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Changes in the Endogenous Content and Gene Expression of Salicylic Acid Correlate with Grapevine Bud Dormancy Release

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Abstract

The accumulation of cold temperature is an important factor for the release of bud dormancy in grapevine. The stress generated by cold is related to changes in defense hormones such as salicylic acid (SA). To understand the participation of this hormone during grapevine bud dormancy release, in this study, we evaluated the effects of cold accumulation on the endogenous SA content and expression patterns of the synthesis and signaling genes of SA as well as budbreak rates. Buds were subjected to an accumulation of 900 or 600 chilling units (CUs). The budbreak percentage was determined when cold-treated buds were transferred to warm temperatures (25 °C). The percentage of budbreak was closely correlated with the amount of cumulative CUs; the percentage increased gradually with the amount of chilling applied before forcing. The increase in the expression level of the SA biosynthesis gene (ICS2) and the endogenous SA content were quantified in cold-treated buds, and the expression was correlated with the percentage of budbreak. These findings may indicate that in dormant grapevine buds, cold accumulation stimulates the synthesis of SA. In cold-treated buds, the cellular levels of SA led to the expression of the NPR1 and PR1 genes, which was mediated by the transcription factor WRKY70. In contrast, expression of NPR1 and PR1 in control buds, which maintained a basal level of SA, and expression of ICS2 and WRKY70 were not detected, suggesting that the constitutive expression of NPR1-SA is independent. Taken together, the results of this study suggest a possible involvement of the SA signaling pathway in grapevine bud dormancy release.

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References

  • Anzanello R, Fialho FB, Santos HPD (2018) Chilling requirements and dormancy evolution in grapevine buds. Ciência e Agrotecnol 42:364–371

    CAS  Google Scholar 

  • Backer R, Naidoo S, van den Berg N (2019) The nonexpressor of pathogenesis-related genes 1 (NPR1) and related family: mechanistic insights in plant disease resistance. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00102

    Article  PubMed  PubMed Central  Google Scholar 

  • Carvalho LC, Vidigal P, Amâncio S (2015) Oxidative stress homeostasis in grapevine (Vitis vinifera L.). Front Environ Sci 3:20

    Google Scholar 

  • Chen M, Tan Q, Sun M, Li D, Fu X, Chen X, Gao D (2016) Genome-wide identification of WRKY family genes in peach and analysis of WRKY expression during bud dormancy. Mol Genet Genomics 29:1319–1332

    Google Scholar 

  • Coombe BG (1995) Growth stages of the grapevine: adoption of a system for identifying grapevine growth stages. Aust J Grape Wine Res 1:104–110

    Google Scholar 

  • Craig S, Ling Y (2014) Regulation of specialized metabolism by WRKY transcription factors. Plant Physiol 167:295–306

    Google Scholar 

  • Criddle RS, Fontana AJ, Rank DR, Paige D, Hansen LD, Breidenbech RW (1991) Simultaneous measurement of metabolic heat rate, CO2 production and O2 consumption by microcalorimetry. Anal Biochem 194:413–417

    CAS  PubMed  Google Scholar 

  • Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (1998) Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116:1351–1357

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dempsey DAC, Vlot MCW, Daniel FK (2011) Salicylic acid biosynthesis and metabolism. Arab Book/Am Soc Plant Biol 9:e0156

    Google Scholar 

  • Díaz-Riquelme J, Grimplet J, Martínez-Zapater JM, Carmona MJ (2012) Transcriptome variation along bud development in grapevine (Vitis vinifera L.). BMC Plant Biol 12:181

    PubMed  PubMed Central  Google Scholar 

  • Dokoozlian NK (1999) Chilling temperature and duration interact on the budbreak of Perlette' grapevine cuttings. HortScience 34:1–3

    Google Scholar 

  • Dokoozlian N, Williams L, Neja R (1995) Chilling exposure and hydrogen cyanamide interact in breaking dormancy of grape buds. HortScience 30:1244–1247

