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Journal of Integrative Agriculture  2022, Vol. 21 Issue (10): 2833-2847    DOI: 10.1016/j.jia.2022.07.031
Special Issue: 油料作物合辑Oil Crops
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Linkage and association mapping of wild soybean (Glycine soja) seeds germinating under salt stress

SHI Mei-qi1, LIAO Xi-liang1, YE Qian1, ZHANG Wei1, LI Ya-kai1, Javaid Akhter BHAT1, KAN Gui-zhen1, YU De-yue1, 2

1 National Key Laboratory of Crop Genetics and Germplasm Enhancement, National Center for Soybean Improvement, Nanjing Agricultural University, Nanjing 210095, P.R.China

2 Innovative Center of Molecular Genetics and Evolution, School of Life Sciences, Guangzhou University, Guangzhou 510405, P.R.China

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摘要  盐分会损害大豆的萌发、生长和产量。萌发期是大豆生长发育的关键时期。野生大豆中含有许多抗性基因,是大豆遗传改良的宝贵资源。为了确定野生大豆在盐胁迫下种子萌发期间激活的遗传位点,本研究对两个群体的3个耐盐相关性状进行了筛选,其中一个是包含142个家系的大豆种间杂交群体,另一个是包含121份野生大豆材料的自然群体。利用3个耐盐指标的单核苷酸多态性(SNP)标记,在两个环境下通过连锁定位和全基因组关联研究(GWAS)检测到25个数量性状位点(QTLs),21个显著SNPs [-Log10(P)≥4.0]和24个潜在SNPs [3.5<-Log10(P)<4.0]。根据这些SNPs和QTLs鉴定出关键遗传区域。根据W05基因组的基因功能注释和盐诱导基因表达实时荧光定量PCR分析,选择GsAKR1作为野生大豆萌发阶段响应盐胁迫的候选基因。这些结果有助于确定野生大豆耐盐遗传网络,并为耐盐大豆的分子标记辅助选择提供依据。

Abstract  

Salinity threatens soybean germination, growth and production.  The germination stage is a key period in the life of soybean.  Wild soybean contains many genes related to stress resistance that are valuable resources for the genetic improvement of soybean.  To identify the genetic loci of wild soybean that are active during seed germination under salt stress, two populations, a soybean interspecific hybrid population comprising 142 lines and a natural population comprising 121 wild soybean accessions, were screened for three germination-related traits in this study.  By using single-nucleotide polymorphism (SNP) markers with three salt tolerance indices, 25 quantitative trait loci (QTLs), 21 significant SNPs (–log10(P)≥4.0) and 24 potential SNPs (3.5<–log10(P)<4.0) were detected by linkage mapping and a genome-wide association study (GWAS) in two environments.  The key genetic region was identified based on these SNPs and QTLs.  According to the gene functional annotations of the W05 genome and salt-induced gene expression qRT-PCR analysis, GsAKR1 was selected as a candidate gene that responded to salt stress at the germination stage in the wild soybean.  These results could contribute to determining the genetic networks of salt tolerance in wild soybean and will be helpful for molecular marker-assisted selection in the breeding of salt-tolerant soybean.

Keywords:  salt tolerance        wild soybean        QTLs        GWAS        GsAKR1  
Received: 05 January 2021   Accepted: 07 May 2021
Fund: This work was supported by the Natural Science Foundation of Jiangsu Province, China (BK20191313), the Fundamental Research Funds for the Central Universities, China (KYZ201705) and the Bioinformatics Center of Nanjing Agricultural University, China.
About author:  SHI Mei-qi, E-mail: 2018101133@njau.edu.cn; Correspondence KAN Gui-zhen, E-mail: kanguizhen@njau.edu.cn; YU De-yue, E-mail: dyyu@njau.edu.cn

Cite this article: 

SHI Mei-qi, LIAO Xi-liang, YE Qian, ZHANG Wei, LI Ya-kai, Javaid Akhter BHAT, KAN Gui-zhen, YU De-yue. 2022. Linkage and association mapping of wild soybean (Glycine soja) seeds germinating under salt stress. Journal of Integrative Agriculture, 21(10): 2833-2847.

