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Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings

Nature Genetics volume 48, pages 1233–1241 (2016)Cite this article

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Abstract

Maize production is threatened by drought stress worldwide. Identification of the genetic components underlying drought tolerance in maize is of great importance. Here we report a genome-wide association study (GWAS) of maize drought tolerance at the seedling stage that identified 83 genetic variants, which were resolved to 42 candidate genes. The peak GWAS signal showed that the natural variation in ZmVPP1, encoding a vacuolar-type H+ pyrophosphatase, contributes most significantly to the trait. Further analysis showed that a 366-bp insertion in the promoter, containing three MYB cis elements, confers drought-inducible expression of ZmVPP1 in drought-tolerant genotypes. Transgenic maize with enhanced ZmVPP1 expression exhibits improved drought tolerance that is most likely due to enhanced photosynthetic efficiency and root development. Taken together, this information provides important genetic insights into the natural variation of maize drought tolerance. The identified loci or genes can serve as direct targets for both genetic engineering and selection for maize trait improvement.

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Figure 1: GWAS for drought tolerance in maize seedlings.
Figure 2: Natural variations in ZmVPP1 were significantly associated with maize drought tolerance.
Figure 3: Functional characterization of ZmVPP1 as a H+-PPase and comparison of ZmVPP1B73 and ZmVPP1CIMBL55 protein function in Arabidopsis.
Figure 4: The 366-bp insertion (indel −379) in the ZmVPP1CIMBL55 allele confers stress-inducible expression of ZmVPP1.
Figure 5: The ZmVPP1 tolerant allele improves drought tolerance in maize seedlings.
Figure 6: Drought tolerance of ZmVPP1 transgenic maize.
Figure 7: Photosynthetic capacity and yield performance of transgenic maize.

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References

  1. Lobell, D.B. et al. Greater sensitivity to drought accompanies maize yield increase in the U.S. Midwest. Science 344, 516–519 (2014).

    Article  CAS  PubMed  Google Scholar 

  2. Boyer, J.S. et al. The U.S. drought of 2012 in perspective: A call to action. Global Food Security. 2, 139–143 (2013).

    Article  Google Scholar 

  3. Yu, C. China's water crisis needs more than words. Nature 470, 307 (2011).

    Article  CAS  PubMed  Google Scholar 

  4. Pennisi, E. Plant genetics. The blue revolution, drop by drop, gene by gene. Science 320, 171–173 (2008).

    Article  CAS  PubMed  Google Scholar 

  5. Maruyama, K. et al. Metabolic pathways involved in cold acclimation identified by integrated analysis of metabolites and transcripts regulated by DREB1A and DREB2A. Plant Physiol. 150, 1972–1980 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Qin, F., Shinozaki, K. & Yamaguchi-Shinozaki, K. Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol. 52, 1569–1582 (2011).

    Article  CAS  PubMed  Google Scholar 

  7. Yamaguchi-Shinozaki, K. & Shinozaki, K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol. 57, 781–803 (2006).

    Article  CAS  PubMed  Google Scholar 

  8. Mackay, T.F.C. Quantitative trait loci in Drosophila. Nat. Rev. Genet. 2, 11–20 (2001).

    Article  CAS  PubMed  Google Scholar 

  9. Yu, J. & Buckler, E.S. Genetic association mapping and genome organization of maize. Curr. Opin. Biotechnol. 17, 155–160 (2006).

    Article  CAS  PubMed  Google Scholar 

  10. Huang, X. et al. Genome-wide association studies of 14 agronomic traits in rice landraces. Nat. Genet. 42, 961–967 (2010).

    Article  CAS  PubMed  Google Scholar 

  11. Huang, X. et al. Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat. Genet. 44, 32–39 (2011).

    Article  CAS  PubMed  Google Scholar 

  12. Gore, M.A. et al. A first-generation haplotype map of maize. Science 326, 1115–1117 (2009).

    Article  CAS  PubMed  Google Scholar 

  13. Yang, X. et al. Characterization of a global germplasm collection and its potential utilization for analysis of complex quantitative traits in maize. Mol. Breed. 28, 511–526 (2011).

