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Genetic variability for physiological traits under drought conditions and differential expression of water stress-associated genes in sunflower (Helianthus annuus L.)

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Abstract

Genotypic variation for water status and gas exchange parameters under different water treatments (well-watered and water-stressed plants before and after rehydration) were investigated in a population of recombinant inbred lines (RILs) of sunflower (Helianthus annuus L.). Afterwards, four RILs and parental lines presenting contrasting responses to dehydration and rehydration were selected to determine the differential expression of four water-stress associated genes: aquaporin, dehydrin, leafy cotyledon1-like protein and fructose-1,6 bisphosphatase. Water stress revealed a high genetic variability for water status and gas exchange parameters when compared with well-watered genotypes. Genetic gain when selected RILs were compared with the best parent was significant for most traits due to transgressive segregation. QTL mapping and graphical genotyping showed that RILs carrying different genomic regions for some QTLs presented also physiological different characteristics as well as gene expression patterns. The expression level of aquaporin genes in leaves of four RILs and their parents was down regulated by water stress and was associated with relative water content (RWC). Down-regulation was also associated with genomic regions having alleles with negative effects on plant water status. The level of dehydrin transcripts increased in leaves of all studied RILs in response to water stress. Transcript accumulations of dehydrin and leafy cotyledon1-like genes, likely involved in protective tolerance processes, were not correlated directly with plant water status or QTL effects. Down-regulation of fructose-1,6 bisphosphatase was observed under water stress. Net photosynthesis rate (Pn) and the fructose-1,6 bisphosphatase gene expression levels were associated mainly after rehydration. This phenomenon indicates an association between physiological response to water stress and differential expression of water-stress related genes.

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References

  • Al-Chaarani G, Gentzbittel L, Huang X, Sarrafi A (2004) Genotypic variation and identification of QTLs for agronomic traits using AFLP and SSR in recombinant inbred lines of sunflower (Helianthus annuus L). Theor Appl Genet 109:1353–1360

    Article  PubMed  Google Scholar 

  • Bajaj S, Targolli J, Liu LF, Ho THD, Wu R (1999) Transgenic approaches to increase dehydration-stress tolerance in plants. Mol Breed 5:493–503

    Article  CAS  Google Scholar 

  • Baker J, Steele C, Dure L (1988) Sequence and characterization of 6 Lea proteins and their genes from cotton. Plant Mol Biol 11:277–291

    Article  CAS  Google Scholar 

  • Basten CJ, Weir BS, Zeng ZB (2002) QTL cartographer version 1.16: program in statistical genetics. Department of Statistics, North Carolina State University, Raleigh

  • Blum A (1989) Osmotic adjustment and growth in barley genotypes under drought stress. Crop Sci 29:230–233

    Article  Google Scholar 

  • Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111

    Article  PubMed  CAS  Google Scholar 

  • Boominathan P, Shukla R, Kumar A, Manna D, Negi D, Verma PK, Debasis C (2004) Long term transcript accumulation during the development of dehydration adaptation in Cicer arietinum. Plant Physiol 135:1608–1620

    Article  PubMed  CAS  Google Scholar 

  • Bray EA (2002) Classification of genes differentially expressed during water-deficit stress in Arabidopsis thaliana: an analysis using microarray and differential expression data. Ann Bot 89 Spec No:803–811

    Google Scholar 

  • Bray EA (2004) Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. J Exp Bot 55:2331–2341

    Article  PubMed  CAS  Google Scholar 

  • Bruce WB, Edmeades GO, Barker TC (2002) Molecular and physiological approaches to maize improvement for drought tolerance. J Exp Bot 53:13–25

    Article  PubMed  CAS  Google Scholar 

  • Burke JJ (2001) Identifcation of genetic diversity and mutations in higher plant acquired thermotolerance. Physiol Plant 112:167–170

    Article  CAS  Google Scholar 

  • Cellier F, Conejero G, Breitler JC, Casse F (1998) Molecular and physiological responses to water deficit in drought-tolerant and drought-sensitive lines of sunflower accumulation of dehydrin transcripts correlates with tolerance. Plant Physiol 116:319–328

    Article  PubMed  CAS  Google Scholar 

  • Charles SA, Halliwell B (1981) Light activation of fructose bisphosphatase in isolated spinach chloroplasts and deactivation by hydrogen peroxide. Planta 151:242–246