    CAS  Google Scholar 

  • Dong CJ, Li L, Shang QM, Liu XY, Zhang ZG (2014) Endogenous salicylic acid accumulation is required for chilling tolerance in cucumber (Cucumis sativus L.) seedlings. Planta 240:687–700

    CAS  PubMed  Google Scholar 

  • Durgbanshi A, Arbona V, Pozo O, Miersch O, Sancho JV, Gómez-Cadenas A (2005) Simultaneous determination of multiple phytohormones in plant extracts by liquid chromatography−electrospray tandem mass spectrometry. J Agric Food Chem 53:8437–8442

    CAS  PubMed  Google Scholar 

  • El-Shereif AR, Mizutani F, Onguso JM, Hossain AS (2005) Effects of different temperatures and sampling dates on bud break and ACC content of muscat bailey A grapevine buds. Int J Bot 1:168–171

    Google Scholar 

  • Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ryals J (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261:754–756

    CAS  PubMed  Google Scholar 

  • García-Baldenegro CV, Vargas-Arispuro I, Islas-Osuna M, Rivera-Domínguez M, Aispuro-Hernández E, Martínez-Téllez MÁ (2015) Total RNA quality of lyophilized and cryopreserved dormant grapevine buds. Electron J Biotechnol 18:134–137

    Google Scholar 

  • Gardea AA, Carvajal-Millan E, Orozco JA, Guerrero VM, Llamas J (2000) Effect of chilling on calorimetric responses of dormant vegetative apple buds. Thermochim Acta 349:89–94

    CAS  Google Scholar 

  • Le Henanff G, Heitz T, Mestre P, Mutterer J, Walter B, Chong J (2009) Characterization of Vitis vinifera NPR1 homologs involved in the regulation of pathogenesis-related gene expression. BMC Plant Biol 9:54

    PubMed  PubMed Central  Google Scholar 

  • Le Henanff G, Farine S, Kieffer-Mazet F, Miclot AS, Heitz T, Mestre P, Chong J (2011) Vitis viniferaVvNPR1. 1 is the functional ortholog of AtNPR1 and its overexpression in grapevine triggers constitutive activation of PR genes and enhanced resistance to powdery mildew. Planta 234:405–417

    CAS  PubMed  Google Scholar 

  • Hintze J (2007) Number cruncher statistical system, NCSS 2007. https://www.ncss.com. Accesed 16 July 2018

  • Janda M, Ruelland E (2015) Magical mystery tour: salicylic acid signalling. Environ Exp Bot 114:117–128

    CAS  Google Scholar 

  • Khodary SE (2004) Effect of salicylic acid on the growth, photosynthesis and carbohydrate metabolism in salt stressed maize plants. Int J Agric Biol 6:1–8

    CAS  Google Scholar 

  • Kim Y, Park S, Gilmour SJ, Thomashow MF (2013) Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis. Plant J 75:364–376

    CAS  PubMed  Google Scholar 

  • Kosová K, Prášil IT, Vítámvás P, Dobrev P, Motyka V, Floková K, Trávničková A (2012) Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. J Plant Physiol 169:567–576

    PubMed  Google Scholar 

  • Lang GA (1987) Dormancy: a new universal terminology. HortScience 22:817–820

    Google Scholar 

  • Larkindale J, Hall JD, Knight MR, Vierling E (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 138:882–897

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16:319–331

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Brader G, Kariola T, Tapio Palva E (2006) WRKY70 modulates the selection of signaling pathways in plant defense. Plant J 46:477–491

    CAS  PubMed  Google Scholar 

  • Li G, Peng X, Wei L, Kang G (2013) Salicylic acid increases the contents of glutathione and ascorbate and temporally regulates the related gene expression in salt-stressed wheat seedlings. Gene 529:321–325

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Márquez-Cervantes JA, Cano-Medrano R, Rodríguez-Alcázar J (2000) Thidiazuron, citrolina y unidades frío en el rompimiento de letargo de yemas de vid (Vitis vinifera L.). Rev Chapingo Serie Hortic 6:105–110

    Google Scholar 

  • Martínez C, Pons E, Prats G, León J (2004) Salicylic acid regulates flowering time and links defence responses and reproductive development. Plant J 37:209–217

