Skip to main content
Log in

Addressing drought tolerance in maize by transcriptional profiling and mapping

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

In order to unravel the genetic architecture underlying plant response to drought, we adopted an integrated approach, combining transcript profiling and quantitative trait loci (QTL) mapping. In fact, improving plant tolerance to water stress is an important, but, at the same time, a difficult task, since plant tolerance is the result of many complex mechanisms acting at different levels of plant organization, and its genetic basis is largely unknown. The phenotypic data, concerning yield components and flowering time, of a population of 142 maize Recombinant Inbred Lines (RILs), grown under well watered conditions or under water stress, were submitted to linkage analysis to detect drought-tolerance QTLs. Thirty genomic regions containing 50 significant QTLs distributed on nine chromosomes were identified. At the same time, a customized targeted oligoarray was used to monitor the expression levels of 1,000 genes, representative of the immature maize kernel transcriptome. Using this DNA array we compared transcripts from 10 days after pollination kernels of two susceptible and two drought tolerant genotypes (extracted from our RILs) grown under control and water stress field conditions. Two hundred and fifty-two genes were significantly affected by stress in at least one genotype. From a set of these, 49 new molecular markers were developed. By mapping most of them and by in silico mapping other regulated sequences, 88 differentially expressed genes were localized onto our linkage map, which, added to the existing 186 markers, brought their total number on the map to 274. Twenty-two of the 88 differentially expressed genes mapped in the same chromosomal segments harbouring QTLs for tolerance, thus representing candidate genes for further functional studies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abiola O, Angel JM, Avner P, Bachmanov AA, Belknap JK, Bennett B, Blankenhorn EP, Blizard DA, Bolivar V, Brockmann GA, Buck KJ, Bureau JF, Casley WL, Chesler EJ, Cheverud JM, Churchill GA, Cook M, Crabbe JC, Crusio WE, Darvasi A, de Haan G, Dermant P, Doerge RW, Elliot RW, Farber CR, Flaherty L, Flint J, Gershenfeld H, Gibson JP, Gu J, Gu W, Himmelbauer H, Hitzemann R, Hsu HC, Hunter K, Iraqi FF, Jansen RC, Johnson TE, Jones BC, Kempermann G, Lammert F, Lu L, Manly KF, Matthews DB, Medrano JF, Mehrabian M, Mittlemann G, Mock BA, Mogil JS, Montagutelli X, Morahan G, Mountz JD, Nagase H, Nowakowski RS, O’Hara BF, Osadchuk AV, Paigen B, Palmer AA, Peirce JL, Pomp D, Rosemann M, Rosen GD, Schalkwyk LC, Seltzer Z, Settle S, Shimomura K, Shou S, Sikela JM, Siracusa LD, Spearow JL, Teuscher C, Threadgill DW, Toth LA, Toye AA, Vadasz C, Van Zant G, Wakeland E, Williams RW, Zhang HG, Zou F (2003) The nature and identification of quantitative trait loci: a community’s view. Nat Rev Genet 4:911–916

    PubMed  Google Scholar 

  • Andjelkovic V, Thompson R (2006) Changes in gene expression in maize kernel in response to water and salt stress. Plant Cell Rep 25:71–79

    Article  PubMed  CAS  Google Scholar 

  • Barnabas B, Jager K, Feher A (2008) The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ 31:11–38

    PubMed  CAS  Google Scholar 

  • Blüthgen N, Brand K, Cajavec B, Swat M, Herzel H, Beule D (2004) Profiling of gene groups utilizing gene ontology—a statistical framework. arXiv:q-bio.GN/0407034 1:1

  • Boyer JS, Westgate ME (2004) Grain yields with limited water. J Exp Bot 55:2385–2394

    Article  PubMed  CAS  Google Scholar 

  • Calinski T, Kaczmarek Z, Krajewski P, Frova C, Sari-Gorla M (2000) A multivariate approach to the problem of QTL localization. Heredity 84:303–310

    Article  PubMed  CAS  Google Scholar 

  • Classen MM, Shaw RH (1970) Water deficit effects on corn. II. Grain components. Agron J 62:652–655

    Article  Google Scholar 

  • Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  PubMed  CAS  Google Scholar 

  • de Vienne D, Leonardi A, Damerval C, Zivy M (1999) Genetics of proteome variation for QTL characterization: application to drought-stress responses in maize. J Exp Bot 50:303–309

    Article  Google Scholar 

  • Dias AP, Braun EL, McMullen MD, Grotewold E (2003) Recently duplicated maize R2R3 Myb genes provide evidence for distinct mechanisms of evolutionary divergence after duplication. Plant Physiol 131:610–620

    Article  PubMed  CAS  Google Scholar 

  • Frova C, Krajewski P, di Fonzo N, Villa M, Sari-Gorla M (1999) Genetic analysis of drought tolerance in maize by molecular markers I. Yield components. Theor Appl Genet 99:280–288

