The scion-driven transcriptomic changes guide the resilience of grafted near-isohydric grapevines under water deficit Open Access

Abstract

The large diversity of grapevine cultivars includes genotypes more tolerant to water deficit than others. Widely distributed cultivars, like Merlot, are more sensitive to water deprivation than local cultivars like Callet, which are more adapted to water deficit due to their Mediterranean origin. Despite their tolerance, adaptation to water deficit influenced by grafting in rootstocks like 110 Richter is key to facing drought in vineyards, defining the scion-rootstock relationship. To understand these differences, we explored transcriptomic, metabolic, hormonal and physiological responses under three levels of water deficit (mild, high, and extreme), using 110 Richter as the rootstock in both cultivars. Results revealed that sensitivity to abscisic acid (ABA) is essential for water deficit tolerance in the aerial part, guiding root responses. Callet/110 Richter activates more gene expression patterns in response to ABA, reducing water loss compared to Merlot/110 Richter in both aerial and root parts. This modulation in Callet/110 Richter involves regulating metabolic pathways to increase cell turgor, reducing photosynthesis, and producing molecules like polyphenols or flavonoids to respond to oxidative stress. In contrast, Merlot/110 Richter shows a lack of specific response, especially in the roots, indicating less resilience to water stress. Therefore, selecting genotypes more sensitive to ABA and their interaction with rootstocks is key for managing vineyards in future climate change scenarios.

Acknowledgements

This study was supported by the Research and Science Ministry of Spain (project RTI2018-094470-R-C21 and PID2021-1255750R-C21). Special acknowledgment to Dr Rosa Arroyo-Garcia, one of the principal researchers of this paper, who tragically passed away after a long illness last year. We miss you so much, Rosa.

Author contributions

A.R.I., D.C., and R.A.G. conceived the study and developed the experimental design for the study. A.R.I., D.C., and C.L.H. performed the laboratory work. A.R.I., D.C., and L.V. performed the data analysis and visualization. A.R.I., D.C., L.V., M.A.R., J.B., and R.A.G. wrote the manuscript. All authors contributed to the article and approved the submitted version.

Data availability

The data underlying this article are available in the European Nucleotide Archive (ENA) (https://www.ebi.ac.uk/ena/browser/home) and can be accessed with PRJEB55563.

Conflict of interests

No conflict of interest is present in this article.

References

[1] International Organisation of Vine and Wine Intergovernmental Organisation O.State of the world vine and wine sector in 2022 2022

[2] International Organisation of Vine and Wine Intergovernmental Organisation. OIV Statistical Report on World Vitiviniculture. 2018.

[3] Duchêne E, Huard F, Dumas V. et al. The challenge of adapting grapevine varieties to climate change. Clim Res. 2010;41:193-204

[4] Bota J, Tomás M, Flexas J. et al. Differences among grapevine cultivars in their stomatal behavior and water use efficiency under progressive water stress. Agric Water Manag. 2016;164:91-9

[5] Bota J, Flexas J, Medrano H. Genetic variability of photosynthesis and water use in Balearic grapevine cultivars. Ann Applied Biol-ogy. 2001;138:353-61

[6] Florez-Sarasa I, Clemente-Moreno MJ, Cifre J. et al. Differ-ences in metabolic and physiological responses between local and widespread grapevine cultivars under water deficit stress. Agronomy. 2020;10:1052

[7] Schultz HR. Differences in hydraulic architecture account for near-isohydric and anisohydric behaviour of two field-grown Vitis vinifera L. cultivars during drought. Plant Cell Environ. 2003;26:1393-405

[8] Hochberg U, Rockwell FE, Holbrook NM. et al. Iso/Anisohydry: a plant-environment interaction rather than a simple hydraulic trait. Trends Plant Sci. 2018;23:112-20

[9] Levin AD, Williams LE, Matthews MA. A continuum of stomatal responses to water deficits among 17 wine grape cultivars (Vitis vinifera). Functional Plant Biol. 2020;47:11

[10] Herrera JC, Calderan A, Gambetta GA. et al. Stomatal responses in grapevine become increasingly more tolerant to low water potentials throughout the growing season. Plant J. 2022;109:804-15

[11] Williams LE, Baeza P. Relationships among ambient tempera-ture and vapor pressure deficit and leaf and stem water poten-tials of fully irrigated, field-grown grapevines. Am J Enol Vitic. 2007;58:173-81

