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Transcript abundance profiles reveal larger and more complex responses of grapevine to chilling compared to osmotic and salinity stress

Functional & Integrative Genomics volume 7, pages 317–333 (2007)Cite this article

Abstract

Cabernet Sauvignon grapevines were exposed to sudden chilling (5°C), water deficit (PEG), and an iso-osmotic salinity (120 mM NaCl and 12 mM CaCl2) for 1, 4, 8, and 24 h. Stomatal conductance and stem water potentials were significantly reduced after stress application. Microarray analysis of transcript abundance in shoot tips detected no significant differences in transcript abundance between salinity and PEG before 24 h. Chilling stress relates to changes in membrane structure, and transcript abundance patterns were predicted to reflect this. Forty-three percent of transcripts affected by stress vs control for 1 through 8 h were affected only by chilling. The functional categories most affected by stress included metabolism, protein metabolism, and signal transduction. Osmotic stress affected more protein synthesis and cell cycle transcripts, whereas chilling affected more calcium signaling transcripts, indicating that chilling has more complex calcium signaling. Stress affected many hormone (ABA, ethylene, and jasmonate) and transcription factor transcripts. The concentrations and transporter transcripts of several anions increased with time, including nitrate, sulfate, and phosphate. The transcript abundance changes in this short-term study were largely the same as a gradually applied long-term salinity and water-deficit study (Cramer et al. Funct Integr Genomics 7:111–134, 2007), but the reverse was not true, indicating a larger and more complex response in the acclimation process of a gradual long-term stress.

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References

  • Allen D, Ort D (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6:36–41

    PubMed  Article  CAS  Google Scholar 

  • Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621

    PubMed  Article  CAS  Google Scholar 

  • Barker DH, Logan BA, Adams WW III, Demmig-Adams B (1998) Photochemistry and xanthophyll cycle-dependent energy dissipation in differently oriented cladodes of Opuntia stricta during the winter. Aust J Plant Physiol 25:95–104

    CAS  Google Scholar 

  • Barker DH, Adams WW III, Demmig-Adams B, Logan BA, Verhoeven AS, Smith SD (2002) Nocturnally retained zeaxanthin does not remain engaged in a state primed for energy dissipation during the summer in two Yucca species growing in the Mojave Desert. Plant Cell Env 25:95–103

    Article  CAS  Google Scholar 

  • Battany M (2004) Grape notes: salinity management for drought years, University of California Cooperative Extension. 2006

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300

    Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    Article  PubMed  CAS  Google Scholar 

  • Broeckling CD, Huhman DV, Farag MA, Smith JT, May GD, Mendes P, Dixon RA, Sumner LW (2005) Metabolic profiling of Medicago truncatula cell cultures reveals the effects of biotic and abiotic elicitors on metabolism. J Exp Bot 56:323–336

    PubMed  Article  CAS  Google Scholar 

  • Chaves MM, Oliveira MM (2004) Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. J Exp Bot 55:2365–2384

    PubMed  Article  CAS  Google Scholar 

  • Cheong YH, Chang HS, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129:661–677

    PubMed  Article  CAS  Google Scholar 

  • Cramer GR, Lauchli A, Epstein E (1986) Effects of NaCl and CaCl2 on ion activities in complex nutrient solutions and root growth of cotton. Plant Physiol 81:792–797

    PubMed  CAS  Google Scholar 

  • Cramer GR, Ergul A, Grimplet J, Tillett RL, Tattersall EA, Bohlman MC, Vincent D, Sonderegger J, Evans J, Osborne C, Quilici D, Schlauch KA, Schooley DA, Cushman JC (2007) Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct Integr Genomics 7:111–134

    PubMed  Article  CAS  Google Scholar 

  • Fischer K, Kammerer B, Gutensohn M, Arbinger B, Weber A, Hausler RE, Flugge UI (1997) A new class of plastidic phosphate translocators: a putative link between primary and secondary metabolism by the phosphoenolpyruvate/phosphate antiporter. Plant Cell 9:453–462

    PubMed  Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Flowers YJ, Yeo AR (1995) Breeding for salinity resistance in crop plants: where next? Aust J Plant Physiol 22:875–884