    Article  CAS  Google Scholar 

  • Close TJ, Fenton RD, Moonan F (1993) A view of plant dehydrins using antibodies specific to the carboxy terminal peptide. Plant Mol Biol 23:279–286

    Article  PubMed  CAS  Google Scholar 

  • Conory JP, Virgona JM, Smillie RM, Barlow EW (1988) Influence of drought acclimation and CO2 enrichment on osmotic adjustment and chlorophyll a fluorescence of sunflower during drought. Plant Physiol 86:1108–1115

    Google Scholar 

  • Cornic G (2000) Drought stress inhibits photosynthesis by decreasing stomatal aperture—not by affecting ATP synthesis. Trends Plant Sci 5:187–188

    Article  Google Scholar 

  • Dure III L, Crouch M, Harada J, Ho T-HD, Mundy J, Quatrano R, Thomas T, Sung ZR (1989) Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol Bio 12:475–486

    Article  CAS  Google Scholar 

  • Fambrini M, Durante C, Cionini G, Geri C, Giorgetti L, Michelotti V, Salvini M, Pugliesi C (2006) Characterization of LEAFY COTYLEDON1-LIKE gene in Helianthuss annuus and its relationship with zygotic and somatic embryogenesis. Dev Genes Evol 216:253–264

    Article  PubMed  CAS  Google Scholar 

  • Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plant: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189

    Article  PubMed  CAS  Google Scholar 

  • Hervé D, Fabre F, Flores Berrios E, Leroux N, Al charani Gh, Planchon C, Sarrafi A, Gentzbittel L (2001) QTL analysis of photosynthesis and water status traits in sunflower (Helianthus annuus L.) under green house condition. J Exp Bot 52:1857–1864

    Article  PubMed  Google Scholar 

  • Hewezi T, Petitprez M, Gentzbittel L (2006) Primary metabolic pathways and signal transduction in sunflower (Helianthus annuus L.): comparison of transcriptional profiling in leaves and immature embryos using cDNA microarray. Planta 223:948–964

    Article  PubMed  CAS  Google Scholar 

  • Holmberg N, Bulow L (1998) Improving stress tolerance in plants by gene transfer. Trends Plant Sci 3:61–66

    Article  Google Scholar 

  • Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403

    Article  PubMed  CAS  Google Scholar 

  • Jamaux I, Steinmetz A, Belhasen E (1997) Looking for molecular and physiological markers for osmotic adjustment in sunflower. New Phytol 137:117–127

    Article  CAS  Google Scholar 

  • Jang JY, Kim DG, Kim YO, Kim JS , Kang H (2004) An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol Biol 54:713–725

    Article  PubMed  CAS  Google Scholar 

  • Joshi CP, Kluveva NY, Morrow KJ, Nguyen HT (1997) Expression of a unique plastid localized heat shock protein is genetically linked to acquired thermotolerance in wheat. Theor Appl Genet 95:834–841

    Article  CAS  Google Scholar 

  • Krishnan M, Nguyen HT, Burke JJ (1989) Heat shock protein synthesis and thermotolerance in wheat. Plant Physiol 90:140–145

    Article  PubMed  CAS  Google Scholar 

  • Lawlor DW (1995) The effects of water deficit on photosynthesis In: Smirnoff N (ed) Environment and plant metabolism flexibility and acclimation. BIOS Scientific publishers, Oxford

    Google Scholar 

  • Lawlor DW (2002) Limitation of photosynthesis in water-stressed leaves: stomata vs metabolism and the role of ATP. Ann Bot 89:871–885

    Article  PubMed  CAS  Google Scholar 

  • Lawlor DW , Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficit in higher plants. Plant Cell Environ 25:275–294

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  PubMed  CAS  Google Scholar 

  • Luu DT, Maurel M (2005) Aquaporins in the challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28:85–96

    Article  CAS  Google Scholar 

  • Martre P, Morillon R, Barrieu F, Gretchen BN, Park SN, Maarten JC (2002) Plasma membrane aquaporin play a significant role during recovery from water deficit. Plant Physiol 130:2101–2110

