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Genome-wide association studies of drought-related metabolic changes in maize using an enlarged SNP panel

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Genetic determinants of metabolites related to drought tolerance in maize.

Abstract

Water deficit or drought is one of the most serious abiotic stresses of plant development and greatly reduces crop production, and the plant’s response to this deficit leads to many metabolic changes. To dissect the genetic basis of these metabolic traits in maize, we performed a genome-wide association analysis of drought-related traits using 156,599 SNPs in 318 maize inbred lines. In total, 123 significant SNP/trait associations (P ≤ 6.39E−6) involving 63 loci were identified for related metabolic and physiological traits in multiple tissues and different environments under two irrigation conditions. Of the 63, 23 loci demonstrated a significant interaction effect between QTL and water status, indicating that these metabolite-associated loci were probably related to drought stress tolerance. To evaluate the potential utility of metabolite-associated loci applied in hybrid maize breeding, we assembled two groups of hybrid entries with high or low drought tolerance and measured the metabolic and physiological traits. In the hybrid pools, a set of 10 metabolite-associated loci identified in leaf and ear were validated as responsive to drought stress. The favorable alleles of these ten loci were significantly enriched in hybrids with high drought tolerance, which jointly explained almost 18.4 % of the variation in drought tolerance using a multivariate logistic regression model. These results provide clues to understanding the genetic basis of metabolic and physiological changes related to drought tolerance, potentially facilitating the genetic improvement of varieties with high drought tolerance in maize breeding programs.

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References

  • Atwell S, Huang YS, Vilhjalmsson BJ, Willems G, Horton M, Li Y, Meng D, Platt A, Tarone AM, Hu TT, Jiang R, Muliyati NW, Zhang X, Amer MA, Baxter I, Brachi B, Chory J, Dean C, Debieu M, de Meaux J, Ecker JR, Faure N, Kniskern JM, Jones JD, Michael T, Nemri A, Roux F, Salt DE, Tang C, Todesco M, Traw MB, Weigel D, Marjoram P, Borevitz JO, Bergelson J, Nordborg M (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465:627–631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58

    Article  CAS  Google Scholar 

  • Brewer PB, Koltai H, Beveridge CA (2013) Diverse roles of strigolactones in plant development. Mol Plant 6:18–28

    Article  CAS  PubMed  Google Scholar 

  • Bu Q, Lv T, Shen H, Luong P, Wang J, Wang Z, Huang Z, Xiao L, Engineer C, Kim TH, Schroeder JI, Huq E (2014) Regulation of drought tolerance by the F-box protein MAX2 in Arabidopsis. Plant Physiol 164:424–439

    Article  CAS  PubMed  Google Scholar 

  • Buckler ES, Holland JB, Bradbury PJ, Acharya CB, Brown PJ, Browne C, Ersoz E, Flint-Garcia S, Garcia A, Glaubitz JC, Goodman MM, Harjes C, Guill K, Kroon DE, Larsson S, Lepak NK, Li H, Mitchell SE, Pressoir G, Peiffer JA, Rosas MO, Rocheford TR, Romay MC, Romero S, Salvo S, Sanchez Villeda H, da Silva HS, Sun Q, Tian F, Upadyayula N, Ware D, Yates H, Yu J, Zhang Z, Kresovich S, McMullen MD (2009) The genetic architecture of maize flowering time. Science 325:714–718

    Article  CAS  PubMed  Google Scholar 

  • Chan EK, Rowe HC, Hansen BG, Kliebenstein DJ (2010) The complex genetic architecture of the metabolome. PLoS Genet 6:e1001198

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen W, Gao Y, Xie W, Gong L, Lu K, Wang W, Li Y, Liu X, Zhang H, Dong H, Zhang W, Zhang L, Yu S, Wang G, Lian X, Luo J (2014) Genome-wide association analyses provide genetic and biochemical insights into natural variation in rice metabolism. Nat Genet 46:714–721

    Article  CAS  PubMed  Google Scholar 

  • Dunn OJ (1959) Estimation of the medians for dependent variables. Ann Math, Stat, pp 192–197

    Google Scholar 

  • Dunn OJ (1961) Multiple comparisons among means. J Am Stat Assoc 56:52–64

    Article  Google Scholar 

  • Duvick DN (2005) The contribution of breeding to yield advances in maize (Zea mays L.). Adv Agron 86:83–145

    Article  Google Scholar 

  • Fu J, Cheng Y, Linghu J, Yang X, Kang L, Zhang Z, Zhang J, He C, Du X, Peng Z, Wang B, Zhai L, Dai C, Xu J, Wang W, Li X, Zheng J, Chen L, Luo L, Liu J, Qian X, Yan J, Wang J, Wang G (2013) RNA sequencing reveals the complex regulatory network in the maize kernel. Nat Commun 4:2832