[12] Pou A, Balda P, Cifre J. et al. Influence of non-irrigation and seasonality on wine colour, phenolic composition and sensory quality of a grapevine (Vitis vinifera cv. Callet) in a Mediterranean climate. OENO One. 2023;57:217-33

[13] Kar RK. Plant responses to water stress: role of reactive oxygen species. Plant Signal Behav. 2011;6:1741-5

[14] Tillett RL, Ergül A, Albion RL. et al. Identification of tissue-specific, abiotic stress-responsive gene expression patterns in wine grape (Vitis vinifera L.) based on curation and mining of large-scale EST data sets. BMC Plant Biol. 2011;11:86

[15] Corso M, Vannozzi A, Maza E. et al. Comprehensive transcript profiling of two grapevine rootstock genotypes contrasting in drought susceptibility links the phenylpropanoid pathway to enhanced tolerance. EXBOTJ. 2015;66:5739-52

[16] Dal Santo S, Palliotti A, Zenoni S. et al. Distinct transcrip-tome responses to water limitation in isohydric and anisohydric grapevine cultivars. BMC Genomics. 2016;17:815

[17] Murcia G, Fontana A, Pontin M. et al. ABA and GA 3 regulate the synthesis of primary and secondary metabolites related to alleviation from biotic and abiotic stresses in grapevine. Phyto-chemistry. 2017;135:34-52

[18] Cochetel N, Escudié F, Cookson SJ. et al. Root transcriptomic responses of grafted grapevines to heterogeneous nitrogen avail-ability depend on rootstock genotype. JExp Bot. 2017;68:4339-55

[19] Haider MS, Zhang C, Kurjogi MM. et al. Insights into grapevine defense response against drought as revealed by biochemical, physiological and RNA-Seq analysis. Sci Rep. 2017;7:13134

[20] Gautier AT, Cochetel N, Merlin I. et al. Scion genotypes exert long distance control over rootstock transcriptome responses to low phosphate in grafted grapevine. BMC Plant Biol. 2020;20:367

[21] Carrasco D, Zhou-Tsang A, Rodriguez-Izquierdo A. et al. Coastal wild grapevine accession (Vitis vinifera L. ssp. sylvestris) shows distinct late and early transcriptome changes under salt stress in comparison to commercial rootstock Richter 110. Plan Theory. 2022;11:2688

[22] Matus JT, Aquea F, Arce-Johnson P.Analysis of the grape MYB R2R3 subfamily reveals expanded wine quality-related clades and conserved gene structure organization across Vitis and Arabidopsis genomes. BMC Plant Biol. 2008;8:83

[23] Matus JT, Aquea F, Espinoza C. et al. Inspection of the grapevine BURP superfamily highlights an expansion of RD 22 genes with distinctive expression features in berry development and ABA-mediated stress responses. PLoS One. 2014;9:e110372

[24] Orduña L, Li M, Navarro-Payá D. et al. Direct regulation of shikimate, early phenylpropanoid, and stilbenoid pathways by subgroup 2 R2R3-MYBs in grapevine. Plant J. 2022;110:529-47

[25] Zhou-Tsang A, Wu Y, Henderson SW. et al. Grapevine salt toler-ance. Aust J Grape Wine Res. 2021;27:149-68

[26] Marguerit E, Brendel O, Lebon E. et al. Rootstock control of scion transpiration and its acclimation to water deficit are controlled by different genes. New Phytol. 2012;194:416-29

[27] Cookson S, Ollat N. Grafting with rootstocks induces extensive transcriptional re-programming in the shoot apical meristem of grapevine. BMC Plant Biol. 2013;13:147

[28] Cramer GR, Ergül A, Grimplet J. et al. Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct Integr Genomics. 2007;7:111-34

[29] Begum N, Ahanger MA, Su Y. et al. Improved drought tolerance by AMF inoculation in maize (Zea mays) involves physiological and biochemical implications. Plan Theory. 2019;8:579

[30] Król A, Amarowicz R, Weidner S.Changes in the composition of phenolic compounds and antioxidant properties of grapevine roots and leaves (Vitis vinifera L.) under continuous of long-term drought stress. Acta Physiol Plant. 2014;36:1491-9

[31] Huang T, Jander G. Abscisic acid-regulated protein degrada-tion causes osmotic stress-induced accumulation of branched-chain amino acids in Arabidopsis thaliana. Planta. 2017;246:737-47

[32] Li L, Dou N, Zhang H. et al.The versatile GABA in plants. Plant Signal Behav. 2021;16:e1862565