    Article  Google Scholar 

  14. Li, H. et al. Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nat. Genet. 45, 43–50 (2013).

    Article  CAS  PubMed  Google Scholar 

  15. Yang, Q. et al. CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize. Proc. Natl. Acad. Sci. USA 110, 16969–16974 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Hung, H.Y. et al. ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize. Proc. Natl. Acad. Sci. USA 109, E1913–E1921 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Wisser, R.J. et al. Multivariate analysis of maize disease resistances suggests a pleiotropic genetic basis and implicates a GST gene. Proc. Natl. Acad. Sci. USA 108, 7339–7344 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Xue, Y. et al. Genome-wide association analysis for nine agronomic traits in maize under well-watered and water-stressed conditions. Theor. Appl. Genet. 126, 2587–2596 (2013).

    Article  CAS  PubMed  Google Scholar 

  19. Thirunavukkarasu, N. et al. Functional mechanisms of drought tolerance in subtropical maize (Zea mays L.) identified using genome-wide association mapping. BMC Genomics 15, 1182 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Setter, T.L. et al. 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 (2011).

    Article  CAS  PubMed  Google Scholar 

  21. Lu, Y. et al. 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 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Liu, S. et al. Genome-wide analysis of ZmDREB genes and their association with natural variation in drought tolerance at seedling stage of Zea mays L. PLoS Genet. 9, e1003790 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Yu, J. et al. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat. Genet. 38, 203–208 (2006).

    Article  CAS  PubMed  Google Scholar 

  24. Ferjani, A. et al. Keep an eye on PPi: the vacuolar-type H+-pyrophosphatase regulates postgerminative development in Arabidopsis. Plant Cell 23, 2895–2908 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Li, J. et al. Arabidopsis H+-PPase AVP1 regulates auxin-mediated organ development. Science 310, 121–125 (2005).

    Article  CAS  PubMed  Google Scholar 

  26. Doebley, J.F., Gaut, B.S. & Smith, B.D. The molecular genetics of crop domestication. Cell 127, 1309–1321 (2006).

    Article  CAS  PubMed  Google Scholar 

  27. Zuo, W. et al. A maize wall-associated kinase confers quantitative resistance to head smut. Nat. Genet. 47, 151–157 (2015).

    Article  CAS  PubMed  Google Scholar 

  28. Semagn, K. et al. Meta-analyses of QTL for grain yield and anthesis silking interval in 18 maize populations evaluated under water-stressed and well-watered environments. BMC Genomics 14, 313 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  29. Huang, C.H., Kuo, W.Y. & Jinn, T.L. Models for the mechanism for activating copper-zinc superoxide dismutase in the absence of the CCS Cu chaperone in Arabidopsis. Plant Signal. Behav. 7, 428–430 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Negi, N.P., Shrivastava, D.C., Sharma, V. & Sarin, N.B. Overexpression of CuZnSOD from Arachis hypogaea alleviates salinity and drought stress in tobacco. Plant Cell Rep. 34, 1109–1126 (2015).

    Article  CAS  PubMed  Google Scholar 

  31. Chen, Z. et al. Mutations in ABO1/ELO2, a subunit of holo-Elongator, increase abscisic acid sensitivity and drought tolerance in Arabidopsis thaliana. Mol. Cell. Biol. 26, 6902–6912 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Voitsik, A.M., Muench, S., Deising, H.B. & Voll, L.M. Two recently duplicated maize NAC transcription factor paralogs are induced in response to Colletotrichum graminicola infection. BMC Plant Biol. 13, 85–100 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Mao, H. et al. A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nat. Commun. 6, 8326 (2015).

    Article  CAS  PubMed  Google Scholar 

  34. Hu, H. et al. Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc. Natl. Acad. Sci. USA 103, 12987–12992 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Nakashima, K. et al. Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J. 51, 617–630 (2007).