    Article  Google Scholar 

  • Fu B-Y, Xiong J-H, Zhu L-H, Zhao X-Q, Xu H-X, Gao Y-M, Li Y-S, Xu J-L, Li Z-K (2007) Identification of functional candidate genes for drought tolerance in rice. Mol Gen Genomics 278:599–609

    Article  CAS  Google Scholar 

  • Gao M, Wanat J, Stinard PS, James MG, Myers AM (1998) Characterization of dull1, a maize gene coding for a novel starch synthase. Plant Cell 10:399–412

    Article  PubMed  CAS  Google Scholar 

  • Gu R, Zhao L, Zhang Y, Chen X, Bao J, Zhao J, Wang Z, Fu J, Liu T, Wang J, Wang G (2006) Isolation of a maize beta-glucosidase gene promoter and characterization of its activity in transgenic tobacco. Plant Cell Rep 25:1157–1165

    Article  PubMed  CAS  Google Scholar 

  • Gupta AK, Kaur N (2005) Sugar signalling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants. J Biosci 30:761–776

    Article  PubMed  CAS  Google Scholar 

  • Haley CS, Knott SA (1992) A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity 69:315–324

    PubMed  CAS  Google Scholar 

  • Jansen RC, Nap JP (2001) Genetical genomics: the added value from segregation. Trends Genet 17:388–391

    Article  PubMed  CAS  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  PubMed  CAS  Google Scholar 

  • Liavonchanka A, Feussner I (2006) Lipoxygenases: occurrence, functions and catalysis. J Plant Physiol 163:348–357

    Article  PubMed  CAS  Google Scholar 

  • Lu G, Tang J, Yan J, Ma X, Li J, Chen S, Ma J, Liu Z, LiZhu E, Zhang Y, Dai J (2006) Quantitative trait loci mapping of maize yield and its components under different water treatments at flowering time. J Integr Plant Biol 48:1233–1243

    Article  CAS  Google Scholar 

  • McLaughlin JE, Boyer JS (2004a) Glucose localization in maize ovaries when kernel number decreases at low water potential and sucrose is fed to the stems. Ann Bot (Lond) 94:75–86

    Article  CAS  Google Scholar 

  • McLaughlin JE, Boyer JS (2004b) Sugar-responsive gene expression, invertase activity, and senescence in aborting maize ovaries at low water potentials. Ann Bot (Lond) 94:675–689

    Article  CAS  Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    Article  PubMed  CAS  Google Scholar 

  • Moffat AS (2002) Plant genetics. Finding new ways to protect drought-stricken plants. Science 296:1226–1229

    Article  PubMed  CAS  Google Scholar 

  • Nemchenko A, Kunze S, Feussner I, Kolomiets M (2006) Duplicate maize 13-lipoxygenase genes are differentially regulated by circadian rhythm, cold stress, wounding, pathogen infection, and hormonal treatments. J Exp Bot 57:3767–3779

    Article  PubMed  CAS  Google Scholar 

  • Nguyen TT, Klueva N, Chamareck V, Aarti A, Magpantay G, Millena AC, Pathan MS, Nguyen HT (2004) Saturation mapping of QTL regions and identification of putative candidate genes for drought tolerance in rice. Mol Genet Genomics 272:35–46

    Article  PubMed  CAS  Google Scholar 

  • Onodera Y, Suzuki A, Wu CY, Washida H, Takaiwa F (2001) A rice functional transcriptional activator, RISBZ1, responsible for endosperm-specific expression of storage protein genes through GCN4 motif. J Biol Chem 276:14139–14152

    PubMed  CAS  Google Scholar 

  • Pelleschi S, Leonardi A, Rocher J, Cornic G, de Vienne D, Thévenot C, Prioul J (2006) Analysis of the relationships between growth, photosynthesis and carbohydrate metabolism using quantitative trait loci (qtls) in young maize plants subjected to water deprivation. Mol Breed 17:21–39

    Article  CAS  Google Scholar 

  • Perez-Enciso M, Toro M, Tenenhaus M, Gianola D (2003) Combining gene expression and molecular marker information for mapping complex trait genes: a simulation study. Genetics 164:1597–1606

    PubMed  CAS  Google Scholar 

  • Porta H, Rocha-Sosa M (2002) Plant lipoxygenases. Physiological and molecular features. Plant Physiol 130:15–21

    Article  PubMed  CAS  Google Scholar 

  • Prioul J, Pelleschi S, Sene M, Theevenot C, Causse M, de Vienne D, Leonardi A (1999) From QTLs for enzyme activity to candidate genes in maize. J Exp Bot 50:1281–1288

    Article  CAS  Google Scholar 

  • Risch NJ (2000) Searching for genetic determinants in the new millennium. Nature 405:847–856

    Article  PubMed  CAS  Google Scholar 

  • Rizhsky L, Liang H, Mittler R (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol 130:1143–1151

    Article  PubMed  CAS  Google Scholar 

  • Rizhsky L, Liang H, Shulaev V, Davletova S, Mittler R (2004) When defence pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696

