The genetic diversity and population structure of Sophora alopecuroides (Faboideae) as determined by microsatellite markers developed from transcriptome

Autoři: Yuan Wang aff001;  Tingting Zhou aff001;  Daihan Li aff001;  Xuhui Zhang aff001;  Wanwen Yu aff001;  Jinfeng Cai aff001;  Guibin Wang aff001;  Qirong Guo aff001;  Xiaoming Yang aff001;  Fuliang Cao aff001
Působiště autorů: Co-Innovation Center for Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing, China aff001
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article


Sophora alopecuroides (Faboideae) is an endemic species, mainly distributed in northwest China. However, the limited molecular markers range for this species hinders breeding and genetic studies. A total of 20,324 simple sequence repeat (SSR) markers were identified from 118,197 assembled transcripts and 18 highly polymorphic SSR markers were used to explore the genetic diversity and population structure of S. alopecuroides from 23 different geographical populations. A relatively low genetic diversity was found in S. alopecuroides based on mean values of the number of effective alleles (Ne = 1.81), expected heterozygosity (He = 0.39) and observed heterozygosity (Ho = 0.55). The results of AMOVA indicated higher levels of variation within populations than between populations. Bayesian-based cluster analysis, principal coordinates analysis and Neighbor-Joining phylogeny analysis roughly divided all genotypes into four major groups with some admixtures. Meanwhile, geographic barriers would have restricted gene flow between the northern and southern regions (separated by Tianshan Mountains), wherein the two relatively ancestral and independent clusters of S. alopecuroides occur. History trade and migration along the Silk Road would together have promoted the spread of S. alopecuroides from the western to the eastern regions of the northwest plateau in China, resulting in the current genetic diversity and population structure. The transcriptomic SSR markers provide a valuable resource for understanding the genetic diversity and population structure of S. alopecuroides, and will assist effective conservation management.

Klíčová slova:

Conservation genetics – Genetic polymorphism – Microsatellite loci – Phylogeography – Population genetics – Sequence databases – Species diversity – Transcriptome analysis


1. Zhao L, Deng Z, Yang W, Cao Y, Wang E, Wei G. Diverse rhizobia associated with Sophora alopecuroides grown in different regions of Loess Plateau in China. Syst Appl Microbiol. 2010; 33: 468–77. doi: 10.1016/j.syapm.2010.08.004 20965680

2. Wang H, Guo S, Qian D, Qian Y, Duan JA. Comparative analysis of quinolizidine alkaloids from different parts of Sophora alopecuroides seeds by UPLC-MS/MS. J Pharm Biomed Anal. 2012; 67–68: 16–21. doi: 10.1016/j.jpba.2012.04.024 22613581

3. Lee ST, Cook D, Molyneux RJ, Marcolongo-Pereira C, Stonecipher CA, Gardner DR. The alkaloid profiles of Sophora nuttalliana and Sophora stenophylla. Biochem Syst Eco. 2013; 48: 58–64.

4. Fu YB. Understanding crop genetic diversity under modern plant breeding. Theor Appl Genet. 2015; 128: 2131–42. doi: 10.1007/s00122-015-2585-y 26246331

5. Liu ZM, Zhao AM, Kang XY, Zhou SL, Lopez-Pujol J. Genetic diversity, population structure, and conservation of Sophora moorcroftiana (Fabaceae), a shrub endemic to the Tibetan Plateau. Plant Biol. 2006; 8: 81–92. doi: 10.1055/s-2005-872889 16435272

6. Pometti CL, Bessega CF, Vilardi JC, Ewens M, Saidman BO. Genetic variation in natural populations of Acacia visco (Fabaceae) belonging to two sub-regions of Argentina using AFLP. Plant Syst Evol. 2016; 302: 901–910.

7. Fan DM, Yue JP, Nie ZL, Li ZM, Comes HP, Sun H. Phylogeography of Sophora davidii (Leguminosae) across the ‘Tanaka-Kaiyong Line’, an important phytogeographic boundary in Southwest China. Mol Ecol. 2013; 22: 4270–4288. doi: 10.1111/mec.12388 23927411

8. Guo Q, Wang JX, Su LZ, Lv W, Sun YH, Li Y. Development and evaluation of a novel set of EST-SSR markers based on transcriptome sequences of Black Locust (Robinia pseudoacacia L.). Genes. 2017; 8: 177.

9. Osorio CE, Udall JA, Salvo-Garrido H, Maureira-Butler IJ. Development and characterization of InDel markers for Lupinus luteus L. (Fabaceae) and cross-species amplification in other Lupin species. Electoron J Biotechn. 2018; 31: 44–47.