    Article  CAS  PubMed  Google Scholar 

  36. Vainonen, J.P. et al. RCD1-DREB2A interaction in leaf senescence and stress responses in Arabidopsis thaliana. Biochem. J. 442, 573–581 (2012).

    Article  CAS  PubMed  Google Scholar 

  37. You, J. et al. The SNAC1-targeted gene OsSRO1c modulates stomatal closure and oxidative stress tolerance by regulating hydrogen peroxide in rice. J. Exp. Bot. 64, 569–583 (2013).

    Article  CAS  PubMed  Google Scholar 

  38. Sivankalyani, V., Geetha, M., Subramanyam, K. & Girija, S. Ectopic expression of Arabidopsis RCI2A gene contributes to cold tolerance in tomato. Transgenic Res. 24, 237–251 (2015).

    Article  CAS  PubMed  Google Scholar 

  39. Mitsuya, S., Taniguchi, M., Miyake, H. & Takabe, T. Disruption of RCI2A leads to over-accumulation of Na+ and increased salt sensitivity in Arabidopsis thaliana plants. Planta 222, 1001–1009 (2005).

    Article  CAS  PubMed  Google Scholar 

  40. Zhang, X., Liu, S. & Takano, T. Two cysteine proteinase inhibitors from Arabidopsis thaliana, AtCYSa and AtCYSb, increasing the salt, drought, oxidation and cold tolerance. Plant Mol. Biol. 68, 131–143 (2008).

    Article  CAS  PubMed  Google Scholar 

  41. Gaxiola, R.A. et al. Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc. Natl. Acad. Sci. USA 98, 11444–11449 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Park, S. et al. Up-regulation of a H+-pyrophosphatase (H+-PPase) as a strategy to engineer drought-resistant crop plants. Proc. Natl. Acad. Sci. USA 102, 18830–18835 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Maeshima, M. Vacuolar H(+)-pyrophosphatase. Biochim. Biophys. Acta 1465, 37–51 (2000).

    Article  CAS  PubMed  Google Scholar 

  44. Bak, G. et al. Rapid structural changes and acidification of guard cell vacuoles during stomatal closure require phosphatidylinositol 3,5-bisphosphate. Plant Cell 25, 2202–2216 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Kriegel, A. et al. Job sharing in the endomembrane system: vacuolar acidification requires the combined activity of V-ATPase and V-PPase. Plant Cell 27, 3383–3396 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Stitt, M. Product inhibition of potato tuber pyrophosphate:fructose-6-phosphate phosphotransferase by phosphate and pyrophosphate. Plant Physiol. 89, 628–633 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Lin, S.M. et al. Crystal structure of a membrane-embedded H+-translocating pyrophosphatase. Nature 484, 399–403 (2012).

    Article  CAS  PubMed  Google Scholar 

  48. Li, Y. et al. Chalk5 encodes a vacuolar H(+)-translocating pyrophosphatase influencing grain chalkiness in rice. Nat. Genet. 46, 398–404 (2014).

    Article  CAS  PubMed  Google Scholar 

  49. Knapp, S.J., Stroup, W.W. & Ross, W.M. Exact confidence intervals for heritability on a progeny mean basis. Crop Sci. 25, 192–194 (1985).

    Article  Google Scholar 

  50. Price, A.L. et al. Principal components analysis corrects for stratification in genome-wide association studies. Nat. Genet. 38, 904–909 (2006).

    Article  CAS  PubMed  Google Scholar 

  51. Falush, D., Stephens, M. & Pritchard, J.K. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Loiselle, B.A., Sork, V.L., Nason, J. & Graham, C. Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am. J. Bot. 82, 1420–1425 (1995).

    Article  Google Scholar 

  53. Bradbury, P.J. et al. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23, 2633–2635 (2007).

    Article  CAS  PubMed  Google Scholar 

  54. Zhang, Z. et al. Mixed linear model approach adapted for genome-wide association studies. Nat. Genet. 42, 355–360 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Kang, H.M. et al. Efficient control of population structure in model organism association mapping. Genetics 178, 1709–1723 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  56. Li, M.X., Yeung, J.M., Cherny, S.S. & Sham, P.C. 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 (2012).

