
pmcid: 6219600
Hodkinson, T. R., Perdereau, A., Klaas, M., Cormican, P. & Barth, S. Genotyping by sequencing and plastome analysis finds high genetic variability and geographical structure in Dactylis glomerata L. in Northwest Europe despite lack of ploidy variation. Agronomy 9, 342. https://doi.org/10.3390/agronomy9070342 (2019).
doi: 10.3390/agronomy9070342
Saarela, J. M. et al. A 250 plastome phylogeny of the grass family (Poaceae): Topological support under different data partitions. PeerJ 6, 4299. https://doi.org/10.7717/peerj.4299 (2018).
doi: 10.7717/peerj.4299
Soreng, R. J. et al. A worldwide phylogenetic classification of the Poaceae (Gramineae) II: An update and a comparison of two 2015 classifications. J. Syst. Evol. 55, 259–290. https://doi.org/10.1111/jse.12262 (2017).
doi: 10.1111/jse.12262
Tzvelev, N. N. Notulae de tribu Stipeae Dum. (fam. Poaceae) in URSS. Novosti Sistematiki Vyssih Rastenij 11, 4–20 (1974).
Nobis, M. Taxonomic revision of the Central Asiatic Stipa tianschanica complex (Poaceae) with particular reference to the epidermal micromorphology of the lemma. Folia Geobot. 49, 283–308. https://doi.org/10.1007/s12224-013-9164-2 (2014).
doi: 10.1007/s12224-013-9164-2
Nobis, M., Gudkova, P., Nowak, A., Sawicki, J. & Nobis, A. A revision of the genus Stipa (Poaceae) in Middle Asia, including a key to species identification, an annotated checklist and phytogeographic analysis. Ann. Mo. Bot. Gard. 105, 1–63. https://doi.org/10.3417/2019378 (2020).
doi: 10.3417/2019378
Hamasha, H. R., von Hagen, K. B. & Röser, M. Stipa (Poaceae) and allies in the Old World: molecular phylogenetics realigns genus circumscription and gives evidence on the origin of American and Australian lineages. Plant Syst. Evol. 298, 351–367. https://doi.org/10.1007/s00606-011-0549-5 (2012).
doi: 10.1007/s00606-011-0549-5
Romaschenko, K. et al. Systematics and evolution of the needle grasses (Poaceae: Pooideae: Stipeae) based on analysis of multiple chloroplast loci, ITS, and lemma micromorphology. Taxon 61, 18–44. https://doi.org/10.1002/tax.611002 (2012).
doi: 10.1002/tax.611002
Kellogg, E. A. Subfamily Pooideae. In The families and genera of vascular plants (ed. Kubitzki, K.) 199–229 (Springer, Berlin, 2015).
Yunatov, A. A. Main patterns of the vegetation cover of the Mongolian People’s Republic. Proc. Mongolian Commission 39, 233 (1950).
Dashnyam, B. Flora and vegetation of Eastern Mongolia 78–115 (Mongolian Academy of Sciences, Mongolia, 1974).
Lavrenko, E. M., Karamasheva, Z. V. & Nikulina, R. I. Eurasian steppe 143 (Nauka, Nauka, 1991).
Nowak, A., Nowak, S., Nobis, A. & Nobis, M. Vegetation of feather grass steppes in the western Pamir Alai Mountains (Tajikistan, Middle Asia). Phytocoenologia 46, 295–315. https://doi.org/10.1127/phyto/2016/0145 (2016).
doi: 10.1127/phyto/2016/0145
Danzhalova, E. V. et al. Indicators of Pasture Digression in Steppe Ecosystems of Mongolia. Explor. into Biol. Resour. Mong. 12, 297–306 (2012).