Abdurakhmonov I Y, Abdukarimov A. 2008. Application of association mapping to understanding the genetic diversity of plant germplasm resources. International Journal of Plant Genomics, 2008, doi: 10.1155/2008/574927.
Acquaah G. 2015. Conventional plant breeding principles and techniques. In: Advances in Plant Breeding Strategies: Breeding, Biotechnology and Molecular Tools. Springer, Cham, Switzerland. pp. 115–158.
Akond M, Liu S, Schoener L, Anderson J A, Kantartzi S, Meksem K, Song Q, Wang D, Wen Z, Lightfoot D, Kassem A. 2013. SNP-Based genetic linkage map of soybean using the SoySNP6K Illumina Infinium BeadChip genotyping array. Journal of Plant Genome Sciences, 1, 80–89.
Andersson M S, Vicente M C. 2010. Gene Flow Between Crops and their Wild Relatives. Johns Hopkins University Press, Baltimore, Maryland, the United States. pp. 402–403.
Ashraf M, Foolad M R. 2013. Crop breeding for salt tolerance in the era of molecular markers and marker-assisted selection. Plant Breeding, 132, 10–20.
Carpentieri-Pipolo V, Pipolo A E, Abdel-Haleem H, Boerma H R, Sinclair T R. 2012. Identification of QTLs associated with limited leaf hydraulic conductance in soybean. Euphytica, 186, 679–686.
Chen H T, Cui S Y, Fu S X, Gai J Y, Yu D Y. 2008. Identification of quantitative trait loci associated with salt tolerance during seedling growth in soybean (Glycine max L.). Australian Journal of Agricultural Research, 59, 1086–1091.
Churchill G A, Doerge R W. 1994. Empirical threshold values for quantitative trait mapping. Genetics, 138, 963–971.
Concibido V, Vallee B L, Mclaird P, Pineda N, Meyer J, Hummel L, Yang J K, Wu K, Delannay X. 2003. Introgression of a quantitative trait locus for yield from Glycine soja into commercial soybean cultivars. Theoretical and Applied Genetics, 106, 575–582.
DeRose-Wilson L, Gaut B S. 2011. Mapping salinity tolerance during Arabidopsis thaliana germination and seedling growth. PLoS ONE, 6, e22832.
Do T D, Vuong T D, Dunn D, Clubb M, Valliyodan B, Patil G, Chen P Y, Xu D, Nguyen H T, Shannon J G. 2019. Identification of new loci for salt tolerance in soybean by high-resolution genome-wide association mapping. BMC Genomics, 20, 318.
Feng X, Feng P, Yu H, Yu X, Sun Q, Liu S, Minh T N, Chen J, Wang D, Zhang Q, Cao L, Zhou C, Li Q, Xiao J, Zhong S, Wang A, Wang L, Pan H, Ding X. 2020. GsSnRK1 interplays with transcription factor GsERF7 from wild soybean to regulate soybean stress resistance. Plant Cell & Environment, 43, 1192–1211.
Guan R, Qu Y, Guo Y, Yu L, Liu Y, Jiang J, Chen J, Ren Y, Liu G, Tian L, Jin L, Liu Z, Hong H, Chang R, Gilliham M, Qiu L. 2014. Salinity tolerance in soybean is modulated by natural variation in GmSALT3. The Plant Journal, 80, 937–950.
Hamwieh A, Xu D. 2008. Conserved salt tolerance quantitative trait locus (QTL) in wild and cultivated soybeans. Breeding Science, 58, 355–359.
Hu D Z, Zhang H R, Du Q, Hu Z B, Yang Z Y, Li X, Wang J, Huang F, Yu D Y, Wang H, Kan G Z. 2020. Genetic dissection of yield-related traits via genome-wide association analysis across multiple environments in wild soybean (Glycine soja Sieb. and Zucc.). Planta, 251, doi: 10.1007/s00425-019-03329-6.
Hyten D L, Song Q J, Zhu Y L, Choi I Y, Nelson R L, Costa J M, Specht J E, Shoemaker R C, Cregan P B. 2006. Impacts of genetic bottlenecks on soybean genome diversity. Proceedings of the National Academy of Sciences of Sciences of the United States of America, 103, 16666–16671.
Jia Q, Li M W, Zheng C, Xu Y, Sun S, Li Z, Wong F L, Song J, Lin W W, Li Q, Zhu Y, Liang K, Lin W, Lam H M. 2020. The soybean plasma membrane-localized cation/H(+)exchanger GmCHX20a plays a negative role under salt stress. Physiologia Plantarum, 171, 714–727.
Jin T, Sun Y, Shan Z, He J, Wang N, Gai J Y, Li Y. 2020. Natural variation in the promoter of GsERD15B affects salt tolerance in soybean. Plant Biotechnology Journal, 19, 1155–1169.