    Article  Google Scholar 

  • Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the cbf cold response pathway. Plant Cell 14:1675–1690

    PubMed  Article  CAS  Google Scholar 

  • Fuller MP, Telli G (1999) An investigation of the frost hardiness of grapevine (Vitis vinifera) during bud break. Ann Appl Biol 135:589–595

    Article  Google Scholar 

  • Grattan S, Grieve CM (1994) Mineral nutrient acquisition and response by plants grown in saline environments. Handbook of Plant and Crop Stress. Pessarakli M. Marcel Dekker, New York, pp 203–226

    Google Scholar 

  • Grimes DW, Williams LE (1990) Irrigation effects on plant water relations and productivity of Thompson seedless grapevines. Crop Sci 30:255–260

    Article  Google Scholar 

  • Guy C (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41:187–223

    CAS  Google Scholar 

  • Hechenberger M, Schwappach B, Fischer WN, Frommer WB, Jentsch TJ, Steinmeyer K (1996) A family of putative chloride channels from Arabidopsis and functional complementation of a yeast strain with a CLC gene disruption. J Biol Chem 271:33632–33638

    PubMed  Article  CAS  Google Scholar 

  • Hendrickson L, Ball MC, Osmond CB, Furbank RT, Chow WS (2003) Assessment of photoprotection mechanisms of grapevines at low temperature. Functional Plant Biol 30:631–642

    Article  CAS  Google Scholar 

  • Hu Y, Schmidhalter U (2005) Drought and salinity: a comparison of their effects on mineral nutrition of plants. J Plant Nutr Soil Sci 168:541–549

    Article  CAS  Google Scholar 

  • Huner NPA, Oquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230

    Article  Google Scholar 

  • Kerr MK, Martin M, Churchill GA (2000) Analysis of variance for gene expression microarray data. J Comput Biol 7:819–837

    PubMed  Article  CAS  Google Scholar 

  • Knight MR (2002) Signal transduction leading to low-temperature tolerance in Arabidopsis thaliana. Philos Trans R Soc Lond B Biol Sci 357:871–875

    PubMed  Article  CAS  Google Scholar 

  • Kotuby-Amacher J, Koenig R, Kitchen B (1997) Salinity and plant tolerance, Utah State University. 2006

  • Kratsch HA, Wise RR (2000) The ultrastructure of chilling stress. Plant Cell Env 23:337–350

    Article  CAS  Google Scholar 

  • Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002). Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141

    PubMed  Article  CAS  Google Scholar 

  • Lee D, Polisensky DH, Braam J (2005) Genome-wide identification of touch- and darkness-regulated Arabidopsis genes: a focus on calmodulin-like and XTH genes. New Phytol 165:429–444

    PubMed  Article  CAS  Google Scholar 

  • Luu-The V, Paquet N, Calvo E, Cumps J (2005) Improved real-time RT-PCR method for high-throughput measurements using second derivative calculation and double correction. Biotechniques 38:287–293

    PubMed  CAS  Google Scholar 

  • Madore MA (1995) Phloem transport of solutes in crop plants. Handbook of Plant and Crop Physiology. Pessarakli M. Marcel Dekker, New York, pp 337–355

    Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    PubMed  Article  CAS  Google Scholar 

  • McGrath KC, Dombrecht B, Manners JM, Schenk PM, Edgar CI, Maclean DJ, Scheible WR, Udvardi MK, Kazan K (2005) Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression. Plant Physiol 139:949–959

    PubMed  Article  CAS  Google Scholar 

  • McKersie BD, Leshem YY (1994). Stress and stress coping in cultivated plants. Dordrecht, The Netherlands, Kluwer

    Google Scholar 

  • Medrano H, Escalona JM, Bota J, Gulias J, Flexas J (2002) Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter. Ann Bot (Lond) 89:895–905

    Article  CAS  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    PubMed  Article  CAS  Google Scholar 

  • Nakamura A, Fukuda A, Sakai S, Tanaka Y (2006) Molecular cloning, functional expression and subcellular localization of two putative vacuolar voltage-gated chloride channels in rice (Oryza sativa L.). Plant Cell Physiol 47:32–42