Yang, Y. Q. et al. Transcriptome analysis reveals diversified adaptation of Stipa purpurea along a drought gradient on the Tibetan Plateau. Funct. Integr. Genomics 15, 295–307. https://doi.org/10.1007/s10142-014-0419-7 (2015).
doi: 10.1007/s10142-014-0419-7
pubmed: 25471470
Lv, X., He, Q. & Zhou, G. Contrasting responses of steppe Stipa ssp. to warming and precipitation variability. Ecol. Evol. 9, 9061–9075. https://doi.org/10.1002/ece3.5452 (2019).
doi: 10.1002/ece3.5452
pubmed: 31463004
pmcid: 6706196
Schubert, M., Grønvold, L., Sandve, S. R., Hvidsten, T. R. & Fjellheim, S. Evolution of cold acclimation and its role in niche transition in the temperate grass subfamily pooideae. Plant Physiol. 180, 404–419. https://doi.org/10.1104/pp.18.01448 (2019).
doi: 10.1104/pp.18.01448
pubmed: 30850470
pmcid: 6501083
Maevsky, V. V. & Amerkhanov, H. H. The note of Poaceae species from former USSR flora, recommended as fodder for agricultural production. Bull. Bot. Garden Saratov State Univ. 6, 80–83 (2007).
Brunetti, G., Soler-Rovira, P., Farrag, K. & Senesi, N. Tolerance and accumulation of heavy metals by wild plant species grown in contaminated soils in Apulia region, Southern Italy. Plant Soil. 318, 285–298. https://doi.org/10.1007/s11104-008-9838-3 (2009).
doi: 10.1007/s11104-008-9838-3
Smirnov, P. A. Stiparum Armeniae minus cognitarum descriptiones. Byull. Moskovsk. Obshch. Isp. Prir. Otd. Biol. 75, 113–115 (1970).
Tzvelev, N. N. Zlaki USSR (Nauka Press, Nauka, 1976).
Kotukhov, Y. A. Synopsis of feather grass (Stipa L.) and false needlegrasses (Ptilagrostis Griseb.) the eastern of Kazakhstan (The Kazakh Altai, Zaisan valley and Prialtayskie ranges). Botanicheskie Issledovaniya Sibiri i Kazakhstana 8, 3–16 (2002).
Nobis, M. Taxonomic revision of the Stipa lipskyi group (Poaceae: Stipa section Smirnovia) in the Pamir Alai and Tian-Shan Mountains. Plant Syst. Evol. 299, 1307–1354. https://doi.org/10.1007/s00606-013-0799-5 (2013).
doi: 10.1007/s00606-013-0799-5
Nobis, M. et al. Hybridisation, introgression events and cryptic speciation in Stipa (Poaceae): a case study of the Stipa heptapotamica hybrid-complex. Perspect. Plant Ecol. Evol. Syst. 39, 125457. https://doi.org/10.1016/j.ppees.2019.05.001 (2019).
doi: 10.1016/j.ppees.2019.05.001
Nobis, M. & Gudkova, P. D. Taxonomic notes on feather grasses (Poaceae: Stipa) from eastern Kazakhstan with typification of seven names and one new combination. Phytotaxa 245, 31–42. https://doi.org/10.11646/phytotaxa.245.1.3 (2016).
doi: 10.11646/phytotaxa.245.1.3
Nobis, M. et al. Stipa ×fallax (Poaceae: Pooideae: Stipeae), a new natural hybrid from Tajikistan, and a new combination in Stipa drobovii. Phytotaxa 303, 141–154. https://doi.org/10.11646/phytotaxa.303.2.4 (2017).
doi: 10.11646/phytotaxa.303.2.4
Tzvelev, N. N. Some notes on the grasses (Poaceae) of the Caucasus. Botanical Zhurnal 78, 83–95 (1993).
Krawczyk, K., Nobis, M., Nowak, A., Szczecińska, M. & Sawicki, J. Phylogenetic implications of nuclear rRNA IGS variation in Stipa L. (Poaceae). Sci. Rep. 7, 11506. https://doi.org/10.1038/s41598-017-11804-x (2017).
doi: 10.1038/s41598-017-11804-x
pubmed: 28912548
pmcid: 5599551
Krawczyk, K., Nobis, M., Myszczyński, K., Klichowska, E. & Sawicki, J. Plastid superbarcodes as a tool for species discrimination in feather grasses (Poaceae: Stipa). Sci. Rep. 8, 1924. https://doi.org/10.1038/s41598-018-20399-w (2018).
