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.
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
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
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
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
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
Classen MM, Shaw RH (1970) Water deficit effects on corn. II. Grain components. Agron J 62:652–655
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
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
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
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
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
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
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
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
Haley CS, Knott SA (1992) A simple regression method for mapping quantitative trait loci in line crosses using flanking markers. Heredity 69:315–324
Jansen RC, Nap JP (2001) Genetical genomics: the added value from segregation. Trends Genet 17:388–391
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
Liavonchanka A, Feussner I (2006) Lipoxygenases: occurrence, functions and catalysis. J Plant Physiol 163:348–357
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
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
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
Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19
Moffat AS (2002) Plant genetics. Finding new ways to protect drought-stricken plants. Science 296:1226–1229
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
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
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
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
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
Porta H, Rocha-Sosa M (2002) Plant lipoxygenases. Physiological and molecular features. Plant Physiol 130:15–21
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
Risch NJ (2000) Searching for genetic determinants in the new millennium. Nature 405:847–856
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
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
Salvi S, Tuberosa R (2005) To clone or not to clone plant QTLs: present and future challenges. Trends Plant Sci 10:297–304
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
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
Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302
Shah N, Paulsen G (2003) Interaction of drought and high temperature on photosynthesis and grain-filling of wheat. Plant Soil 257:219–226
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227
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
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
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
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
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
Wang D, Nettleton D (2006) Identifying genes associated with a quantitative trait or quantitative trait locus via selective transcriptional profiling. Biometrics 62:504–514
Weigel D, Nordborg M (2005) Natural variation in Arabidopsis. How do we find the causal genes? Plant Physiol 138:567–568
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
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
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
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
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
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
Corresponding author
Additional information
Communicated by K. Shirasu.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-008-0401-y