    PubMed  Article  CAS  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    PubMed  Article  CAS  Google Scholar 

  • Nishida I, Murata N (1996). Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 47:541–568

    PubMed  Article  CAS  Google Scholar 

  • Novillo F, Alonso JM, Ecker JR, Salinas J (2004) CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 101:3985–3990

    PubMed  Article  CAS  Google Scholar 

  • Oono Y, Seki M, Satou M, Iida K, Akiyama K, Sakurai T, Fujita M, Yamaguchi-Shinozaki K, Shinozaki K (2006) Monitoring expression profiles of Arabidopsis genes during cold acclimation and deacclimation using DNA microarrays. Funct Integr Genomics 6:212–234

    PubMed  Article  CAS  Google Scholar 

  • Palta JP, Whitaker BD, Weiss LS (1993) Plasma membrane lipids associated with genetic variability in freezing tolerance and cold acclimation of Solanum species. Plant Physiol 103:793–803

    PubMed  CAS  Google Scholar 

  • Reid RJ, Smith FA (2000) The limits of sodium/calcium interactions in plant growth. Aust J Plant Phys 27:709–715

    CAS  Google Scholar 

  • Rensink WA, Iobst S, Hart A, Stegalkina S, Liu J, Buell CR (2005) Gene expression profiling of potato responses to cold, heat, and salt stress. Funct Integr Genomics 5:201–207

    PubMed  Article  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 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13:61–72

    PubMed  Article  CAS  Google Scholar 

  • Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-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

    PubMed  Article  CAS  Google Scholar 

  • Shani U, Ben-Gal A (2005) Long-term response of grapevines to salinity: osmotic effects and ion toxicity. Am J Enol Vitic 56:148–154

    Google Scholar 

  • Shen L, Gong J, Caldo RA, Nettleton D, Cook D, Wise RP, Dickerson JA (2005) BarleyBase—an expression profiling database for plant genomics. Nucleic Acids Res 33:D614–618

    PubMed  Article  CAS  Google Scholar 

  • Smillie RM, Hetherington SE (1990). Screening for stress tolerance by chlorophyll fluorescence. Measurement Techniques in Plant Science. Hashimoto Y. Academic, San Diego, pp 229–261

    Google Scholar 

  • Smyth GK (2005) Limma: linear models for microarray data. Bioinformatics and Computational Biology Solutions using R and Bioconductor. Gentleman R, Carey V, Dudoit S, Irizarry R and Huber W. Springer, New York, pp 397–420

    Book  Google Scholar 

  • Takahashi S, Seki M, Ishida J, Satou M, Sakurai T, Narusaka M, Kamiya A, Nakajima M, Enju A, Akiyama K, Yamaguchi-Shinozaki K, Shinozaki K (2004) Monitoring the expression profiles of genes induced by hyperosmotic, high salinity, and oxidative stress and abscisic acid treatment in Arabidopsis cell culture using a full-length cDNA microarray. Plant Mol Biol 56:29–55

    PubMed  Article  CAS  Google Scholar 

  • Tattersall EAR, Ergul A, Al-Kayal F, DeLuc L, Cushman JC, Cramer GR (2005) Comparison of methods for isolating RNA from leaves of grapevine. Am J Enol Vitic 56:400–407

    CAS  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    PubMed  Article  CAS  Google Scholar 

  • Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu JK (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45:523–539

    PubMed  Article  CAS  Google Scholar 

  • Villora G, Moreno DA, Pulgar G, Romero L (2000) Salinity affects phosphorus uptake and partitioning in zucchini. Commun Soil Sci Plant Anal 31:501–507

    CAS  Google Scholar 

  • Viswanathan C, Zhu JK (2002) Molecular genetic analysis of cold-regulated gene transcription. Philos Trans R Soc Lond B Biol Sci 357:877–886

    PubMed  Article  CAS  Google Scholar 

  • Walker MA, McKersie BD, Pauls KP (1991) Effects of chilling on the biochemical and functional properties of thylakoid membranes. Plant Physiol 97:663–669

    PubMed  CAS  Article  Google Scholar 

  • Watson JW (2005) Drought advisory: Grapes, Washington State University Extension: 2

