Morphological and molecular evidence for natural hybridization between Sorbus pohuashanensis and S. discolor (Rosaceae)

doi:10.1007/s11676-023-01659-6

Abstract

Abstract:

In overlapping distribution areas of Sorbus pohuashanensis and S. discolor in North China (Mount Tuoliang, Mount Xiling and Mount Baihua), Sorbus individuals were found with pink fruit, which have never been recorded for the flora of China. Fourteen morphological characters combined with four chloroplast DNA markers and internal transcribed spacer (ITS) were used to analyze the origin of the Sorbus individuals with pink fruits and their relationship to S. pohuashanensis and S. discolor. PCA, SDA and one-way (taxon) ANOVA of morphological characters provided convincing evidence of the hybrid origin of Sorbus individuals with pink fruits based on a novel morphological character and many intermediate characters. Haplotype analysis based on four cpDNA markers showed that either S. pohuashanensis or S. discolor were maternal parents of Sorbus individuals with pink fruits. Incongruence of the position of Sorbus individuals with pink fruits between cpDNA and ITS in cluster trees supported by DNA sequence comparative analysis, implying former hybridization events between S. pohuashanensis and S. discolor. Multiple hybridization events between S. pohuashanensis and S. discolor might have contributed to the generation of Sorbus individuals with pink fruits. This study has provided insights into hybridization between species of the same genus in sympatric areas, which is of great significance for the study of interspecific hybridization.

Key words: Hybridization, ITS, Chloroplast DNA, Morphological characters, Sorbus

Yuxia Wu, Xuedan Yu, Wei Tang, Wenhua Yang, Qidi Fu, Yongqi Zheng, Chuanhong Zhang. Morphological and molecular evidence for natural hybridization between Sorbus pohuashanensis and S. discolor (Rosaceae)[J]. JOURNAL OF FORESTRY RESEARCH, 2024, 35(1): 25-.

Yuxia Wu, Xuedan Yu, Wei Tang, Wenhua Yang, Qidi Fu, Yongqi Zheng, Chuanhong Zhang. [J]. 林业研究(英文版), 2024, 35(1): 25-.