    Article  PubMed  CAS  Google Scholar 

  • Maury P, Mojayad F, Berger M, Planchon C (1996) Photosynthesis response to drought acclimation in two sunflower genotypes. Physiol Plant 98:57–66

    Article  CAS  Google Scholar 

  • Maury P, Berger M, Mojayad F, Planchon C (2000) Leaf water characteristics and drought acclimation in sunflower genotypes. Plant Soil 223:153–160

    Article  CAS  Google Scholar 

  • Moons A, Bauw G, Dekeyser R, Von Montagu M, Van Der Straeten D (1995) Novel ABA responsive proteins in vegetative rice tissue. Curr Topics Plant Physiol 10:288–289

    Google Scholar 

  • Morgan J M (1984) Osmoregulation and water stress in higher plants. Annu Rev Plant Physiol 35:299–319

    Article  Google Scholar 

  • Ober ES, Le Bloa M, Clark C JA, Royal A, Jaggard K W, Pidgeon J D (2005) Evaluation of physiological traits as indirect selection criteria for drought tolerance in sugar beet. Field Crop Res 91:231–249

    Article  Google Scholar 

  • Oono Y, Seki M, Nnjo T, Narusaka M, Fujita M, Satoh R, Satou M, Sakurai T, Ishida J, Akiyama K, Lida K, Maruyama K, Satoh S, Yamaguchi-Shinozaki K, Shinozaki K (2003) Monitoring expression profile of Arabidopsis gene expression during rehydration process after dehydration using ca 7000 full-lengh cDNA microarray. Plant J 34:868–887

    Article  PubMed  CAS  Google Scholar 

  • Ouvrard O, Cellier F, Ferrare K, Tousch D, Lamaze T, Dupuis J-M , Casse-Delbart F (1996) Identification and expression of water stress- and abscisic acid-regulated genes in a drought-tolerant sunflower genotype. Plant Mol Biol 31:819–829

    Article  PubMed  CAS  Google Scholar 

  • Parcy F, Valon C, Kohara A, Miséra S , Giraudat J (1997) The ABSCISIC ACIDINSENSITIVE3, FUSCA3 and LEAFY COTYLEDON1 genes act in concert to control multiple aspects of Arabidopsis seed development. Plant Cell 9:1265–1277

    Article  PubMed  CAS  Google Scholar 

  • Ramanjulu S, Bartels D (2002) Drought and dessication-induced modulation of gene expression in plants. Plant Cell Environ 25:141–151

    Article  PubMed  CAS  Google Scholar 

  • Reid JL, Walker-Simmons MK (1993) Group 3 late embryogenesis abundant proteins in desiccation tolerant seedlings of wheat (Triticum aestivum L). Plant Physiol 102:125–131

    Google Scholar 

  • Sarda X, Tousch D, Ferrare K, Legrand E, Dupuis JM, Casse- Delbart F, Lamaze T (1997) Two TIP-like genes encoding aquaporins are expressed in sunflower guard cells. Plant J 12:1103–1111

    Article  PubMed  CAS  Google Scholar 

  • Sarda X, Tousch D, Ferrare K, Cellier F, Alcon C, Dupuis JM, Casse F, Lamaze T (1999) Characterization of closely related δ-TIP gene encoding aquaporins which are differentially expressed in sunflower roots upon water deprivation through exposure to air. Plant Mol Biol 40:179–191

    Article  PubMed  CAS  Google Scholar 

  • Schneiter AA, Miller JF (1981) Description of sunflower growth stages. Crop Sci 21:901–903

    Article  Google Scholar 

  • Scholander PF, Hammel HT, Bradstreet ED, Hemmingsen EA (1965) Sap pressure in vascular plants. Science 148:339–364

    Article  PubMed  CAS  Google Scholar 

  • Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi- Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1,300 Arabidopsis genes under drought and cold stresses using full-length cDNA microarray. Plant Cell 13:61–72

    Article  PubMed  CAS  Google Scholar 

  • Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamya A, Nakajama M, Enju A, Sakurai T, Satou K, Akyama K, Taji T, Yamahuchi-Shinozaki K, Carninci P, kawai J, hayashizaki Y , Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signal transduction in water-stress response. Plant Physiol 115:327–334

    Article  PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (1999) Molecular responses to drought stress In: Shinozaki K, Yamaguchi-Shinozaki K Molecular (eds) Responses to cold, drought, heat and salt stress in higher plants austin. RG Landes, TX, pp 11–28