Jin T, Sun Y, Zhao R, Shan Z, Gai J Y, Li Y. 2019. Overexpression of peroxidase gene GsPRX9 confers salt tolerance in soybean. International Journal of Molecular Sciences, 20, doi: 10.3390/ijms20153745.
Kan G Z, Ning L H, Li Y K, Hu Z B, Zhang W, He X H, Yu D Y. 2016. Identification of novel loci for salt stress at the seed germination stage in soybean. Breeding Science, 66, 530–541.
Kan G Z, Zhang W, Yang W M, Ma D Y, Zhang D, Hao D R, Hu Z B, Yu D Y. 2015. Association mapping of soybean seed germination under salt stress. Molecular Genetics and Genomics, 290, 2147–2162.
Karikari B, Li S G, Bhat J A, Cao Y C, Kong J J, Yang J Y, Gai J Y, Zhao T J. 2019. Genome-wide detection of major and epistatic effect QTLs for seed protein and oil content in soybean under multiple environments using high-density bin map. International Journal of Molecular Sciences, 20, doi: 10.3390/ijms20040979.
King K E, Lauter N, Lin S F, Scott M P, Shoemaker R C. 2013. Evaluation and QTL mapping of phosphorus concentration in soybean seed. Euphytica, 189, 261–269.
Lee G A, Crawford G W, Liu L, Sasaki Y, Chen X. 2011. Archaeological soybean (Glycine max) in East Asia: Does size matter? PLoS ONE, 6, 26720.
Lee J D, Shannon J G, Vuong T D, Nguyen H T. 2009. Inheritance of salt tolerance in wild soybean (Glycine soja Sieb. and Zucc). Accession PI483463. Journal of Heredity, 100, 798–801.
Li Y. 2008. Effect of salt stress on seed germination and seedling growth of three salinity plants. Pakistan Journal of Biological Sciences, 11, 1268–1272.
Liang H Z, Yu Y L, Yang H Q, Xu L J, Dong W, Du H, Cui W W, Zhang H Y. 2014. Inheritance and QTL mapping of related root traits in soybean at the seedling stage. Theoretical and Applied Genetics, 127, 2127–2137.
Lipka A E, Tian F, Wang Q S, Peiffer J, Li M, Bradbury P J, Gore M A, Buckler E S, Zhang Z. 2012. GAPIT: Genome association and prediction integrated tool. Bioinformatics, 28, 2397–2399.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT method. Methods, 25, 402–408.
Long N V, Dolstra O, Malosetti M, Kilian B, Graner A, Visser R G F, van der Linden C G. 2013. Association mapping of salt tolerance in barley (Hordeum vulgare L.). Theoretical and Applied Genetics, 126, 2335–2351.
Merk H L, Yarnes S C, Deynze A V, Tong N, Menda N, Mueller L A, Mutschler M A, Loewen S A, Myers J R, Francis D M. 2012. Trait diversity and potential for selection indices based on variation among regionally adapted processing tomato germplasm. Journal of the American Society for Horticultural Science, 137, 427–437.
Van Ooijen J W. 2011. Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genetics Research, 93, 343–349.
Pathan M S, Lee J D, Shannon J G, Nguyen H T. 2007. Recent advances in breeding for drought and salt stress tolerance in soybean. In: Advances in Molecular Breeding Toward Drought and Salt Tolerant Crops. Springer, Dordrecht. pp. 739–773.
Phang T H, Shao G, Lam H M. 2008. Salt tolerance in soybean. Journal of Integrative Plant Biology, 50, 1196–1212.
Price A H. 2006. Believe it or not, QTLs are accurate! Trends in Plant Science, 11, 213–216.
Qi X P, Li M W, Xie M, Liu X, Ni M, Shao G, Song C, Kay-Yuen Yim A, Tao Y, Wong F L, Isobe S, Wong C F, Wong K S, Xu C, Li C, Wang Y, Guan R, Sun F, Fan G, Xiao Z, et al. 2014. Identification of a novel salt tolerance gene in wild soybean by whole-genome sequencing. Nature Communications, 5, 1–11.
Qiu P, Zhang W, Liu C, Jiang H, Li C, Fan H, Zeng Q, Hu G, Cheng Q. 2011. QTL identification of salt tolerance in germination stage of soybean. Legume Genomics Genetics, 2, 20–27.
Sengupta D, Naik D, Reddy A R. 2015. Plant aldo-keto reductases (AKRs) as multi-tasking soldiers involved in diverse plant metabolic processes and stress defense: A structure-function update. Journal of Plant Physiology, 179, 40–55.