References 58

1	Aizawa M, Iwaizumi MG. Natural hybridization and introgression of Abies firma and Abies homolepis along the altitudinal gradient and genetic insights into the origin of Abies umbellata. Plant Species Biol, 2020, 35(2): 147-157, DOI
2	Areces-Berazain F, Wang YX, Hinsinger DD, Strijk JS. Plastome comparative genomics in maples resolves the infrageneric backbone relationships. PeerJ, 2020, 8, DOI
3	Bandelt HJ, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol, 1999, 16(1): 37-48, DOI
4	Brochmann C, Borgen L, Stabbetorp OE. Multiple diploid hybrid speciation of the Canary Island endemic Argyranthemum sundingii (Asteraceae). Plant Syst Evol, 2000, 220(1): 77-92, DOI
5	Cho MS, Kim CS, Kim SH, Kim TO, Heo KI, Jun J, Kim SC. Molecular and morphological data reveal hybrid origin of wild Prunus yedoensis (Rosaceae) from Jeju Island, Korea: implications for the origin of the flowering cherry. Am J Bot, 2014, 101(11): 1976-1986, DOI
6	Coyne JA, Orr HA. Speciation, 2004 Sunderland Sinauer Associates
7	Ďurkovič J, Kardošová M, Čaňová I, Lagaňa R, Priwitzer T, Chorvát D Jr, Cicák A, Pichler V. Leaf traits in parental and hybrid species of Sorbus (ROSACEAE). Am J Bot, 2012, 99(9): 1489-1500, DOI
8	Emms SK, Arnold ML. The effect of habitat on parental and hybrid fitness: transplant experiments with Louisianan irises. Evolution, 1997, 51: 1112-1119, DOI
9	Felsenstein J. Phylogenies and the comparative method. Am Nat, 1985, 125(1): 1-15, DOI
10	Gross BL, Schwarzbach AE, Rieseberg LH. Origin (s) of the diploid hybrid species Helianthus deserticola (Asteraceae). Am J Bot, 2003, 90(12): 1708-1719, DOI
11	Hajrudinović A, Frajman B, Schönswetter P, Silajdžić E, Siljak-Yakovlev S, Bogunić F. Towards a better understanding of polyploid Sorbus (Rosaceae) from Bosnia and Herzegovina (Balkan Peninsula), including description of a novel, tetraploid apomictic species. Bot J Linn Soc, 2015, 178(4): 670-685, DOI
12	Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser, 1999, 41: 95-98
13	Hamilton MB. Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Mol Ecol, 1999, 8(3): 521-523
14	Hebda A, Kempf M, Wachowiak W, Pluciński B, Kauzal P, Zwijacz-Kozica T. Hybridization and introgression of native and foreign Sorbus tree species in unique environments of protected mountainous areas. AoB Plants, 2021, 13(1): 1-15, DOI
15	Huang JF, Xu R, Peng YQ. Research progress of interspecific hybridization in genus ficus. Biodivers Sci, 2019, 27(04): 457-467, in Chinese) DOI
16	Jiang YF, Yan R, Su X, Chen W, Sun K. Molecular evidence for bidirectional hybrid origin and Hippophae rhamnoides ssp. sinensis as the mainly maternal plant of the diploid hybrid H. goniocarpa (Elaeagnaceae). Bull Bot Res, 2014, 1: 32-36 (in Chinese)
17	Jiggins CD, Mallet J. Bimodal hybrid zones and speciation. Trends Ecol Evol, 2000, 15(6): 250-255, DOI
18	Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol, 2016, 33(7): 1870-1874, DOI
19	Lê S, Josse J, Husson F. FactoMineR: an R package for multivariate analysis. J Stat Softw, 2008, 25(1): 1-18, DOI
20	Levin J, Fay MF, Pellicer J, Hedrén M (2018) Multiple independent origins of intermediate species between Sorbus aucuparia and S. hybrida (Rosaceae) in the Baltic region. Nord J Bot, 36(12)
21	Li DZ, Gao LM, Li HT, Wang H, Ge XJ, Liu JQ, Chen ZD, Zhou SL, Chen SL, Yang JB, Fu CX, Zeng CX, Yan HF, Zhu YJ, Sun YS, Chen SY, Zhao L, Wang K, Yang T, Duan GW. Comparative analysis of a large dataset indicates that internal transcribed spacer (ITS) should be incorporated into the core barcode for seed plants. Proc Natl Acad Sci U S A, 2011, 108(49): 19641-19646, DOI
22	Li X, Wei GM, El-Kassaby YA, Fang YW. Hybridization and introgression in sympatric and allopatric populations of four oak species. BMC Plant Biol, 2021, 21(1): 1-14
23	Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinform, 2009, 25(11): 1451-1452, DOI
24	Ludwig S, Robertson A, Rich TCG. Breeding systems, hybridization and continuing evolution in Avon Gorge Sorbus. Ann Bot, 2013, 111(4): 563-575, DOI
25	McAllister H. The genus Sorbus: mountain ash and other rowans, 2005 Kew Royal Botanic Garden
26	Meyer N, Gregor T, Meierott L, Paule J. Diploidy suggests hybrid origin and sexuality in Sorbus subgen. Tormaria from Thuringia Central Germany. Plant Syst Evol, 2014, 300(10): 2169-2175, DOI
27	Morales-Briones DF, Liston A, Tank DC. Phylogenomic analyses reveal a deep history of hybridization and polyploidy in the Neotropical genus Lachemilla (Rosaceae). New Phytol, 2018, 218(4): 1668-1684, DOI
28	Németh C, Papp N, Nosková J, Höhn M. Speciation by triparental hybridization in genus Sorbus (Rosaceae). Biol Futur, 2020, 71(3): 209-222, DOI
29	Nobre LLM, Santos JDO, Leite R, Almeida C. Phylogenomic and single nucleotide polymorphism analyses revealed the hybrid origin of Spondias bahiensis (family anacardiaceae): de novo genome sequencing and comparative genomics. Genet Mol Biol, 2018, 41(4): 878-883, DOI