10. Zou X, Shi C, Austin RS, Merico D, Munholland S, Marsolais F, et al. Genome-wide single nucleotide polymorphism and Insertion-Deletion discovery through next-generation sequencing of reduced representation libraries in common bean. Mol Breeding. 2013; 33: 769–778.

11. Ma T, Yan H, Shi X, Liu B, Ma Z, Zhang X. Comprehensive evaluation of effective constituents in total alkaloids from Sophora alopecuroides L. and their joint action against aphids by laboratory toxicity and field efficacy. Ind Crop Prod. 2018; 111: 149–157.

12. Huang YX, Wang G, Zhu JS, Zhang R, Zhang J. Traditional uses, phytochemistry, and pharmacological properties of Sophora alopecuroides L. Eur J Inflamm. 2016; 14: 128–132.

13. Zhao L, Xu Y, Sun R, Deng Z, Yang W, Wei G. Identification and characterization of the endophytic plant growth prompter Bacillus Cereus strain mq23 isolated from Sophora Alopecuroides root nodules. Braz J Microbiol. 2011; 42: 567–575. doi: 10.1590/S1517-838220110002000022 24031669

14. Kalia RK, Rai MK, Kalia S, Singh R, Dhawan AK. Microsatellite markers: an overview of the recent progress in plants. Euphytica. 2010; 177: 309–334.

15. Agarwal M, Shrivastava N, Padh H. Advances in molecular marker techniques and their applications in plant sciences. Plant Cell Rep. 2008; 27: 617–31. doi: 10.1007/s00299-008-0507-z 18246355

16. Zalapa JE, Cuevas H, Zhu H, Steffan S, Senalik D, Zeldin E, et al. Using next-generation sequencing approaches to isolate simple sequence repeat (SSR) loci in the plant sciences. Am J Bot. 2012, 99, 193–208. doi: 10.3732/ajb.1100394 22186186

17. Xu M, Li Z, Wang J, Liu S, Cai H. RNA sequencing and SSR marker development for genetic diversity research in Woonyoungia septentrionalis (Magnoliaceae). Conserv Genet Resour. 2017; 10: 867–872.

18. Li Z, Zhong Y, Yu F, Xu M. Novel SSR marker development and genetic diversity analysis of Cinnamomum camphora based on transcriptome sequencing. Plant Genet Resour. 2018; 16: 568–571.

19. Jhanwar S, Priya P, Garg R, Parida S K, Tyagi A K, Jain M. Transcriptome sequencing of wild chickpea as a rich resource for marker development. Plant Biotechnol J. 2012; 10: 690–702. doi: 10.1111/j.1467-7652.2012.00712.x 22672127

20. Wong QN, Tanzi AS, Ho WK, Malla S, Blythe M, Karunaratne A, et al. Development of gene-based SSR markers in Winged Bean (Psophocarpus tetragonolobus (L.) DC.) for diversity assessment. Genes. 2017; 8: 100.

21. Wang JX, Lu C, Yuan CQ, Cui BB, Qiu QD, Sun P, et al. Characterization of ESTs from black locust for gene discovery and marker development. Genet Mol Res. 2015; 14: 12684–91. doi: 10.4238/2015.October.19.12 26505419

22. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014; 30: 2114–20. doi: 10.1093/bioinformatics/btu170 24695404

23. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013; 8: 1494–1512. doi: 10.1038/nprot.2013.084 23845962

24. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009; 10: 421. doi: 10.1186/1471-2105-10-421 20003500

25. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM et al. Gene Ontology: tool for the unification of biology. Nat Genet. 2000; 25:25–29 doi: 10.1038/75556 10802651

26. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. Blast2GO: a universal tool for visualization and analysis in functional genomics research. Bioinformatics. 2005; 21:3674–3676 doi: 10.1093/bioinformatics/bti610 16081474

27. Ye J, Zhang Y, Cui H, Liu J, Wu Y, Cheng Y, et al. WEGO 2.0: a web tool for analysing and plotting GO annotations, 2018 update. Nucleic Acids Res. 2018; 46:71–75.