    PubMed  Google Scholar 

  • Ganal MW, Durstewitz G, Polley A, Berard A, Buckler ES, Charcosset A, Clarke JD, Graner EM, Hansen M, Joets J, Le Paslier MC, McMullen MD, Montalent P, Rose M, Schon CC, Sun Q, Walter H, Martin OC, Falque M (2011) A large maize (Zea mays L.) SNP genotyping array: development and germplasm genotyping, and genetic mapping to compare with the B73 reference genome. PLoS One 6:e28334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haley C (2011) A cornucopia of maize genes. Nat Genet 43:87–88

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Wei X, Sang T, Zhao Q, Feng Q, Zhao Y, Li C, Zhu C, Lu T, Zhang Z, Li M, Fan D, Guo Y, Wang A, Wang L, Deng L, Li W, Lu Y, Weng Q, Liu K, Huang T, Zhou T, Jing Y, Lin Z, Buckler ES, Qian Q, Zhang QF, Li J, Han B (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42:961–967

    Article  CAS  PubMed  Google Scholar 

  • Keurentjes JJ, Fu J, De Vos CR, Lommen A, Hall RD, Bino RJ, van der Plas LH, Jansen RC, Vreugdenhil D, Koornneef M (2006) The genetics of plant metabolism. Nat Genet 38:842–849

    Article  CAS  PubMed  Google Scholar 

  • Koops P, Pelser S, Ignatz M, Klose C, Marrocco-Selden K, Kretsch T (2011) EDL3 is an F-box protein involved in the regulation of abscisic acid signalling in Arabidopsis thaliana. J Exp Bot 62:5547–5560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lebreton C, Lazić-Jančić V, Steed A, Pekić S, Quarrie S (1995) Identification of QTL for drought responses in maize and their use in testing causal relationships between traits. J Exp Bot 46:853–865

    Article  CAS  Google Scholar 

  • Li MX, Yeung JM, Cherny SS, Sham PC (2012a) Evaluating the effective numbers of independent tests and significant P-value thresholds in commercial genotyping arrays and public imputation reference datasets. Hum Genet 131:747–756

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Yang X, Xu S, Cai Y, Zhang D, Han Y, Li L, Zhang Z, Gao S, Li J, Yan J (2012b) Genome-wide association studies identified three independent polymorphisms associated with alpha-tocopherol content in maize kernels. PLoS One 7:e36807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Peng Z, Yang X, Wang W, Fu J, Wang J, Han Y, Chai Y, Guo T, Yang N, Liu J, Warburton ML, Cheng Y, Hao X, Zhang P, Zhao J, Liu Y, Wang G, Li J, Yan J (2013) Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nat Genet 45:43–50

    Article  CAS  PubMed  Google Scholar 

  • Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang Z (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics 28:2397–2399

    Article  CAS  PubMed  Google Scholar 

  • Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425

    Article  Google Scholar 

  • Lu Y, Zhang S, Shah T, Xie C, Hao Z, Li X, Farkhari M, Ribaut JM, Cao M, Rong T, Xu Y (2010) Joint linkage-linkage disequilibrium mapping is a powerful approach to detecting quantitative trait loci underlying drought tolerance in maize. Proc Natl Acad Sci USA 107:19585–19590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo J (2015) Metabolite-based genome-wide association studies in plants. Curr Opin Plant Biol 24:31–38

    Article  CAS  PubMed  Google Scholar 

  • Maher B (2008) The case of the missing heritability. Nature 456:18–21

    Article  CAS  PubMed  Google Scholar 

  • Meyer RC, Steinfath M, Lisec J, Becher M, Witucka-Wall H, Torjek O, Fiehn O, Eckardt A, Willmitzer L, Selbig J, Altmann T (2007) The metabolic signature related to high plant growth rate in Arabidopsis thaliana. Proc Natl Acad Sci USA 104:4759–4764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohammadkhani N, Heidari R (2008) Drought-induced accumulation of soluble sugars and proline in two maize varieties. World Appl Sci J 3:448–453

    Google Scholar 

  • Paupière MJ, van Heusden AW, Bovy AG (2014) The metabolic basis of pollen thermo-tolerance: perspectives for breeding. Metabolites 4:889–920

    Article  PubMed  PubMed Central  Google Scholar 

  • Pinheiro C, Chaves M (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882

    Article  CAS  PubMed  Google Scholar 

  • Ribaut JM, Hoisington DA, Deutsch JA, Jiang C, Gonzalez-de-Leon D (1996) Identification of quantitative trait loci under drought conditions in tropical maize. 1. Flowering parameters and the anthesis-silking interval. Theor Appl Genet 92:905–914

