Genome-wide association among soybean accessions for the genetic basis of salinity-alkalinity tolerance during germination
Yongce Cao A , Xincao Zhang A , Shihao Jia A , Benjamin Karikari B C , Mingjun Zhang D , Zhangyi Xia A , Tuanjie Zhao B E and Fuqin Liang D EA Shaanxi Key Laboratory of Chinese Jujube, College of Life Science, Yan’an University, Yan’an, Shaanxi 716000, China.
B Soybean Research Institute of Nanjing Agricultural University, Key Laboratory of Biology and Genetic Improvement of Soybean, Ministry of Agriculture, National Centre for Soybean Improvement, National Key Laboratory for Crop Genetics and Germplasm Enhancement, Nanjing, Jiangsu 210095, China.
C Department of Crop Science, Faculty of Agriculture, Food and Consumer Sciences, University for Development Studies, PO Box TL 1882, Tamale, Ghana.
D Institute of Yan’an Agricultural Science, Yan’an, Shaanxi 716000, China.
E Corresponding authors. Email: tjzhao@njau.edu.cn; yankslfq@126.com
Crop and Pasture Science 72(4) 255-267 https://doi.org/10.1071/CP20459
Submitted: 19 November 2020 Accepted: 2 March 2021 Published: 28 April 2021
Abstract
Salinity-alkalinity stress is one of the main factors limiting crop growth and production. However, few genetic sources that can be used to improve soybean salinity-alkalinity tolerance are available. The objective of this study was to determine the genetic mechanisms for salinity-alkalinity tolerance in soybean during germination by a genome-wide association study (GWAS) using 281 accessions with 58 112 single nucleotide polymorphisms (SNPs). Four salinity-alkalinity tolerance (ST) indices namely ST-GR (germination ratio), ST-RFW (root fresh weight), ST-DRW (root dry weight), and ST-RL (root length) were used to assess soybean salinity-alkalinity tolerance. A total of 8, 4, 6, and 4 quantitative trait loci (QTL) accounted for 3.83–8.01% phenotypic variation in ST-GR, ST-RL, ST-RFW, and ST-RDW, respectively. Two common QTL (qST.5.1 and qST.16.1) associated with at least three indices located on chromosome 5 (~38.4 Mb) and chromosome 16 (~29.8 Mb), were determined as important loci for controlling salinity-alkalinity tolerance in soybean. We also predicted candidate genes for the two QTL. The significant SNPs and common QTL as well as the salinity-alkalinity tolerant accessions will improve the efficiency of marker-assisted breeding and candidate gene discovery for soybean salinity-alkalinity tolerance.
Keywords: crop production, genome-wide association study, soybean, germination, seed yield, seed quality, salinity-alkalinity stress, single nucleotide polymorphism, quantitative trait locus, recombinant inbred line, genetic mechanism.
References
Al-Karaki GN (2006) Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water. Scientia Horticulturae 109, 1–7.| Nursery inoculation of tomato with arbuscular mycorrhizal fungi and subsequent performance under irrigation with saline water.Crossref | GoogleScholarGoogle Scholar |
Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Research 19, 1655–1664.
| Fast model-based estimation of ancestry in unrelated individuals.Crossref | GoogleScholarGoogle Scholar | 19648217PubMed |
Aragüés R, Medina ET, Zribi W, Clavería I, Álvaro-Fuentes J, Faci J (2015) Soil salinization as a threat to the sustainability of deficit irrigation under present and expected climate change scenarios. Irrigation Science 33, 67–79.
| Soil salinization as a threat to the sustainability of deficit irrigation under present and expected climate change scenarios.Crossref | GoogleScholarGoogle Scholar |
Barrett JC (2009) Haploview: visualization and analysis of SNP genotype data. Cold Spring Harbor Protocols 2009, pdb-ip71
| Haploview: visualization and analysis of SNP genotype data.Crossref | GoogleScholarGoogle Scholar | 20147036PubMed |
Bewley JD (1997) Seed germination and dormancy. The Plant Cell 9, 1055–1066.