doi: 10.1038/s41598-018-20399-w
pubmed: 29386579
pmcid: 5792575
Gudkova, P. D., Olonova, M. V. & Feoktisov, D. S. The comparison of ecologo-climatic niches of two species feather grass Stipa sareptana A.K. Becker and S. krylovii Roshev. (Poaceae). Ukrainian J. Ecol. 7, 263–269. https://doi.org/10.15421/2017_115 (2017).
doi: 10.15421/2017_115
Lu, S. L. & Wu, Z. L. On the geographical distribution of the genus Stipa L., China. Acta Phytotaxon. Sin. 34, 242–253 (1996).
Wu, Z. L. & Phillips, S. M. Stipa. In Flora of China (eds Wu, Z. Y. et al.) 196–203 (Science Press, Beijing, 2006).
Olonova, M. V., Barkworth, M. E. & Gudkova, P. D. Lemma micromorphology and the systematics of Siberian species of Stipa (Poaceae). Nordic J. Bot. 34, 319–328. https://doi.org/10.1111/njb.00881 (2016).
doi: 10.1111/njb.00881
Barkworth, M. E. & Everett, J. Evolution in the Stipeae: identification and relationships of its monophyletic taxa. In Grass systematics and evolution (eds Soderstrom, T. R. et al.) 251–264 (Smithsonian Institution Press, Washington, 1987).
Xia, L. et al. DArT for high-throughput genotyping of cassava (Manihot esculenta) and its wild relatives. Theor. Appl. Genetics 110, 1092–1098. https://doi.org/10.1007/s00122-005-1937-4 (2005).
doi: 10.1007/s00122-005-1937-4
Akbari, M. et al. Diversity arrays technology (DArT) for high-throughput profiling of the hexaploid wheat genome. Theor. Appl. Genetics 113, 1409–1420. https://doi.org/10.1007/s00122-006-0365-4 (2006).
doi: 10.1007/s00122-006-0365-4
Mace, E. S. et al. DArT markers: diversity analyses and mapping in Sorghum bicolor. BMC Genom. 9, 26. https://doi.org/10.1186/1471-2164-9-26 (2008).
doi: 10.1186/1471-2164-9-26
Simko, I., Eujayl, I. & van Hintum, T. J. Empirical evaluation of DArT, SNP, and SSR marker-systems for genotyping, clustering, and assigning sugar beet hybrid varieties into populations. Plant Sci. 184, 54–62. https://doi.org/10.1016/j.plantsci.2011.12.009 (2012).
doi: 10.1016/j.plantsci.2011.12.009
pubmed: 22284710
Alam, M., Neal, J., O’Connor, K., Kilian, A. & Topp, B. Ultra-high-throughput DArTseq-based silicoDArT and SNP markers for genomic studies in macadamia. PLoS ONE 13, e0203465. https://doi.org/10.1371/journal.pone.0203465 (2018).
doi: 10.1371/journal.pone.0203465
pubmed: 30169500
pmcid: 6118395
Abu Zaitoun, S. Y., Jamous, R. M., Shtaya, M. J., Eid, I. S. & Ali-Shtayeh, M. S. Characterizing Palestinian snake melon (Cucumis melo var flexuosus) germplasm diversity and structure using SNP and DArTseq markers. BMC Plant Biol. 18, 246. https://doi.org/10.1186/s12870-018-1475-2 (2018).
doi: 10.1186/s12870-018-1475-2
pubmed: 30340523
pmcid: 6194588
Bello, E. B. et al. Genetic diversity analysis of selected sugarcane (Saccharum spp. hybrids) varieties using DArT-Seq technology. Philippine J. Sci. 148, 103–114 (2019).