    Article  CAS  PubMed  Google Scholar 

  57. Yang, W. et al. Combining high-throughput phenotyping and genome-wide association studies to reveal natural genetic variation in rice. Nat. Commun. 5, 5087 (2014).

    Article  CAS  PubMed  Google Scholar 

  58. Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Zhao, K. et al. Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat. Commun. 2, 467 (2011).

    Article  PubMed  CAS  Google Scholar 

  60. Ishida, Y., Hiei, Y. & Komari, T. Agrobacterium-mediated transformation of maize. Nat. Protoc. 2, 1614–1621 (2007).

    Article  CAS  PubMed  Google Scholar 

  61. Musick, G.J., Fairchild, M.L., Fergason, V.L. & Zuber, M.S. A method of measuring root volume in corn (Zea mays L.). Crop Sci. 5, 601–602 (1965).

    Article  Google Scholar 

  62. Li, B., Wei, A., Song, C., Li, N. & Zhang, J. Heterologous expression of the TsVP gene improves the drought resistance of maize. Plant Biotechnol. J. 6, 146–159 (2008).

    Article  CAS  PubMed  Google Scholar 

  63. Hsiao, Y.Y., Van, R.C., Hung, S.H., Lin, H.H. & Pan, R.L. Roles of histidine residues in plant vacuolar H(+)-pyrophosphatase. Biochim. Biophys. Acta 1608, 190–199 (2004).

    Article  CAS  PubMed  Google Scholar 

  64. Wilson, G.H., Grolig, F. & Kosegarten, H. Differential pH restoration after ammonia-elicited vacuolar alkalisation in rice and maize root hairs as measured by fluorescence ratio. Planta 206, 154–161 (1998).

    Article  CAS  Google Scholar 

  65. Yoo, S.D., Cho, Y.H. & Sheen, J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2, 1565–1572 (2007).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank T. Komori (Japan Tobacco, Inc.) for kindly providing us with the maize transformation plasmids pSBI and pSBII. Y. Ma helped in maize transformation vector construction. We would also like to thank S. Li and Z. Li for their excellent technical support in maize transformation and seed propagation. This research was supported by grants from the National High-Tech Research and Development Program of China (2012AA10A306-4), the National Basic Research Program of China (2012CB114302-4), Chinese Academy of Sciences grant (XDA08010206), and the National Natural Science Foundation of China (31471505) to F.Q.

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  1. Xianglan Wang and Hongwei Wang: These authors contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Plant Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing, China

    Xianglan Wang, Hongwei Wang, Shengxue Liu & Feng Qin

  2. Graduate University of the Chinese Academy of Sciences, Beijing, China

    Xianglan Wang & Hongwei Wang

  3. Department of Biology, Tokyo Gakugei University, Tokyo, Japan

    Ali Ferjani

  4. National Maize Improvement Center of China, Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing, China

    Jiansheng Li & Xiaohong Yang

  5. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, China

    Jianbing Yan

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Contributions

X.W. resequenced ZmVPP1, analyzed gene and protein expression levels, and performed Arabidopsis transformation and transgenic analysis and the yield test of transgenic maize in fields. H.W. carried out the GWAS of maize drought tolerance and identified the ZmVPP1 gene, and analyzed the phenotype of transgenic maize in the lab. S.L. helped with the phenotypic analysis of maize drought tolerance. X.Y., J.Y., and J.L. provided the maize materials and the SNP information, and X.Y. advised on the experiments. A.F. provided the fugu5 mutant seeds and advised on the experiments. F.Q. designed and advised on the experiments and wrote the manuscript.

Corresponding authors

Correspondence to Xiaohong Yang or Feng Qin.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Phenotypic variation of maize drought tolerance at the seedling stage in the natural variation population.