| Seed germination and dormancy.Crossref | GoogleScholarGoogle Scholar | 12237375PubMed |
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23, 2633–2635.
| TASSEL: software for association mapping of complex traits in diverse samples.Crossref | GoogleScholarGoogle Scholar | 17586829PubMed |
Breseghello F, Sorrells ME (2006) Association analysis as a strategy for improvement of quantitative traits in plants. Crop Science 46, 1323–1330.
| Association analysis as a strategy for improvement of quantitative traits in plants.Crossref | GoogleScholarGoogle Scholar |
Chang F, Guo C, Sun F, Zhang J, Wang Z, Kong J, He Q, Sharmin RA, Zhao T (2018) Genome-wide association studies for dynamic plant height and number of nodes on the main stem in summer sowing soybeans. Frontiers in Plant Science 9, 1184
| Genome-wide association studies for dynamic plant height and number of nodes on the main stem in summer sowing soybeans.Crossref | GoogleScholarGoogle Scholar | 30177936PubMed |
Chen HT, Cui SY, Fu SX, Gai JY, Yu DY (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.
| Identification of quantitative trait loci associated with salt tolerance during seedling growth in soybean (Glycine max L.).Crossref | GoogleScholarGoogle Scholar |
Chen WC, Cui PJ, Sun HY, Guo WQ, Yang CW, Jin H, Fang B, Shi DC (2009) Comparative effects of salt and alkali stresses on organic acid accumulation and ionic balance of seabuckthorn (Hippophae rhamnoides L.). Industrial Crops and Products 30, 351–358.
| Comparative effects of salt and alkali stresses on organic acid accumulation and ionic balance of seabuckthorn (Hippophae rhamnoides L.).Crossref | GoogleScholarGoogle Scholar |
Chen HT, Liu XQ, Zhang HM, Yuan XX, Gu HP, Cui XY, Chen X (2018a) Advances in salinity tolerance of soybean: genetic diversity heredity and gene identification contribute to improving salinity tolerance. Journal of Integrative Agriculture 17, 2215–2221.
| Advances in salinity tolerance of soybean: genetic diversity heredity and gene identification contribute to improving salinity tolerance.Crossref | GoogleScholarGoogle Scholar |
Chen H, Ye H, Do TD, Zhou J, Valliyodan B, Shannon GJ, Chen PY, Chen X, Nguyen HT (2018b) Advances in genetics and breeding of salt tolerance in soybean. In ‘Salinity responses and tolerance in plants. Vol. 2’. (Eds V Kumar, S Wani, P Suprasanna, LS Tran) pp. 217–237. (Springer: Cham, Switzerland)
Chen Y, Chi Y, Meng Q, Wang X, Yu D (2018c) GmSK1 an SKP1 homologue in soybean is involved in the tolerance to salt and drought. Plant Physiology and Biochemistry 127, 25–31.
| GmSK1 an SKP1 homologue in soybean is involved in the tolerance to salt and drought.Crossref | GoogleScholarGoogle Scholar | 29544210PubMed |
Cornelious B, Chen P, Chen Y, De Leon N, Shannon JG, Wang D (2005) Identification of QTLs underlying water-logging tolerance in soybean. Molecular Breeding 16, 103–112.
| Identification of QTLs underlying water-logging tolerance in soybean.Crossref | GoogleScholarGoogle Scholar |
Cui Y, Zhang F, Zhou Y (2018) The application of multi-locus GWAS for the detection of salt-tolerance loci in rice. Frontiers in Plant Science 9, 1464
| The application of multi-locus GWAS for the detection of salt-tolerance loci in rice.Crossref | GoogleScholarGoogle Scholar | 30337936PubMed |
Do TD, Vuong TD, Dunn D, Smothers S, Patil G, Yungbluth DC, Chen PY, Scaboo A, Xu D, Carter TE, et al (2018) Mapping and confirmation of loci for salt tolerance in a novel soybean germplasm, Fiskeby III. Theoretical and Applied Genetics 131, 513–524.