    Article  PubMed  CAS  Google Scholar 

  • Salvi S, Tuberosa R (2005) To clone or not to clone plant QTLs: present and future challenges. Trends Plant Sci 10:297–304

    Google Scholar 

  • Sari-Gorla M, Calinski T, Kaczmarek Z, Krajewski P (1997) Detection of QTLxenviroment interaction in maize by least squares interval mapping method. Heredity 78:146–157

    Google Scholar 

  • Sari-Gorla M, Krajewski P, Di Fonzo N, Villa M, Frova C (1999) Genetic analysis of drought tolerance in maize by molecular markers. II. Plant height and flowering. Theor Appl Genet 99:289–295

    Article  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  PubMed  CAS  Google Scholar 

  • Shah N, Paulsen G (2003) Interaction of drought and high temperature on photosynthesis and grain-filling of wheat. Plant Soil 257:219–226

    Article  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    Article  PubMed  CAS  Google Scholar 

  • Soleimani VD, Baum BR, Johnson DA (2003) Efficient validation of single nucleotide polymorphisms in plants by allele-specific PCR, with an example from barley. Plant Mol Biol Rep 21:281–288

    Article  CAS  Google Scholar 

  • Szalma SJ, Hostert BM, Ledeaux JR, Stuber CW, Holland JB (2007) QTL mapping with near-isogenic lines in maize. Theor Appl Genet 114:1211–1228

    Article  PubMed  CAS  Google Scholar 

  • Taira T, Ohnuma T, Yamagami T, Aso Y, Ishiguro M, Ishihara M (2002) Antifungal activity of rye (Secale cereale) seed chitinases: the different binding manner of class I and class II chitinases to the fungal cell walls. Biosci Biotechnol Biochem 66:970–977

    Article  PubMed  CAS  Google Scholar 

  • Tuberosa R, Salvi S, Sanguineti MC, Landi P, Maccaferri M, Conti S (2002) Mapping QTLs regulating morpho-physiological traits and yield: case studies, shortcomings and perspectives in drought-stressed maize. Ann Bot (Lond) 89 Spec No:941–963

  • Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci 98:5116–5121

    Article  PubMed  CAS  Google Scholar 

  • Vargas M, FAv Eeuwijk, Crossa J, Ribaut JM (2006) Mapping QTLs and QTL x environment interaction for CIMMYT maize drought stress program using factorial regression and partial least squares methods. Theor Appl Genet 112:1009–1023

    Article  PubMed  CAS  Google Scholar 

  • Wang D, Nettleton D (2006) Identifying genes associated with a quantitative trait or quantitative trait locus via selective transcriptional profiling. Biometrics 62:504–514

    Article  PubMed  Google Scholar 

  • Weigel D, Nordborg M (2005) Natural variation in Arabidopsis. How do we find the causal genes? Plant Physiol 138:567–568

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yu LX, Setter TL (2003) Comparative transcriptional profiling of placenta and endosperm in developing maize kernels in response to water deficit. Plant Physiol 131:568–582

    Article  PubMed  CAS  Google Scholar 

  • Zhao TY, Corum JWIII, Mullen J, Meeley RB, Helentjaris T, Martin D, Downie B (2006) An alkaline alpha -galactosidase transcript is present in maize seeds and cultured embryo cells, and accumulates during stress. Seed Sci Res 16:107–121

    Article  CAS  Google Scholar 

  • Zhuang Y, Ren G, Yue G, Li Z, Qu X, Hou G, Zhu Y, Zhang J (2007) Effects of water-deficit stress on the transcriptomes of developing immature ear and tassel in maize. Plant Cell Rep 26:2137–2147

    Article  PubMed  CAS  Google Scholar 

  • Zinselmeier C, Sun Y, Helentjaris T, Beatty M, Yang S, Smith H, Habben J (2002) The use of gene expression profiling to dissect the stress sensitivity of reproductive development in maize. Field Crops Res 75:111–121

    Google Scholar 

Download references

Acknowledgments

The research was supported by the Italian Ministry of University and Research (FIRB 2001 and PRIN 2006). The cooperation with P. Krajewski was made possible by the agreement on scientific cooperation between Italian National Research Council (CNR) and Polish Academy of Sciences (PAN). The Authors thank Marzio Villa for his skilful technical assistance and Natale Di Fonzo for hosting the experimental fields at the C. R. A. Experimental Institute for Cereal Research, in Foggia, Italy.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mirella Sari-Gorla.

Additional information

Communicated by K. Shirasu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

(DOC 95 kb)

(DOC 976 kb)

(DOC 36 kb)

(DOC 187 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Marino, R., Ponnaiah, M., Krajewski, P. et al. Addressing drought tolerance in maize by transcriptional profiling and mapping. Mol Genet Genomics 281, 163–179 (2009). https://doi.org/10.1007/s00438-008-0401-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-008-0401-y

Keywords

Navigation