  • Wilkinson S, Clephan AL, Davies WJ (2001) Rapid low temperature-induced stomatal closure occurs in cold-tolerant Commelina communis leaves but not in cold-sensitive tobacco leaves, via a mechanism that involves apoplastic calcium but not abscisic acid. Plant Physiol 126:1566–1578

    PubMed  Article  CAS  Google Scholar 

  • Wolswinkel P (1999) Long-distance nutrient transport in plants and movement into developing grains. Mineral nutrition of crops: fundamental mechanisms and implications. Rengel Z. Food Products, New York, pp 91–113

    Google Scholar 

  • Wong CE, Li Y, Labbe A, Guevara D, Nuin P, Whitty B, Diaz C, Golding GB, Gray GR, Weretilnyk EA, Griffith M, Moffatt BA (2006) Transcriptional profiling implicates novel interactions between abiotic stress and hormonal responses in Thellungiella, a close relative of Arabidopsis. Plant Physiol 140:1437–1450

    PubMed  Article  CAS  Google Scholar 

  • Xiong L, Zhu JK (2001) Abiotic stress signal transduction in plants: molecular and genetic perspectives. Physiol Plant 112:152–166

    PubMed  Article  CAS  Google Scholar 

  • Yang Z, Tian L, Latoszek-Green M, Brown D, Wu K (2005) Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Mol Biol 58:585–596

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the National Science Foundation (NSF) Plant Genome program (#0217653), and a graduate student fellowship to E.A.R. Tattersall from the NSF EPSCoR Integrated Approaches to Abiotic Stress program (#0132556). The Nevada Genomics Center is supported by grants from the NIH Biomedical Research Infrastructure Network (NIH-NCRR, P20 RR16464) and NIH IDeA Network of Biomedical Research Excellence (INBRE, RR-03-008).

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Affiliations

  1. Department of Biochemistry & Molecular Biology, University of Nevada, Reno, NV, 89557-0014, USA

    Elizabeth A. R. Tattersall, Jérôme Grimplet, Laurent DeLuc, Matthew D. Wheatley, Delphine Vincent, Evan Lomen, John C. Cushman & Grant R. Cramer

  2. Biotechnology Institute, Ankara University, 06500, Besevler-Ankara, Turkey

    Ali Ergül

  3. Department of Animal Biotechnology, University of Nevada, Reno, NV, 89557-0014, USA

    Craig Osborne

  4. USDA-Agricultural Research Service, Reno, NV, 89512, USA

    Robert R. Blank

  5. Boston University School of Medicine, Department of Genetics and Genomics, Boston University, E632, Boston, MA, 02118, USA

    Karen A. Schlauch

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  1. Elizabeth A. R. Tattersall
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Correspondence to Grant R. Cramer.

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Supplemental Figure 1S
figure 7

Percent of transcripts representing significantly different abundance (p < 0.01) in stress versus control (1, 4 and 8 hours) that were assigned to MIPS functional categories. Results are given as a percentage of the total number of transcripts in the set to reflect relative differences among treatments (GIF 15 kb)

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Supplemental Figure 2S
figure 8

Concentrations of anions found in shoot tips (peak area/hippuric acid standard). Mean and s.d of three biological replicates. Square (■), chilling. Triangle (▲), PEG. Inverted triangle (▼), salinity. Diamond (◆), control (GIF 22 kb)

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Supplemental Figure 3S
figure 9

Percentage of transcripts with significant differences in abundance (p < 0.01) for salinity and PEG/water-deficit versus control at 24 hours and day 16 that were assigned to MIPS functional categories. Transcripts common to both 24 hours and day 16 for either stress were omitted from this analysis (GIF 20 kb)

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Tattersall, E.A.R., Grimplet, J., DeLuc, L. et al. Transcript abundance profiles reveal larger and more complex responses of grapevine to chilling compared to osmotic and salinity stress. Funct Integr Genomics 7, 317–333 (2007). https://doi.org/10.1007/s10142-007-0051-x

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  • DOI: https://doi.org/10.1007/s10142-007-0051-x

Keywords

  • Vitis vinifera
  • Abiotic stress
  • Microarray