| Mapping and confirmation of loci for salt tolerance in a novel soybean germplasm, Fiskeby III.Crossref | GoogleScholarGoogle Scholar | 29151146PubMed |
Do TD, Vuong TD, Dunn D, Clubb M, Valliyodan B, Patil G, Chen PY, Xu D, Nguyen HT, Shannon JG (2019) Identification of new loci for salt tolerance in soybean by high-resolution genome-wide association mapping. BMC Genomics 20, 318
| Identification of new loci for salt tolerance in soybean by high-resolution genome-wide association mapping.Crossref | GoogleScholarGoogle Scholar | 31023240PubMed |
Doyle JJ (1990) Isolation of plant DNA from fresh tissue. Focus 12, 13–15.
Du W, Wang M, Fu S, Yu D (2009) Mapping QTLs for seed yield and drought susceptibility index in soybean (Glycine max L.) across different environments. Journal of Genetics and Genomics 36, 721–731.
| Mapping QTLs for seed yield and drought susceptibility index in soybean (Glycine max L.) across different environments.Crossref | GoogleScholarGoogle Scholar | 20129399PubMed |
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.
| Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.Crossref | GoogleScholarGoogle Scholar | 15969739PubMed |
Forni C, Duca D, Glick BR (2017) Mechanisms of plant response to salt and drought stress and their alteration by rhizobacteria. Plant and Soil 410, 335–356.
| Mechanisms of plant response to salt and drought stress and their alteration by rhizobacteria.Crossref | GoogleScholarGoogle Scholar |
Guan R, Chen J, Jiang J, Liu G, Liu Y, Tian L, Yu L, Chang R, Qiu LJ (2014a) Mapping and validation of a dominant salt tolerance gene in the cultivated soybean (Glycine max) variety Tiefeng 8. The Crop Journal 2, 358–365.
| Mapping and validation of a dominant salt tolerance gene in the cultivated soybean (Glycine max) variety Tiefeng 8.Crossref | GoogleScholarGoogle Scholar |
Guan R, Qu Y, Guo Y, Yu L, Liu Y, Jiang J, Chen J, Ren Y, Liu G, Tian L, et al (2014b) Salinity tolerance in soybean is modulated by natural variation in GmSALT3. The Plant Journal 80, 937–950.
| Salinity tolerance in soybean is modulated by natural variation in GmSALT3.Crossref | GoogleScholarGoogle Scholar | 25292417PubMed |
Guo R, Shi L, Yan C, Zhong X, Gu F, Liu Q, Xia X, Li H (2017) Ionomic and metabolic responses to neutral salt or alkaline salt stresses in maize (Zea mays L.) seedlings. BMC Plant Biology 17, 41
| Ionomic and metabolic responses to neutral salt or alkaline salt stresses in maize (Zea mays L.) seedlings.Crossref | GoogleScholarGoogle Scholar | 28187710PubMed |
Gupta PK, Rustgi S, Kulwal PL (2005) Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Molecular Biology 57, 461–485.
| Linkage disequilibrium and association studies in higher plants: present status and future prospects.Crossref | GoogleScholarGoogle Scholar | 15821975PubMed |
He J, Meng S, Zhao T, Xing G, Yang S, Li Y, Guan R, Lu J, Wang Y, Xia Q, Yang B, Gai J (2017) An innovative procedure of genome-wide association analysis fits studies on germplasm population and plant breeding. Theoretical and Applied Genetics 130, 2327–2343.
| An innovative procedure of genome-wide association analysis fits studies on germplasm population and plant breeding.Crossref | GoogleScholarGoogle Scholar | 28828506PubMed |
Huang RD (2018) Research progress on plant tolerance to soil salinity and alkalinity in sorghum. Journal of Integrative Agriculture 17, 739–746.
