Abstract
Water-deficit stress during meiosis is one of the most serious threats to crop production. To elucidate the mechanisms of the response to water-deficit stress in the reproductive organs of maize, we have characterized the changes in transcription that occur during meiosis in the tassels and floret formation in the ears following water deficit stress. We used oligo microarray analysis, which included 57,452 transcripts representing more than 30,000 identifiable unique maize genes, and combined this with reverse Northern blot analysis. After 7 days of stress, immature tassels and ears differed considerably in their transcriptional responses, and the majority of changes were organ specific. In the tassels, 1,513 transcripts were differentially expressed (by threefold or greater) with 62% of these being upregulated by water stress. In the ears, 202 transcripts were differentially expressed with 95% being upregulated by water stress. Most of these transcripts have not been previously reported to be associated with water stress. Only 74 of these transcripts were co-regulated in the two organs. The stress-regulated transcripts are involved in a broad range of cellular and biochemical activities. The most notable may function in carbohydrate metabolism, particular in sucrose, trehalose and raffinose metabolism, and in cell wall metabolism in the tassels. Collectively, these data suggest that the transcripts differentially expressed during reproductive organic development may represent candidate genes for dissecting molecular mechanism of this important biological process in response to water-deficit stress.
Similar content being viewed by others
References
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
Arioli T, Peng L, Betzner AS, Burn J, Wittke W, Herth W, Camilleri C, Hofte H, Plazinski J, Birch R, Cork A, Glover J, Redmond J, Williamson RE (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279:717–720
Betrán FJ, Beck D, Bänziger M, Edmeades GO (2003) Genetic analysis of inbred and hybrid grain yield under stress and nonstress environments in tropical maize. Crop Sci 43:807–817
Brenac P, Horbowicz M, Downer SM, Dickermn AM, Smith ME, Obendorf RL (1997) Raffinose accumulation related to desiccation tolerance during maize (Zea mays L) seed development and maturation. J Plant Physiol 150:481–488
Bruce WB, Edmeades GO, Barker TC (2002) Molecular and physiological approaches to maize improvement for drought tolerance. J Exp Bot 53:13–25
Carlson SJ, Chourey PS, Helentjaris T, Datta R (2002) Gene expression studies on developing kernels of maize sucrose synthase (SuSy) mutants show evidence for a third SuSy gene. Plant Mol Biol 49:15–29
Chen Z, Hong X, Zhang H, Wang Y, Li X, Zhu JK, Gong Z (2005) Disruption of the cellulose synthase gene, AtCesA8/IRX1, enhances drought and osmotic stress tolerance in Arabidopsis. Plant J 43:273–283
Cho SK, Kim JE, Park JA, Eom TJ, Kim WT (2006) Constitutive expression of abiotic stress-inducible hot pepper CaXTH3, which encodes a xyloglucan endotransglucosylase/hydrolase homolog, improves drought and salt tolerance in transgenic Arabidopsis plant. FEBS Lett 580:3136–3144
Cochard H, Froux F, Mayr S, Coutand C (2004) Xylem wall collapse in water-stressed pine needles. Plant Physiol 134:401–408
Denmead OT, Show RH (1960) The effects of soil moisture stress at different stages of growth on the development and yield of corn. Agron J 52:272–274
Dorion S, Lalonde S, Saini HS (1996) Induction of male sterility in wheat by meiotic stage water deficit is preceded by a decline in invertase activity and changes in carbohydrate metabolism in anthers. Plant Physiol 111:137–145
Downey LA (1969) Crop density and water use studies with irrigated maize (Zea mays L) on Sodic clay soils M. Sc thesis University of Sydney, Sydney
Duncan KA, Hardin SC, Huber SC (2005) The third sucrose synthase in Zea mays (SUS3) is a ubiquitous protein that is phosphorylated and membrane associated (abstract no 22005). In: Plant Biology, July 16–20, Seattle American Society of Plant Biologists, Rockville
Eastmond PJ, van Dijken AJH, Spielman M, Kerr A, Tissier AF, Dickinson HG, Jones JDG, Smeekens SC, Graham IA (2002) Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. Plant J 29:225–235
Edmeades GO, Bolaños J, Chapman SC, Lafitte HR, Bänzige M (1999) Selection improves drought tolerance in tropical maize populations: I Gains in biomass, grain yield, and harvest index. Crop Sci 39:1306–1315
Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R-27R
Fridman E, Pleban T, Zamir D (2000) A recombination hotspot delimits a wild-species quantitative trait locus for tomato sugar content to 484 bp within an invertase gene. Proc Natl Acad Sci USA 97:4718–4723