(a) Distribution of plant survival rate in a drought test (SR) of genotypes from different origins. Temperate origins contain non-stiff stalk (NSS) and stiff stalk (SS). (b) Box-plot of the SR of genotypes from different origins. The solid lines in the boxes denotes the median value; dashed lines indicate variability outside the upper and lower quartiles; and dots denote outliers.

Supplementary Figure 2 Analysis of conditional GWAS and two sub-population GWAS.

Manhattan plot of the conditional GWAS (a), GWAS of TST (c) and NSS (e) subpopulations. The dashed horizontal line depicts the significance threshold (P = 1.0 × 10-5). The SNPs locating within the candidate genes, identified by the GWAS, are labeled in red dots. The X-axis indicates the SNP location along the 10 chromosomes, with chromosomes separated by different colors; Y-axis is the -log10(Pobserved) for each analysis. Quantile-quantile plot of conditional GWAS (b), GWAS of TST (d) and NSS (f) subpopulations under GLM (black dots) and MLM (red dots).

Supplementary Figure 3 The BAC sequence of ZmVPP1CIMBL55 and its synteny with the B73 genomic sequence.

Red and blue arrows represent the generic region of ZmVPP1 and GRMZM2G105167 (the gene upstream from ZmVPP1), respectively. Homologous regions are indicated by numbered boxes. Transposons are indicated by empty arrows. Sequence synteny is indicated by light-blue shading.

Supplementary Figure 4 Comparison of the 3'-UTR of ZmVPP1B73 and ZmVPP1CIMBL55 on GFP expression.

The GFP induction rate under ABA and mannitol treatments. “CK” indicates that the transfected protoplasts were cultured under normal conditions. The GFP expression levels in the samples transfected by the empty vector “GFP-NosT” were defined as 1. pUbi:Luciferase is co-transfected and acts as a reference gene. The means and errors (s.d.) were calculated from at least three biological replicates.

Supplementary Figure 5 Investigation of the performance of ZmVPP1 transgenics under field conditions.

(a) Comparison of plant height, leaf number, leaf length, leaf width, leaf numbers above the ear (LAE), days to anthesis (DTA), days to silking (DTS), tassel length, tassel branch number (TBN), ear length, row number, kernel per row between WT and ZmVPP1 transgenic maize under watered conditions. Leaf length and width were measured on the ear leaf and data were obtained from at least 30 plants of each kind. (b) Representative photo of ears for each kind of plant. (c) Photosynthesis parameters (PS, SC, TR and WUE) were measured and calculated under the drought-2 conditions. Data were obtained from 8 seedlings. Error bars represent the s.d. and significance was derived from a two-sided t-test, * P < 0.05, ** P < 0.01.

Supplementary Figure 6 Phylogenetic tree of ZmVPP1 from different plant species and gene expression profile of the paralogous ZmVPP1 gene.

(a) The abbreviation in the gene code or name of “Zm” stands for Zea mays, “Os” for Oryza sativa; “Sb” for Sorghum bicolor; “At” for Arabidopsis thaliana; “Vr” for Vigna radiate; and “Th” for Thellungiella halophila. Bootstrap values from 1,000 replicates were indicated at each node and the scale represents branch length. (b) A heat map illustrating levels of type-I ZmVPP gene expression in fifteen different tissues from various developmental stages. Normalized gene expression values (Plant J. 66, 553–563, 2011) are shown in different colors that represent the levels of expression as indicated by the scale bar.

Supplementary Figure 7 The original photo of western-blot analysis of the transgenic maize with increased ZmVPP1 protein levels as detected by ZmVPP1 anti-serum.

WT denotes the transgenic-negative siblings; “others” denotes a failed sample; “OE” denotes the independent transgenic lines with enhanced ZmVPP1 expression. CBB staining indicates equivalent loading of samples.

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Wang, X., Wang, H., Liu, S. et al. Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings. Nat Genet 48, 1233–1241 (2016). https://doi.org/10.1038/ng.3636

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