| Research progress on plant tolerance to soil salinity and alkalinity in sorghum.Crossref | GoogleScholarGoogle Scholar |
Huang L, Zeng A, Chen P, Wu C, Wang D, Wen Z (2018a) Genome wide association analysis of salt tolerance in soybean (Glycine max (L.) Merr.). Plant Breeding 137, 714–720.
| Genome wide association analysis of salt tolerance in soybean (Glycine max (L.) Merr.).Crossref | GoogleScholarGoogle Scholar |
Huang K, Peng L, Liu Y, Yao R, Liu Z, Li X, Yang Y, Wang J (2018b) Arabidopsis calcium-dependent protein kinase AtCPK1 plays a positive role in salt/drought-stress response. Biochemical and Biophysical Research Communications 498, 92–98.
| Arabidopsis calcium-dependent protein kinase AtCPK1 plays a positive role in salt/drought-stress response.Crossref | GoogleScholarGoogle Scholar | 29196259PubMed |
Hwang EY, Song QJ, Jia GF, Specht JE, Hyten DL, Costa J, Cregan PB (2014) A genome-wide association study of seed protein and oil content in soybean. BMC Genomics 15, 1
| A genome-wide association study of seed protein and oil content in soybean.Crossref | GoogleScholarGoogle Scholar | 24382143PubMed |
Josephs EB, Stinchcombe JR, Wright SI (2017) What can genome-wide association studies tell us about the evolutionary forces maintaining genetic variation for quantitative traits? New Phytologist 214, 21–33.
| What can genome-wide association studies tell us about the evolutionary forces maintaining genetic variation for quantitative traits?Crossref | GoogleScholarGoogle Scholar |
Kaler AS, Dhanapal AP, Ray JD, King CA, Fritschi FB, Purcell LC (2017) Genome‐wide association mapping of carbon isotope and oxygen isotope ratios in diverse soybean genotypes. Crop Science 57, 3085–3100.
| Genome‐wide association mapping of carbon isotope and oxygen isotope ratios in diverse soybean genotypes.Crossref | GoogleScholarGoogle Scholar |
Kan G, Zhang W, Yang W, Ma D, Zhang D, Hao D, Hu Z, Yu D (2015) Association mapping of soybean seed germination under salt stress. Molecular Genetics and Genomics 290, 2147–2162.
| Association mapping of soybean seed germination under salt stress.Crossref | GoogleScholarGoogle Scholar | 26001372PubMed |
Kan G, Ning L, Li Y, Hu Z, Zhang W, He X, Yu D (2016) Identification of novel loci for salt stress at the seed germination stage in soybean. Breeding Science 66, 530–541.
| Identification of novel loci for salt stress at the seed germination stage in soybean.Crossref | GoogleScholarGoogle Scholar | 27795678PubMed |
Lam HM, Xu X, Liu X, Chen WB, Yang GH, Wong FL, Li MW, He WM, Qin N, Wang B, et al (2010) Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nature Genetics 42, 1053–1059.
| Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection.Crossref | GoogleScholarGoogle Scholar | 21076406PubMed |
Lee GJ, Boerma HR, Villagarcia MR, Zhou X, Carter TE, Li Z, Gibbs MO (2004) A major QTL conditioning salt tolerance in S-100 soybean and descendent cultivars. Theoretical and Applied Genetics 109, 1610–1619.