    Article  CAS  PubMed  Google Scholar 

  • Ribaut JM, Betran J, Monneveux P, Setter T (2009) Drought tolerance in maize. In: Handbook of maize: its biology. Springer, New York, pp 311–344

  • Riedelsheimer C, Lisec J, Czedik-Eysenberg A, Sulpice R, Flis A, Grieder C, Altmann T, Stitt M, Willmitzer L, Melchinger AE (2012) Genome-wide association mapping of leaf metabolic profiles for dissecting complex traits in maize. Proc Natl Acad Sci USA 109:8872–8877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302

    Article  CAS  PubMed  Google Scholar 

  • Setter TL, Yan J, Warburton M, Ribaut JM, Xu Y, Sawkins M, Buckler ES, Zhang Z, Gore MA (2011) Genetic association mapping identifies single nucleotide polymorphisms in genes that affect abscisic acid levels in maize floral tissues during drought. J Exp Bot 62:701–716

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Tuteja N, Gill SS (2013) Climate change and plant abiotic stress tolerance. Wiley, New York

    Book  Google Scholar 

  • Wen W, Li D, Li X, Gao Y, Li W, Li H, Liu J, Liu H, Chen W, Luo J, Yan J (2014) Metabolome-based genome-wide association study of maize kernel leads to novel biochemical insights. Nat Commun 5:3438

    PubMed  PubMed Central  Google Scholar 

  • Wen W, Li K, Alseekh S, Omranian N, Zhao L, Zhou Y, Xiao Y, Jin M, Yang N, Liu H, Florian A, Li W, Pan Q, Nikoloski Z, Yan J, Fernie AR (2015) Genetic determinants of the network of primary metabolism and their relationships to plant performance in a maize recombinant inbred line population. Plant Cell 27:1839–1856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whipple CJ, Ciceri P, Padilla CM, Ambrose BA, Bandong SL, Schmidt RJ (2004) Conservation of B-class floral homeotic gene function between maize and Arabidopsis. Development 131:6083–6091

    Article  CAS  PubMed  Google Scholar 

  • Wuest SE, O’Maoileidigh DS, Rae L, Kwasniewska K, Raganelli A, Hanczaryk K, Lohan AJ, Loftus B, Graciet E, Wellmer F (2012) Molecular basis for the specification of floral organs by APETALA3 and PISTILLATA. Proc Natl Acad Sci USA 109:13452–13457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue Y, Warburton ML, Sawkins M, Zhang X, Setter T, Xu Y, Grudloyma P, Gethi J, Ribaut JM, Li W, Zhang X, Zheng Y, Yan J (2013) Genome-wide association analysis for nine agronomic traits in maize under well-watered and water-stressed conditions. Theor Appl Genet 126:2587–2596

    Article  CAS  PubMed  Google Scholar 

  • Yan J, Shah T, Warburton ML, Buckler ES, McMullen MD, Crouch J (2009) Genetic characterization and linkage disequilibrium estimation of a global maize collection using SNP markers. PLoS One 4:e8451

    Article  PubMed  PubMed Central  Google Scholar 

  • Yan J, Warburton M, Crouch J (2011) Association mapping for enhancing maize (Zea may L.) genetic improvement. Crop Sci 51:433–449

    Article  Google Scholar 

  • Yang N, Lu Y, Yang X, Huang J, Zhou Y, Ali F, Wen W, Liu J, Li J, Yan J (2014) Genome wide association studies using a new nonparametric model reveal the genetic architecture of 17 agronomic traits in an enlarged maize association panel. PLoS Genet 10:e1004573

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang Ye XuW, Li Z, Deng XW, Wu W, Xue Y (2008) F-box protein DOR functions as a novel inhibitory factor for abscisic acid-induced stomatal closure under drought stress in Arabidopsis. Plant Physiol 148:2121–2133

    Article  Google Scholar 

  • Zhang Z, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu J, Arnett DK, Ordovas JM, Buckler ES (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42:355–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This research was supported by the National Hi-Tech Research and Development Program of China (2012AA10A307), the National Natural Science Foundation of China (31222041, 31401389) and the Generation Challenge Program of the CGIAR.

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Correspondence to Yingjie Xiao.

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Communicated by C. Carolin Schön.

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Zhang, X., Warburton, M.L., Setter, T. et al. Genome-wide association studies of drought-related metabolic changes in maize using an enlarged SNP panel. Theor Appl Genet 129, 1449–1463 (2016). https://doi.org/10.1007/s00122-016-2716-0

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