Rutherford, S. et al. Speciation in the presence of gene flow: population genomics of closely related and diverging Eucalyptus species. Heredity 121, 126–141. https://doi.org/10.1038/s41437-018-0073-2 (2018).
doi: 10.1038/s41437-018-0073-2
pubmed: 29632325
pmcid: 6039520
Ivanizs, L. et al. Unlocking the genetic diversity and population structure of a wild gene source of wheat, Aegilops biuncialis Vis., and its relationship with the heading time. Front Plant Sci. 10, 1531. https://doi.org/10.3389/fpls.2019.01531 (2019).
doi: 10.3389/fpls.2019.01531
pubmed: 31824545
pmcid: 6882925
Yu, J., Jing, Z. B. & Cheng, J. M. Genetic diversity and population structure of Stipa bungeana, an endemic species in Loess Plateau of China, revealed using combined ISSR and SRAP markers. Genet. Mol. Res. 13, 1097–1108. https://doi.org/10.4238/2014.February.20.11 (2014).
doi: 10.4238/2014.February.20.11
pubmed: 24634131
Kopylov-Guskov, Y. O. & Kramina, T. E. Investigating of Stipa ucrainica и Stipa zalesskii (Poaceae) from Rostov Oblast using morphological and ISSR analyses. Bull. Moscow Soc. Nat. Biol. Ser. 119, 46–53 (2014).
Boussaid, M., Benito, C., Harche, M., Naranjo, T. & Zedek, M. Genetic variation in natural populations of Stipa tenacissima from Algeria. Biochem. Genet. 48, 857–872. https://doi.org/10.1007/s10528-010-9367-7 (2010).
doi: 10.1007/s10528-010-9367-7
pubmed: 20652395
Zhao, N. X., Gao, Y. B., Wang, J. L. & Ren, A. Z. Genetic diversity and population differentiation of the dominant species Stipa krylovii in the Inner Mongolia Steppe. Biochem. Genet. 44, 513–526. https://doi.org/10.1007/s10528-006-9054-x (2006).
doi: 10.1007/s10528-006-9054-x
pubmed: 17143720
Zhao, N. X., Gao, Y. B., Wang, J. L., Ren, A. Z. & Xu, H. RAPD diversity of Stipa grandis populations and its association with some ecological factors. Acta Ecol. Sin. 26, 1312–1319. https://doi.org/10.1016/S1872-2032(06)60023-1 (2006).
doi: 10.1016/S1872-2032(06)60023-1
Thiers, B. Index Herbariorum: a Global Directory of Public Herbaria and Associated Staff. New York Botanical Garden’s Virtual Herbarium https://sweetgumnybg.org/science/ih (2018).
WCSP. World Checklists of Selected Plant Families https://wcsp.science.kew.org/home.do (2019).
Sokal, R. R. & Sneath, P. H. A. Principles of Numerical Taxonomy (W.H. Freeman, San Francisco, 1963).
Korkmaz, S., Goksuluk, D. & Zararsiz, G. Mvn: an r package for assessing multivariate normality. R J. 6, 151–162. https://doi.org/10.32614/rj-2014-031 (2014).
doi: 10.32614/rj-2014-031
Pagès, J. Analyse Factorielle de Donnees Mixtes. Revue Statistique Appliquee 4, 93–111 (2004).
Husson, F., Josse, J., Le, S. & Mazet, J. FactoMineR: multivariate exploratory data analysis and data mining https://factominer.free.fr (2015).
Cattell, R. B. The scree test for the number of factors. Multivariate Behav Res. 1, 245–276 (1966).
doi: 10.1207/s15327906mbr0102_10
Kassambara, A. Factoextra: Extract and Visualize the Results of Multivariate Data Analyses https://rdrr.io/cran/factoextra (2015).
Sievert, C. et al. plotly: create interactive web graphics via 'plotly.js' https://rdrr.io/cran/plotly (2017).
Wickham, H. ggplot2: elegant graphics for data analysis (Springer, New York, https://ggplot2.tidyverse.org (2016).