| A major QTL conditioning salt tolerance in S-100 soybean and descendent cultivars.Crossref | GoogleScholarGoogle Scholar | 15365627PubMed |
Li D, Dossa K, Zhang Y, Wei X, Wang L, Zhang Y, Liu A, Zhou R, Zhang X (2018) GWAS uncovers differential genetic bases for drought and salt tolerances in sesame at the germination stage. Genes 9, 87
| GWAS uncovers differential genetic bases for drought and salt tolerances in sesame at the germination stage.Crossref | GoogleScholarGoogle Scholar |
Li B, Chen L, Sun W, Wu D, Wang M, Yu Y, Chen G, Yang W, Lin Z, Zhang X, et al (2020) Phenomics‐based GWAS analysis reveals the genetic architecture for drought resistance in cotton. Plant Biotechnology Journal.
| Phenomics‐based GWAS analysis reveals the genetic architecture for drought resistance in cotton.Crossref | GoogleScholarGoogle Scholar | 32854160PubMed |
Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang ZW (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics 28, 2397–2399.
| GAPIT: genome association and prediction integrated tool.Crossref | GoogleScholarGoogle Scholar | 22796960PubMed |
Liu S, Guo X, Feng G, Maimaitiaili B, Fan J, He X (2016) Indigenous arbuscular mycorrhizal fungi can alleviate salt stress and promote growth of cotton and maize in saline fields. Plant and Soil 398, 195–206.
| Indigenous arbuscular mycorrhizal fungi can alleviate salt stress and promote growth of cotton and maize in saline fields.Crossref | GoogleScholarGoogle Scholar |
Long NV, Dolstra O, Malosetti M, Kilian B, Graner A, Visser RGF, van der Linden CG (2013) Association mapping of salt tolerance in barley (Hordeum vulgare L.). Theoretical and Applied Genetics 126, 2335–2351.
| Association mapping of salt tolerance in barley (Hordeum vulgare L.).Crossref | GoogleScholarGoogle Scholar | 23771136PubMed |
Luo Z, Szczepanek A, Abdel-Haleem H (2020) Genome-wide association study (GWAS) analysis of Camelina seedling germination under salt stress condition. Agronomy 10, 1444
| Genome-wide association study (GWAS) analysis of Camelina seedling germination under salt stress condition.Crossref | GoogleScholarGoogle Scholar |
Ma L, Hu L, Fan J, Amombo E, Khaldun ABM, Zheng Y, Chen L (2017) Cotton GhERF38 gene is involved in plant response to salt/drought and ABA. Ecotoxicology 26, 841–854.
| Cotton GhERF38 gene is involved in plant response to salt/drought and ABA.Crossref | GoogleScholarGoogle Scholar | 28536792PubMed |
Mian MAR, Bailey MA, Ashley DA, Wells R, Carter TE, Parrott WA, Boerma HR (1996) Molecular markers associated with water use efficiency and leaf ash in soybean. Crop Science 36, 1252–1257.
| Molecular markers associated with water use efficiency and leaf ash in soybean.Crossref | GoogleScholarGoogle Scholar |
Niu J, Guo N, Zhang Z, Wang Z, Huang J, Zhao J, Chang F, Wang H, Zhao T, Xing H (2018) Genome-wide SNP-based association mapping of resistance to Phytophthora sojae in soybean (Glycine max (L.) Merr.). Euphytica 214, 187
| Genome-wide SNP-based association mapping of resistance to Phytophthora sojae in soybean (Glycine max (L.) Merr.).Crossref | GoogleScholarGoogle Scholar |
Padmanaban S, Lin X, Perera I, Kawamura Y, Sze H (2004) Differential expression of vacuolar H+-ATPase subunit c genes in tissues active in membrane trafficking and their roles in plant growth as revealed by RNAi. Plant Physiology 134, 1514–1526.