28. Peakall R, Smouse PE. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics. 2012; 28: 2537–2539. doi: 10.1093/bioinformatics/bts460 22820204

29. Excoffier L, Lischer HEL. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010; 10: 564–567. doi: 10.1111/j.1755-0998.2010.02847.x 21565059

30. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000; 155: 945–959. 10835412

31. Earl DA, VonHoldt BM. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour. 2011; 4: 359–361.

32. Jakobsson M, Rosenberg NA. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics. 2007; 23: 1801. doi: 10.1093/bioinformatics/btm233 17485429

33. Rosenberg NA. distruct: a program for the graphical display of population structure. Mol Ecol Notes. 2010; 4: 137–138.

34. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013; 30: 2725–2729. doi: 10.1093/molbev/mst197 24132122

35. Cornuet JM, Luikart G. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics. 1996; 144: 2001–2014. 8978083

36. Piry S, Luikart G, Cornuet J. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J Hered. 1999; 90: 502–503.

37. Ockendon NF, O’Connell LA, Bush SJ, Monzón-Sandoval J, Barnes H, Székely T, et al. Optimization of next-generation sequencing transcriptome annotation for species lacking sequenced genomes. Mol Ecol Resour. 2016; 16: 446–458. doi: 10.1111/1755-0998.12465 26358618

38. Li H, Yao W, Fu Y, Li S, Guo Q. De novo assembly and discovery of genes that are involved in drought tolerance in Tibetan Sophora moorcroftiana. PloS One. 2015; 10: e111054. doi: 10.1371/journal.pone.0111054 25559297

39. Sonnet H, Carpendale S, Strothotte T. Long microsatellite alleles in drosophila melanogaster have a downward mutation bias and short. Genetics. 2000; 155: 1213. 10880482

40. Hamrick JL, Godt MJW. Effects of life history traits on genetic diversity in plant species. Phlos T R Soc B. 1996; 351: 1291–1298.

41. Masmoudi MB, Chaoui L, Topçu NE, Hammami P, Kara MH, Aurelle D. Contrasted levels of genetic diversity in a benthic Mediterranean octocoral: Consequences of different demographic histories? Ecol Evol. 2016; 6: 8665–8678. doi: 10.1002/ece3.2490 28035258

42. Heenan P, Mitchell C, Houliston G. Genetic variation and hybridisation among eight species of kōwhai (Sophora: Fabaceae) from New Zealand revealed by microsatellite markers. Genes. 2018; 9: 111.

43. Shu WJ, Tang Jm, Chen ZY, Jiang YS, Wang ZF, Wei X. Analysis of genetic diversity and population structure in Sophora japonica Linn. in China with newly developed SSR markers. Plant Mol Biol Rep. 2019; 37: 87–97.

44. Tectonophysics AW, Kelly D, Ladley JJ. Futile Selfing in the Trees Fuchsia excorticata (Onagraceae) and Sophora microphylla (Fabaceae): inbreeding depression over 11 years. Int J Plant Sci. 2011; 172: 191–198.

45. Hoskin CJ, Higgie M, Mcdonald KR, Moritz C. Reinforcement drives rapid allopatric speciation. Nature. 2005; 437: 1353–1356. doi: 10.1038/nature04004 16251964

46. Yang X, Li H, Yu H, Chai L, Xu Q, Deng X. Molecular phylogeography and population evolution analysis of Citrus ichangensis (Rutaceae). Tree Genet Genomes. 2017; 13: 29.

47. Orr HA. Dobzhansky, Bateson, and the genetics of speciation. Genetics. 1996; 144: 1331–1335. 8978022

48. Ma SM, Zhang ML, Sanderson SC. Phylogeography of the rare Gymnocarpos przewalskii (Caryophyllaceae): indications of multiple glacial refugia in northwestern China. Aust J Bot. 2012; 60: 20–31.

49. Sun JM. Source regions and formation of the Loess sediments on the high mountain regions of northwestern China. Quaternary Res. 2002; 58: 341–351.

50. Du ZY, Wang QF. Allopatric divergence of Stuckenia filiformis (Potamogetonaceae) on the Qinghai-Tibet Plateau and its comparative phylogeography with S. pectinata in China. Sci Rep, 2016; 6: 20883. doi: 10.1038/srep20883 26864465

51. Spengler RN. Fruit from the Sands: The Silk Road origins of the foods we eat. University of California Press. 2019.

52. Frankham R. Challenges and opportunities of genetic approaches to biological conservation. Biol Conserv. 2010; 143: 1919–1927.

53. Yang X, Yang Z, Li H. Genetic diversity, population genetic structure and protection strategies for Houpoëa officinalis (Magnoliaceae), an endangered Chinese medical plant. J Plant Biol. 2018; 61: 159–168.

Článek vyšel v časopise


2019 Číslo 12
Nejčtenější tento týden