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol 3:217–223

    PubMed  CAS  Google Scholar 

  • Smart LB, Moskal WA, Cameron KD, Bennett AB (2001) MIP Genes are down-regulated under drought stress in Nicotiana glauca. Plant Cell Physiol 42:686–693

    Article  PubMed  CAS  Google Scholar 

  • Srikanthbabu V, Ganesh K, Krishnaprasad BT, Gopalakrishna R, Savitha M, Udaya Kumar M (2002) Identifcation of pea genotypes with enhanced thermotolerance using temperature induction response (TIR) technique. J Plant Physiol 159:535–545

    Article  CAS  Google Scholar 

  • Stitt M (1990) Fructose-2,6-bisphosphate as a regulatory protein in plants. Annu Rev Plant Physiol Plant Mol Biol 41:153–185

    Article  CAS  Google Scholar 

  • Supronova T, Krugman T, Fahima T, Chien G, Shams I, Korel A , Nevo E (2004) Differential expression of dehydrin genes in wild barley, Hordeum spontaneum, associated with resistance to water deficit. Plant Cell Environ 27:1297–1308

    Article  Google Scholar 

  • Tezara W, Mitchall V, Driscoll S P, Lawlor DW (2002) Effects of water deficit and its interaction with CO2 supply on the biochemistry and physiology of photosynthesis in sunflower. J Exp Bot 375:1781–1791

    Article  CAS  Google Scholar 

  • Turner NC, Jones MM (1980) Turgor maintenance by osmotic adjustment; a review and evaluation. In: Turner N, Kramer PJ (eds) Adaptation of plants to water and high temperature stress. Wiley, New York, pp 87–107

    Google Scholar 

  • Van Berloo R (1999) GGT software for the display of graphical genotypes. J Heredity 90:328–329

    Article  Google Scholar 

  • Vander Willigen C, Pammenter NW, Mundree SG , Farrant JM (2004) Mechanical stabilization of desiccated vegetative tissues of the resurrection grass Eragrostis nindensis: does a TIP3;1 and/or compartmentalization of subcellular components and metabolites play a role? J Exp Bot 55:651–661

    Article  PubMed  CAS  Google Scholar 

  • Verwoerd TC, Bekker BM ,Hoekema A(1989) A small scale procedure for the rapid isolation of plant RNAs. Nucleic Acid Res 17(16):2362

    PubMed  CAS  Google Scholar 

  • Watkinson JI, Sioson AA, Vasquez-Robinet C, Shukla M, Kuma D, Ellis M, Heath LS, Ramakrishnan N, Chevone B, Watson L T, Van Zyl L, Egertsdotter U, Sederoff R R, Grene R (2003) Photosynthetic acclimation is reflected in specific patterns of gene expression in drought-stressed loblolly pine. Plant Physiol 133:1702–1716

    Article  PubMed  CAS  Google Scholar 

  • Yamada S, Komori T, Myers PN, Kuwata S, Kubo T, Imaseki H (1997) Expression of plasma membrane water channel genes under water stress in Nicotiana excelsior. Plant Cell Physiol 38:1226–1231

    PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Koizumi M, Urao S, Shinozaki K (1992) Molecular cloning of 9 cDNA that are responsive to dessication in Arabidopsis thaliana sequence analysis of one cDNA that encodes a putative transmembrane channel protein. Plant Cell Physiol 33:217–224

    CAS  Google Scholar 

  • Zrenner R, Krause KP, Apel P, Sonnewald U (1996) Reduction of the cytosolic fructose-1,6-bisphosphatase in transgenic potato plants limits photosynthesis sucrose biosynthesis with no impact on plant growth and tuber yield. Plant J 9:671–681

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank Professor Catherine Carter (South Dakota States University) for English corrections.

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Correspondence to A. Sarrafi.

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Communicated by D. A. Lightfoot.

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Poormohammad Kiani, S., Grieu, P., Maury, P. et al. Genetic variability for physiological traits under drought conditions and differential expression of water stress-associated genes in sunflower (Helianthus annuus L.). Theor Appl Genet 114, 193–207 (2007). https://doi.org/10.1007/s00122-006-0419-7

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