| Differential expression of vacuolar H+-ATPase subunit c genes in tissues active in membrane trafficking and their roles in plant growth as revealed by RNAi.Crossref | GoogleScholarGoogle Scholar | 15051861PubMed |
Pathan MS, Lee JD, Shannon JG, Nguyen HT (2007) Recent advances in breeding for drought and salt stress tolerance in soybean. In ‘Advances in molecular-breeding toward drought and salt tolerant crops’. (Eds MA Jenks, PM Hasegawa, SM Jain) pp. 739–773. (Springer: Dordrecht)
Patil G, Do TD, Vuong TD, Valliyodan B, Lee JD, Chaudhary J, Shannon JG, Nguyen HT (2016) Genomic-assisted haplotype analysis and the development of high-throughput SNP markers for salinity tolerance in soybean. Scientific Reports 6, 19199
| Genomic-assisted haplotype analysis and the development of high-throughput SNP markers for salinity tolerance in soybean.Crossref | GoogleScholarGoogle Scholar | 26781337PubMed |
Phang TH, Shao GH, Lam HM (2008) Salt tolerance in soybean. Journal of Integrative Plant Biology 50, 1196–1212.
| Salt tolerance in soybean.Crossref | GoogleScholarGoogle Scholar | 19017107PubMed |
Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nature Genetics 38, 904–909.
| Principal components analysis corrects for stratification in genome-wide association studies.Crossref | GoogleScholarGoogle Scholar | 16862161PubMed |
Qadir M, Quillérou E, Nangia V, Murtaza G, Singh M, Thomas R, Drechsel P, Noble A (2014) Economics of salt-induced land degradation and restoration. Natural Resources Forum 38, 282–295.
| Economics of salt-induced land degradation and restoration.Crossref | GoogleScholarGoogle Scholar |
Qi XP, Li MW, Xie M, Liu X, Ni M, Shao GH, Song C, Yim AKY, Tao Y, Wong FL, et al (2014) Identification of a novel salt tolerance gene in wild soybean by whole-genome sequencing. Nature Communications 5, 4340
| Identification of a novel salt tolerance gene in wild soybean by whole-genome sequencing.Crossref | GoogleScholarGoogle Scholar |
Qiu PC, Zhang WB, Liu CY, Jiang HW, Li CD, Fan HM, Zeng QL, Hu GH, Cheng QS (2011) QTL identification of salt tolerance in germination stage of soybean. Legume Genomics and Genetics 2, 20–27.
Rizal G, Karki S (2011) Alcohol dehydrogenase (ADH) activity in soybean (Glycine max (L.) Merr.) under flooding stress. Electronic Journal of Plant Breeding 2, 50–57.
Roy SJ, Negrao S, Tester M (2014) Salt resistant crop plants. Current Opinion in Biotechnology 26, 115–124.
| Salt resistant crop plants.Crossref | GoogleScholarGoogle Scholar | 24679267PubMed |
Schmutz J, Cannon SB, Schlueter J, Ma JX, Mitros T, Nelson W, Hyten DL, Song QJ, Thelen JJ, Cheng JL, et al (2010) Genome sequence of the palaeopolyploid soybean. Nature 46, 3178–3183.
Shi X, Yan L, Yang CY, Yan WW, Moseley DO, Wang T, Liu BQ, Di R, Chen PY, Zhang MC (2018a) Identification of a major quantitative trait locus underlying salt tolerance in ‘Jidou 12’ soybean cultivar. BMC Research Notes 11, 95
| Identification of a major quantitative trait locus underlying salt tolerance in ‘Jidou 12’ soybean cultivar.Crossref | GoogleScholarGoogle Scholar | 29402302PubMed |
Shi WY, Du YT, Ma J, Min DH, Jin LG, Chen J, Chen M, Zhou Y, Ma Y, Xu Z, et al (2018b) The WRKY transcription factor GmWRKY12 confers drought and salt tolerance in soybean. International Journal of Molecular Sciences 19, 4087
| The WRKY transcription factor GmWRKY12 confers drought and salt tolerance in soybean.Crossref | GoogleScholarGoogle Scholar |
Singh AK, Kumar R, Tripathi AK, Gupta BK, Pareek A, Singla-Pareek SL (2015) Genome-wide investigation and expression analysis of Sodium/Calcium exchanger gene family in rice and Arabidopsis. Rice 8, 21
| Genome-wide investigation and expression analysis of Sodium/Calcium exchanger gene family in rice and Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Sneller C, Mather DE, Crepieux S (2009) Analytical approaches and population types for finding and utilizing QTL in complex plant populations. Crop Science 49, 363–380.