Shen X J, Wang Y Y, Zhang Y X, Guo W, Jiao Y Q, Zhou X A. 2018. Overexpression of the wild soybean R2R3-MYB transcription factor GsMYB15 enhances resistance to salt stress and Helicoverpa armigera in transgenic Arabidopsis. International Journal of Molecular Sciences, 19, doi: 10.3390/ijms19123958.
Soto-Cerda B J, Cloutier S. 2012. Association Mapping in Plant Genomes, Genetic Diversity in Plants. In: Caliskan M, ed., InTech. [2020-12-22]. Available from: http://www.intechopen.com/books/genetic-diversity-in-plants/association-mapping-in-plant-genomes
Sun G Y, He Y, Zhang R H, Zhang D P. 1996. Studies on growth and activities of soybean root. Soybean Science, 15, 317–321. (in Chinese)
Tanksley S D, McCouch S R. 1997. Seed banks and molecular maps: Unlocking genetic potential from the wild. Science, 277, 1063–1066.
Tuyen D D, Lal S K, Xu D H. 2010. Identification of a major QTL allele from wild soybean (Glycine soja Sieb. & Zucc.) for increasing alkaline salt tolerance in soybean. Theoretical and Applied Genetics, 121, 229–236.
Tuyen D D, Zhang H M, Xu D H. 2013. Validation and high-resolution mapping of a major quantitative trait locus for alkaline salt tolerance in soybean using residual heterozygous line. Molecular Breeding, 31, 79–86.
Wang N, Zhao S Z, Lv M H, Xiang F N, Li S. 2016. Research progress on identification of QTLs and functional genes involved in salt tolerance in soybean. Hereditas, 38, 992–1003.
Wang Z, Wang J, Bao Y, Wu Y, Zhang H. 2011. Quantitative trait loci controlling rice seed germination under salt stress. Euphytica, 178, 297–307.
Wani S H, Sah S K, Hossain M A, Kumar V, Balachandran S M. 2016. Transgenic approaches for abiotic stress tolerance in crop plants. In: Advances in Plant Breeding Strategies: Agronomic, Abiotic and Biotic Stress Traits. Springer, Cham, Switzerland. pp. 345–396. 
Xia J, Ren J, Zhang S, Wang Y, Fang Y. 2019. Forest and grass composite patterns improve the soil quality in the coastal saline-alkali land of the Yellow River Delta, China. Geoderma, 349, 25–35.
Yamaguchi T, Blumwald E. 2005. Developing salt-tolerant crop plants: Challenges and opportunities. Trends in Plant Science, 10, 615–620.
Yang J, Zaitlen N A, Goddard M E, Visscher P M, Price A L. 2014. Advantages and pitfalls in the application of mixed-model association methods. Nature Genetics, 46, 100–106.
Zeng A, Chen P, Korth K, Hancock F, Pereira A, Brye K, Wu C, Shi A. 2017. Genome-wide association study. GWAS of salt tolerance in worldwide soybean germplasm lines. Molecular Breeding, 37, 1–14.
Zhang K, Tang J, Wang Y, Kang H, Zeng J. 2020. The tolerance to saline-alkaline stress was dependent on the roots in wheat. Physiology and Molecular Biology of Plants, 26, 947–954.
Zhang W, Liao X L, Cui Y M, Ma W Y, Zhang X N, Du H Y, Ma Y J, Ning L H, Wang H, Huang F, Yang H, Kan G Z, Yu D Y. 2019. A cation diffusion facilitator, GmCDF1, negatively regulates salt tolerance in soybean. PLoS Genetics, 15, e1007798.
Zhang W J, Niu Y, Bu S H, Li M, Feng J Y, Zhang J, Yang S X, Odinga M M, Wei S P, Liu X F, Zhang Y M. 2014. Epistatic association mapping for alkaline and salinity tolerance traits in the soybean germination stage. PLoS ONE, 9, e84750.
Zhang Z, Ersoz E, Lai C Q, Todhunter R J, Tiwari H K, Gore M A, Bradbury P J, Yu J, Arnett D K, Ordovas J M, Buckler E S. 2010. Mixed linear model approach adapted for genome-wide association studies. Nature Genetics, 42, 355–360.
Zhifang G, Loescher W H. 2003. Expression of a celery mannose 6-phosphate reductase in Arabidopsis thaliana enhances salt tolerance and induces biosynthesis of both mannitol and a glucosyl-mannitol dimer. Plant, Cell & Environment, 26, 275–283.
Zhuang B C. 1999. Researches on wild soybean (Glycine soja) in China for twenty years. Journal of Jilin Agricultural Sciences, 24, 3–10. (in Chinese)

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