    PubMed  Google Scholar 

  • Melke A (2015) The physiology of chilling temperature requirements for dormancy release and bud-break in temperate fruit trees grown at mild winter tropical climate. J Plant Stud 4:110

    Google Scholar 

  • Miura K, Tada Y (2014) Regulation of water, salinity, and cold stress responses by salicylic acid. Front Plant Sci 5:4

    PubMed  PubMed Central  Google Scholar 

  • Mohamed HB, Vadel AM, Geuns JM, Khemira H (2012) Carbohydrate changes during dormancy release in superior seedless grapevine cuttings following hydrogen cyanamide treatment. Sci Hortic 140:19–25

    Google Scholar 

  • Mornya PMP, Cheng F (2013) Seasonal changes in endogenous hormone and sugar contents during bud dormancy in tree peony. J Appl Hortic 15:159–165

    Google Scholar 

  • Mou Z, Fan W, Dong X (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113:935–944

    CAS  PubMed  Google Scholar 

  • Nazar R, Umar S, Khan NA (2015) Exogenous salicylic acid improves photosynthesis and growth through increase in ascorbate-glutathione metabolism and S assimilation in mustard under salt stress. Plant Signal Behav 10:e1003751

    PubMed  PubMed Central  Google Scholar 

  • Niculcea M, Martinez-Lapuente L, Guadalupe Z, Sánchez-Díaz M, Morales F, Ayestarán B, Antolín MC (2013) Effects of water-deficit irrigation on hormonal content and nitrogen compounds in developing berries of Vitis vinifera L. cv. Tempranillo. J Plant Growth Regul 32:551–563

    CAS  Google Scholar 

  • Or E, Vilozny I, Eyal Y, Ogradovitch A (2000) The transduction of the signal for grape bud dormancy breaking induced by hydrogen cyanamide may involve the SNF-like protein kinase GDBRPK. Plant Mol Biol 43:483–494

    CAS  PubMed  Google Scholar 

  • Pacey-Miller T, Scott K, Ablett E, Tingey S, Ching A, Henry R (2003) Genes associated with the end of dormancy in grapes. Funct Integr Genomics 4:144–152

    Google Scholar 

  • Pan Q, Zhan J, Liu H, Zhang J, Chen J, Wen P, Huang W (2006) Salicylic acid synthesized by benzoic acid 2-hydroxylase participates in the development of thermotolerance in pea plants. Plant Sci 171:226–233

    CAS  Google Scholar 

  • Pape S, Thurow C, Gatz C (2010) The Arabidopsis PR-1 promoter contains multiple integration sites for the coactivator NPR1 and the repressor SNI1. Plant Physiol 154:1805–1818

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez F, Vergara R, Rubio S (2008) H2O2 is involved in the dormancy-breaking effect of hydrogen cyanamide in grapevine buds. Plant Growth Regul 55:149–155

    Google Scholar 

  • Powell LE (1987) Hormonal aspects of bud and seed dormancy in temperate-zone woody plants. HortScience 22:845–850

    CAS  Google Scholar 

  • Prasad T (1996) Mechanisms of chilling-induced oxidative stress injury and tolerance in developing maize seedlings: changes in antioxidant system, oxidation of proteins and lipids and protease activity. Plant J 10:1017–1026

    CAS  Google Scholar 

  • Reid KE, Olsson N, Schlosser J, Peng F, Lund ST (2006) An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biol 6:27

    PubMed  PubMed Central  Google Scholar 

  • Richardson EA, Seeley SD, Walker DR (1974) A model for estimating the completion of rest for 'Redhaven' and 'Elberta' peach trees. HortScience 9:331–332

    Google Scholar 

  • Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot 62:3321–3338

    CAS  PubMed  Google Scholar 

  • Saure MC (1985) Dormancy release in deciduous fruit trees. Hortic Rev 7:239–300

    Google Scholar 

  • Seo PJ, Kim MJ, Park JY, Kim SY, Jeon J, Lee YH, Kim J, Park CM (2010) Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis. Plant J 61:661–671