Fridman E, Carrari F, Liu YS, Fernie AR, Zamir D (2004) Zooming in on a quantitative trait for tomato yield using interspecific introgressions. Science 305:1786–1789
Garcion C, Applimath FRI, Métraux JP (2006) FiRe and microarray: a fast answer to burning questions. Trends Plant Sci 11:320–322
Goddijn OJM, van Dun K (1999) Trehalose metabolism in plants. Trends Plant Sci 4:315–319
Holland N, Holland D, Helentjaris T, Dhugga KS, Xoconostle-Cazares B, Delmer DP (2000) A comparative analysis of the plant cellulose synthase (CesA) gene family. Plant Physiol 123:1313–1324
Huang X, Madan A (1999) CAP3: A DNA sequence assembly program. Genome Res 9:868–877
Imin N, Kerim T, Rolfe BG, Weinman JJ (2004) Effect of early cold stress on the maturation of rice anthers. Proteomics 4:1873–1882
Ismail A, Hall A, Close T (1999) Allelic variation of a dehydrin gene cosegregates with chilling tolerance during seedling emergence. Proc Natl Acad Sci USA 96:9
Jia J, Fu J, Zheng J, Zhou X, Huai J, Wang J, Wang M, Zhang Y, Chen X, Zhang J, Zhao J, Su Z, Lv Y, Wang G (2006) Annotation and expression profile analysis of 2073 full-length cDNAs from stress-induced maize (Zea mays L) seedlings. Plant J 48:710–727
Keller R, Brearley CA, Trethewey RN, Müller-Röber B (1998) Reduced inositol content and altered morphology in transgenic potato plants inhibited for 1D-myo-inositol 3-phosphate synthase. Plant J 16:403–410
Lee JM, Williams ME, Tingey SV, Rafalski JA (2002) DNA array profiling of gene expression changes during maize embryo development. Funct Integr Genomics 2:13–27
McCarty DR (1986) A simple method for extraction of RNA from maize tissues. MNL 60,61
Mecham BH, Klus GT, Strovel J, Augustus M, Byrne D, Bozso P, Wetmore DZ, Mariani TJ, Kohane IS, Szallasi Z (2004) Sequence-matched probes produce increased cross-platform consistency and more reproducible biological results in microarray-based gene expression measurements. Nucleic Acids Res 32:e74
Minic Z, Jouanin L (2006) Plant glycoside hydrolases involved in cell wall polysaccharide degradation. Plant Physiol Biochem 44:435–449
Ouyang B, Yang T, Li H, Zhang L, Zhang Y, Zhang J, Fei Z, Ye Z (2007) Identification of early salt stress response genes in tomato root by suppression subtractive hybridization and microarray analysis. J Exp Bot 58:507–520
Quan R, Shang M, Zhang J (2004) Improved chilling tolerance by transformation with betA gene for the enhancement of glycinebetaine synthesis in maize. Plant Sci 166:141–149
Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755–1767
Roitsch T, Gonzälez MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9:606–613
Saini HS (1997) Effects of water stress on male gametophyte development in plants. Sex Plant Reprod 10:67–73
Schena M, Shalon D, Davis RW, Brown PO (1995) Quantitative monitoring of gene expression patterns with a complimentary DNA microarray. Science 270:467–470
Subbaiah CC, Duncan APK, Rhoads DM, Huber SC, Sachs MM (2006) Mitochondrial localization and putative signaling function of sucrose synthase in maize. J Biol Chem 23:15625–15635
Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important role of drought and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426
Tuberosa R, Salvi S, Sanguineti M, Landi P, Maccaferri M, Conti S (2002) Mapping QTLs regulating morphophysiological traits and yield: case studies, shortcomings and perspectives in drought-stressed maize. Ann Bot 89:941–963
Wang H, Miyazak S, Kawai K, Deyholos M, Galbraith DW, Bohnert HJ (2003) Temporal progression of gene expression responses to salt shock in maize roots. Plant Mol Biol 52:873–891
Wu Y, Jeong BR, Fry SC, Boyer JS (2005) Change in XET activities, cell wall extensibility and hypocotyl elongation of soybean seedlings at low water potential. Planta 220:593–601
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
Zheng J, Zhao J, Tao Y, Wang J, Liu Y, Fu J, Jin Y, Gao P, Zhang J, Bai Y, Wang G (2004) Isolation and analysis of water stress induced genes in maize seedlings by subtractive PCR and cDNA macroarray. Plant Mol Biol 55:807–823
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 Crop Res 75:111–121
Acknowledgments
The authors thank Dr. Roberta Greenwood and Dr. Jian Li for critically reading and improving the English manuscript, as well as Shi Yan for technical assistance.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by J. Zou.
Yunlong Zhuang and Guijie Ren have contributed equally to this paper.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhuang, Y., Ren, G., Yue, G. et al. Effects of water-deficit stress on the transcriptomes of developing immature ear and tassel in maize. Plant Cell Rep 26, 2137–2147 (2007). https://doi.org/10.1007/s00299-007-0419-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-007-0419-3