| Analytical approaches and population types for finding and utilizing QTL in complex plant populations.Crossref | GoogleScholarGoogle Scholar |
Takagi H, Tamiru M, Abe A, Yoshida K, Uemura A, Yaegashi H, Obara T, Oikawa K, Utsushi H, Kanzaki E, Mitsuoka C, Natsume S, Kosugi S, Kanzaki H, Matsumura H, Urasaki N, Kamoun S, Terauchi R (2015) MutMap accelerates breeding of a salt-tolerant rice cultivar. Nature Biotechnology 33, 445–449.
| MutMap accelerates breeding of a salt-tolerant rice cultivar.Crossref | GoogleScholarGoogle Scholar | 25798936PubMed |
Tuyen DD, Lal SK, Xu DH (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.
| Identification of a major QTL allele from wild soybean (Glycine soja Sieb & Zucc) for increasing alkaline salt tolerance in soybean.Crossref | GoogleScholarGoogle Scholar | 20204319PubMed |
Tuyen DD, Zhang HM, Xu DH (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.
| Validation and high-resolution mapping of a major quantitative trait locus for alkaline salt tolerance in soybean using residual heterozygous line.Crossref | GoogleScholarGoogle Scholar |
Wang P, Li Z, Wei J, Zhao Z, Sun D, Cui S (2012) A Na+/Ca2+ exchanger-like protein (AtNCL) involved in salt stress in Arabidopsis. The Journal of Biological Chemistry 287, 44062–44070.
| A Na+/Ca2+ exchanger-like protein (AtNCL) involved in salt stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 23148213PubMed |
Wang FW, Wang C, Sun Y, Wang N, Li XW, Dong YY, Yao N, Liu XM, Chen H, Chen XF, et al (2016) Overexpression of vacuolar proton pump ATPase (V-H+-ATPase) subunits B C and H confers tolerance to salt and saline-alkali stresses in transgenic alfalfa (Medicago sativa L.). Journal of Integrative Agriculture 15, 2279–2289.
| Overexpression of vacuolar proton pump ATPase (V-H+-ATPase) subunits B C and H confers tolerance to salt and saline-alkali stresses in transgenic alfalfa (Medicago sativa L.).Crossref | GoogleScholarGoogle Scholar |
Wilson RF (2008) Soybean: market driven research needs. In ‘Genetics and genomics of soybean’. (Ed. G Stacey) pp. 3–15. (Springer: New York, USA)
Xu DH, Do TD (2012) Genetic studies on saline and sodic tolerances in soybean. Breeding Science 61, 559–565.
| Genetic studies on saline and sodic tolerances in soybean.Crossref | GoogleScholarGoogle Scholar |
Yamaguchi T, Blumwald E (2005) Developing salt-tolerant crop plants: challenges and opportunities. Trends in Plant Science 10, 615–620.
| Developing salt-tolerant crop plants: challenges and opportunities.Crossref | GoogleScholarGoogle Scholar | 16280254PubMed |
Yu Y, Wu G, Yuan H, Cheng L, Zhao D, Huang W, Zhang S, Zhang L, Chen H, Zhang J (2016) Identification and characterization of miRNAs and targets in flax (Linum usitatissimum) under saline alkaline and saline-alkaline stresses. BMC Plant Biology 16, 124
| Identification and characterization of miRNAs and targets in flax (Linum usitatissimum) under saline alkaline and saline-alkaline stresses.Crossref | GoogleScholarGoogle Scholar | 27234464PubMed |
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, 30
| Genome-wide association study (GWAS) of salt tolerance in worldwide soybean germplasm lines.Crossref | GoogleScholarGoogle Scholar |
Zhang LM, Liu XG, Qu XN, Yu Y, Han SP, Dou Y, Xu YY, Jing HC, Hao DY (2013a) Early transcriptomic adaptation to Na2CO3 stress altered the expression of a quarter of the total genes in the maize genome and exhibited shared and distinctive profiles with NaCl and high pH stresses. Journal of Integrative Plant Biology 55, 1147–1165.