    CAS  PubMed  Google Scholar 

  • Seyfferth C, Tsuda K (2014) Salicylic acid signal transduction: the initiation of biosynthesis, perception and transcriptional reprogramming. Front Plant Sci 5:697

    PubMed  PubMed Central  Google Scholar 

  • Singh VP, Prasad SM, Munné-Bosch S, Müller M (2017) Phytohormones and the regulation of stress tolerance in plants: current status and future directions. Front Plant Sci 8:1871

    PubMed  PubMed Central  Google Scholar 

  • Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J, Wang C, Zuo J, Dong X (2008) Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science 32:952–956

    Google Scholar 

  • Theocharis A, Clément C, Barka EA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105

    CAS  PubMed  Google Scholar 

  • Trejo-Martínez MA, Orozco JA, Almaguer-Vargas G, Carvajal-Millán E, Gardea AA (2009) Metabolic activity of low chilling grapevine buds forced to break. Thermochim Acta 481:28–31

    Google Scholar 

  • Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71–W74

    PubMed  PubMed Central  Google Scholar 

  • Uquillas C, Letelier I, Blanco F, Jordana X, Holuigue L (2004) NPR1-independent activation of immediate early salicylic acid-responsive genes in Arabidopsis. Mol Plant Microbe Interact 17:34–42

    CAS  PubMed  Google Scholar 

  • Vanacker H, Lu H, Rate DN, Greenberg JT (2001) A role for salicylic acid and NPR1 in regulating cell growth in Arabidopsis. Plant J 28:209–216

    CAS  PubMed  Google Scholar 

  • Wan SB, Tian L, Tian RR, Pan QH, Zhan JC, Wen PF, Huang WD (2009) Involvement of phospholipase D in the low temperature acclimation-induced thermotolerance in grape berry. Plant Physiol Biochem 47:504–510

    CAS  PubMed  Google Scholar 

  • Wang LJ, Li SH (2006) Thermotolerance and related antioxidant enzyme activities induced by heat acclimation and salicylic acid in grape (Vitis vinifera L.) leaves. Plant Growth Regul 48:137–144

    CAS  Google Scholar 

  • Wang D, Amornsiripanitch N, Dong X (2006) A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog 2:1042–1050

    CAS  Google Scholar 

  • Yuri J (2002) El receso en frutales. Pomáceas Bol Tec 2:1

    Google Scholar 

  • Zhang Z, Zhuo X, Zhao K, Zheng T, Han Y, Yuan C, Zhang Q (2018) Transcriptome profiles reveal the crucial roles of hormone and sugar in the bud dormancy of Prunus mume. Sci Rep 8:5090

    PubMed  PubMed Central  Google Scholar 

  • Zheng C, Halaly T, Acheampong AK, Takebayashi Y, Jikumaru Y, Kamiya Y, Or E (2015) Abscisic acid (ABA) regulates grape bud dormancy, and dormancy release stimuli may act through modification of ABA metabolism. J Exp Bot 66:1527–1542

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This research was supported by the National Council of Science and Technology (research grant 176 SEP-CONACyT 157334).

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  1. Centro de Investigación en Alimentación y Desarrollo, A. C. Carretera Gustavo Enrique Astiazarán Rosas No 46, Col. La Victoria, 83304, Hermosillo, Sonora, Mexico

    María Armida Orrantia-Araujo, Miguel Ángel Martínez-Téllez, Marisela Rivera-Domínguez, Miguel Ángel Hernández-Oñate & Irasema Vargas-Arispuro

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  1. María Armida Orrantia-Araujo
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  2. Miguel Ángel Martínez-Téllez
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Orrantia-Araujo, M.A., Martínez-Téllez, M.Á., Rivera-Domínguez, M. et al. Changes in the Endogenous Content and Gene Expression of Salicylic Acid Correlate with Grapevine Bud Dormancy Release. J Plant Growth Regul 40, 254–262 (2021). https://doi.org/10.1007/s00344-020-10100-9

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