30	Nylander J. Mrmodeltest v2, 2004 Program distributed by the author, Evolutionary Biology Centre Uppsala University
31	Parisod C, Besnard G. Glacial in situ survival in the Western Alps and polytopic autopolyploidy in Biscutella laevigata L. (Brassicaceae). Mol Ecol, 2007, 16(13): 2755-2767, DOI
32	Park JS, Jin DP, Choi BH. Insights into genomic structure and evolutionary processes of coastal Suaeda species in East Asia using cpDNA, nDNA, and genome-wide SNPs. Sci Rep, 2020, 10(1): 1-11, DOI
33	Price DT, Rich TCG. One-way introgressive hybridisation between Sorbus aria and S. torminalis (Rosaceae) in southern Britain. Watsonia, 2007, 26(4): 419-432
34	R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Analysis, Vienna, Austria. Website https://www.R-project.org
35	Rieseberg LH, Buerkle CA. Genetic Mapping in Hybrid Zones. Am Nat, 2002, 159(S3): S36-S50, DOI
36	Rieseberg LH, Ellstrand NC, Arnold M. What can morphological and molecular marker tell us about plant hybridization. CRC Crit Rev Plant Sci, 1993, 12(3): 213-241
37	Robertson A, Sydes C. Sorbus pseudomeinichii a new endemic Sorbus (Rosaceae) microspecies from Arran. Scotland Watsonia, 2006, 26(1): 9-14
38	Robertson A, Newton AC, Ennos RA. Multiple hybrid origins, genetic diversity and population genetic structure of two endemic Sorbus taxa on the Isle of Arran. Scotland Mol Ecol, 2004, 13(1): 123-134, DOI
39	Robertson A, Rich T, Allen AM, Houston L, Roberts CAT, Bridle JR, Harris SA, Hiscock SJ. Hybridization and polyploidy as drivers of continuing evolution and speciation in Sorbus. Mol Ecol, 2010, 19(8): 1675-1690, DOI
40	Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol, 2012, 61(3): 539-542, DOI
41	Sennikov AN, Hjertson M, Salvesen PH. Atlas Florae Europaeae notes 27. Taxonomy of the Sorbus arranensis group (Rosaceae) in Norway, a hybrid aggregate between S. aria s. lato and S. aucuparia. Ann Bot Fenn, 2016, 53(1–2): 1-13, DOI
42	Taberlet P, Gielly L, Pautou G, Bouvet J. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol, 1991, 17(5): 1105-1109, DOI
43	Tang W, Yu XD, Zhang CH, Ye XM, Fu QD, Zheng YQ. Molecular evidence for maternal origin of Sorbus with pink fruits. For Res, 2016, 29(6): 834-838
44	Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res, 1997, 25(24): 4876-4882, DOI
45	Triplett JK, Clark LG. Hybridization in the temperate bamboos (Poaceae: Bambusoideae: Arundinarieae): a phylogenetic study using AFLPs and cpDNA sequence data. Syst Bot, 2021, 46(1): 48-69, DOI
46	Uhrinová V, Zozomová-Lihová J, Bernátová D, Paule J, Paule L, Gömöry D. Origin and genetic differentiation of pink-flowered Sorbus hybrids in the Western Carpathians. Ann Bot, 2017, 120(2): mcx013, DOI
47	Vaezi J, Arjmandi AA, Sharghi HR. Origin of Rosa × binaloudensis (Rosaceae), a new natural hybrid species from Iran. Phytotaxa, 2019, 411(1): 23-38, DOI
48	Van DT, Xu B, Gao XF. Molecular phylogeny and character evolution of Flemingia (Leguminosae, Papilionoideae, Phaseoleae, Cajaninae) inferred from three cpDNA and nrITS sequence data. Plant Syst Evol, 2021, 307(2): 1-17
49	Wang YG. Natural hybridization and speciation. Biodivers Sci, 2017, 25(6): 565-576, DOI
50	Wang ZF, Jiang YZ, Bi H, Lu ZQ, Ma YZ, Yang XY, Chen NN, Tian B, Liu BB, Mao XX, Ma T, DiFazio SP, Hu QJ, Abbott RJ, Liu JQ. Hybrid speciation via inheritance of alternate alleles of parental isolating genes. Mol Plant, 2021, 14(2): 208-222, DOI
51	Yockey RD, Pearson (2010) Spss demystified: a step by step approach. Pearson Schweiz Ag
52	Yousefzadeh H, Colagar AH, Yousefi E, Badbar M, Kozlowski G. Phylogenetic relationship and genetic differentiation of Populus caspica and Populus alba using cpDNA and ITS noncoding sequences. J Forestry Res, 2019, 30: 451-461, DOI
53	Yü TT, Lu LD (1974) Sorbus L. Flora Reipublicae Popularis Sinicae, 36: 283–344. (in Chinese)
54	Yuan JL, Yue JJ, Zhong YB, Wu XL, Gu XP. Genetic variation in distant and inbred hybridization progenies from three sympodial bamboo parent species. J Forestry Res, 2019, 30(4): 1323-1329, DOI
55	Zbiljić M, Lakušić B, Marčetić M, Bogdanović S, Lakušić D. Morphological and chemical evidence of Teucrium×rohlenae K. Malý (Lamiaceae), a new hybrid in Croatia. Acta Bot Croat, 2021, 80(1): 48-55, DOI
56	Zhang JL, Zhang CQ, Gao LM, Yang JB, Li HT. Natural hybridization origin of Rhododendron agastum (Ericaceae) in Yunnan, China: inferred from morphological and molecular evidence. J Plant Res, 2007, 120(3): 457-463, DOI
57	Zheng J, Zheng YQ, Zong YC, Li BJ. Phenotypic diversity of fruits and seeds in natural populations of Sorbus pohuashanensis. Zhiwu Yichuan Ziyuan Xuebao, 2009, 10(03): 385-391 (in Chinese)
58	Zheng SL, Tian XL, Huang CL, Wang LJ, Feng Y, Zhang JL. Molecular and morphological evidence for natural hybridization between Rhododendron decorum and R. delavayi (Ericaceae). Biodivers Sci, 2017, 5(6): 627, in Chinese) DOI

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