Sansaloni, C. et al. Diversity arrays technology (DArT) and next-generation sequencing combined: genome-wide, high throughput, highly informative genotyping for molecular breeding of Eucalyptus. BMC Proc. 5, 54. https://doi.org/10.1186/1753-6561-5-S7-P54 (2011).
doi: 10.1186/1753-6561-5-S7-P54
Kilian, A. et al. Diversity arrays technology: a generic genome profiling technology on open platforms. Methods Mol. Biol. 888, 67–89. https://doi.org/10.1007/978-1-61779-870-2_5 (2012).
doi: 10.1007/978-1-61779-870-2_5
pubmed: 22665276
Courtois, B. et al. Genome-wide association mapping of root traits in a Japonica rice panel. PLoS ONE 8, e78037. https://doi.org/10.1371/journal.pone.0078037 (2013).
doi: 10.1371/journal.pone.0078037
pubmed: 24223758
pmcid: 3818351
Cruz, V. M. V., Kilian, A. & Dierig, D. A. Development of DArT marker platforms and genetic diversity assessment of the US collection of the new oilseed crop lesquerella and related species. PLoS ONE 8, e64062. https://doi.org/10.1371/journal.pone.0064062 (2013).
doi: 10.1371/journal.pone.0064062
pubmed: 23724020
pmcid: 3665832
Raman, H. et al. Genome-wide delineation of natural variation for pod shatter resistance in Brassica napus. PLoS ONE 9, e101673. https://doi.org/10.1371/journal.pone.0101673 (2014).
doi: 10.1371/journal.pone.0101673
pubmed: 25006804
pmcid: 4090071
Gruber, B., Georges, A., Berry, O. & Unmack, P. dartR: importing and analysing snp and Silicodart data generated by genome-wide restriction fragment analysis https://cran.rproject.org/web/packages/dartR/index.html (2017).
Raj, A., Stephens, M. & Pritchard, J. K. fastSTRUCTURE: variational inference of population structure in large SNP data sets. Genetics 197, 573–589. https://doi.org/10.1534/genetics.114.164350 (2014).
doi: 10.1534/genetics.114.164350
pubmed: 24700103
pmcid: 4063916
RStudio Team. RStudio: Integrated Development for R www.rstudio.com (2016).
Burgarella, C. et al. Detection of hybrids in nature: application to oaks (Quercus suber and Q. ilex). Heredity 102, 442–452. https://doi.org/10.1038/hdy.2009.8 (2009).
doi: 10.1038/hdy.2009.8
pubmed: 19240752
Winkler, K. A., Pamminger-Lahnsteiner, B., Wanzenböck, J. & Weiss, S. Hybridization and restricted gene flow between native and introduced stocks of Alpine whitefish (Coregonus sp.) across multiple environments. Mol. Ecol. 20, 456–472. https://doi.org/10.1111/j.1365-294X.2010.04961.x (2011).
doi: 10.1111/j.1365-294X.2010.04961.x
pubmed: 21199024
pmcid: 3045663
Dierking, J. et al. Anthropogenic hybridization between endangered migratory and commercially harvested stationary whitefish taxa (Coregonus spp.). Evol. Appl. 7, 1068–1083. https://doi.org/10.1111/eva.12166 (2014).
doi: 10.1111/eva.12166
pubmed: 25553068
pmcid: 4231596
Malde, K. et al. Whole genome resequencing reveals diagnostic markers for investigating global migration and hybridization between minke whale species. BMC Genom. 18, 76. https://doi.org/10.1186/s12864-016-3416-5 (2017).
doi: 10.1186/s12864-016-3416-5
Beugin, M. P., Gayet, T., Pontier, D., Devillard, S. & Jombart, T. A fast likelihood solution to the genetic clustering problem. Methods Ecol. Evol. 9, 1006–1016. https://doi.org/10.1111/2041-210X.12968 (2018).
doi: 10.1111/2041-210X.12968
pubmed: 29938015
pmcid: 5993310
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2019).
Li, H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics 34, 3094–3100. https://doi.org/10.1093/bioinformatics/bty191 (2018).
doi: 10.1093/bioinformatics/bty191
pubmed: 29750242
pmcid: 6137996
Schlüter, P. M. & Harris, S. A. Analysis of multilocus fingerprinting data sets containing missing data. Mol. Ecol. Notes 6, 569–572. https://doi.org/10.1111/j.1471-8286.2006.01225.x (2006).
doi: 10.1111/j.1471-8286.2006.01225.x
Rambaut, A. Figtree v1.4.4 https://tree.bio.ed.ac.uk/software/figtree (2018).