| Early transcriptomic adaptation to Na2CO3 stress altered the expression of a quarter of the total genes in the maize genome and exhibited shared and distinctive profiles with NaCl and high pH stresses.Crossref | GoogleScholarGoogle Scholar | 24034274PubMed |
Zhang X, Wei LQ, Wang ZZ, Wang T (2013b) Physiological and molecular features of Puccinellia tenuiflora tolerating salt and alkaline-salt stress. Journal of Integrative Plant Biology 55, 262–276.
| Physiological and molecular features of Puccinellia tenuiflora tolerating salt and alkaline-salt stress.Crossref | GoogleScholarGoogle Scholar | 23176661PubMed |
Zhang WJ, Niu Y, Bu SH, Li M, Feng JY, Zhang J, Yang SX, Odinga MM, Wei SP, Liu XF, Zhang YM (2014) Epistatic association mapping for alkaline and salinity tolerance traits in the soybean germination stage. PLoS One 9, e84750
| Epistatic association mapping for alkaline and salinity tolerance traits in the soybean germination stage.Crossref | GoogleScholarGoogle Scholar | 25255097PubMed |
Zhang D, Li H, Wang J, Zhang H, Hu Z, Chu S, Lv H, Yu D (2016) High-density genetic mapping identifies new major loci for tolerance to low-phosphorus stress in soybean. Frontiers in Plant Science 7, 372
| High-density genetic mapping identifies new major loci for tolerance to low-phosphorus stress in soybean.Crossref | GoogleScholarGoogle Scholar | 27065041PubMed |
Zhang W, Liao X, Cui Y, Ma W, Zhang X, Du H, Ma Y, Ning L, Wang H, Huang F, et al (2019) A cation diffusion facilitator GmCDF1 negatively regulates salt tolerance in soybean. PLOS Genetics 15, e1007798
| A cation diffusion facilitator GmCDF1 negatively regulates salt tolerance in soybean.Crossref | GoogleScholarGoogle Scholar | 31430288PubMed |
Zhao K, Tung C, Eizenga GC, Wright MH, Ali ML, Price AH, Norton GJ, Islam MR, Reynolds A, Mezey J, et al (2011) Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nature Communications 2, 467
| Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa.Crossref | GoogleScholarGoogle Scholar | 21915109PubMed |
Zhao C, Zhang H, Song C, Zhu JK, Shabala S (2020) Mechanisms of plant responses and adaptation to soil salinity. The Innovation 1, 100017
| Mechanisms of plant responses and adaptation to soil salinity.Crossref | GoogleScholarGoogle Scholar |
Zhu JK (2001) Plant salt tolerance. Trends in Plant Science 6, 66–71.
| Plant salt tolerance.Crossref | GoogleScholarGoogle Scholar | 11173290PubMed |
Zhu C, Gore M, Buckler ES, Yu J (2008) Status and prospects of association mapping in plants. The Plant Genome 1, 5–20.
| Status and prospects of association mapping in plants.Crossref | GoogleScholarGoogle Scholar |
Zhu M, Meng X, Cai J, Li G, Dong T, Li Z (2018) Basic leucine zipper transcription factor SlbZIP1 mediates salt and drought stress tolerance in tomato. BMC Plant Biology 18, 83
| Basic leucine zipper transcription factor SlbZIP1 mediates salt and drought stress tolerance in tomato.Crossref | GoogleScholarGoogle Scholar | 29739325PubMed |