[33] Muhammad Aslam M, Waseem M, Jakada BH. et al. Mechanisms of abscisic acid-mediated drought stress responses in plants. IJMS. 2022;23:1084

[34] Degu A, Hochberg U, Wong DCJ. et al. Swift metabolite changes and leaf shedding are milestones in the acclimation process of grapevine under prolonged water stress. BMC Plant Biol. 2019;19:69

[35] Baiges I, Schäffner AR, Mas A. Eight cDNA encoding putative aquaporins in Vitis hybrid Richter-110 and their differential expression. JExp Bot. 2001;52:1949-51

[36] Tyerman SD, Niemietz CM, Bramley H. Plant aquaporins: mul-tifunctional water and solute channels with expanding roles: function and expression of plant aquaporins. Plant Cell Environ. 2002;25:173-94

[37] Galmés J, Pou A, Alsina MM. et al. Aquaporin expression in response to different water stress intensities and recovery in Richter-110 (Vitis sp.): relationship with ecophysiological status. Planta. 2007;226:671-81

[38] Chen Y, Liu WJ, Su YQ. et al. Different response of photosystem II to short and long-term drought stress in Arabidopsis thaliana. Physiol Plant. 2016;158:225-35

[39] Medici A, Laloi M, Atanassova R. Profiling of sugar transporter genes in grapevine coping with water deficit. FEBS Lett. 2014;588:3989-97

[40] Zhang Z, Zou L, Ren C. et al. VvSWEET 10 mediates sugar accu-mulationingrapes. Genes. 2019;10:255

[41] Castellarin SD, Pfeiffer A, Sivilotti P. et al. Transcriptional regula-tion of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. Plant Cell Environ. 2007;30:1381-99

[42] Bray EA. Classification of genes differentially expressed during water-deficit stress in Arabidopsis thaliana: an analysis using microarray and differential expression data. Ann Bot. 2002;89:803-11

[43] Yıldırım K, Yağcı A, Sucu S. et al. Responses of grapevine root-stocks to drought through altered root system architecture and root transcriptomic regulations. Plant Physiol Biochem. 2018;127:256-68

[44] Savoi S, Wong DCJ, Degu A. et al. Multi-omics and integrated network analyses reveal new insights into the systems relation-ships between metabolites, structural genes, and transcriptional regulators in developing grape berries (Vitis vinifera L.) exposed to water deficit. Front Plant Sci. 2017;8:1124

[45] Galbiati M, Matus JT, Francia P. et al. The grapevine guard cell-related VvMYB 60 transcription factor is involved in the reg-ulation of stomatal activity and is differentially expressed in response to ABA and osmotic stress. BMC Plant Biol. 2011;11:142

[46] Savoi S, Wong DCJ, Arapitsas P. et al. Transcriptome and metabo-lite profiling reveals that prolonged drought modulates the phenylpropanoid and terpenoid pathway in white grapes ( Vitis vinifera L.). BMC Plant Biol. 2016;16:67

[47] Liu C, Wu Y, Wang X. bZIP transcription factor OsbZIP52/RISBZ5: a potential negative regulator of cold and drought stress response in rice. Planta. 2012;235:1157-69

[48] Tu M, Wang X, Zhu Y. et al. VlbZIP 30 of grapevine functions in dehydration tolerance via the abscisic acid core signaling pathway. Hortic Res. 2018;5:49

[49] Khoso MA, Hussain A, Ritonga FN. et al. WRKY transcription fac-tors (TFs): molecular switches to regulate drought, temperature, and salinity stresses in plants. Front Plant Sci. 2022;13:1039329

[50] Zhang L, Marguerit E, Rossdeutsch L. et al. The influence of grapevine rootstocks on scion growth and drought resistance. Theor Exp Plant Physiol. 2016;28:143-57

[51] Rossdeutsch L, Edwards E, Cookson SJ. et al. ABA-mediated responses to water deficit separate grapevine genotypes by their genetic background. BMC Plant Biol. 2016;16:91

[52] Franck N, Zamorano D, Wallberg B. et al. Contrasting grapevines grafted into naturalized rootstock suggest scion-driven tran-scriptomic changes in response to water deficit. Sci Hortic. 2020;262:109031

[53] Coombe BG. Growth stages of the grapevine: adoption of a system for identifying grapevine growth stages. Aust J Grape Wine Res. 1995;1:104-10

[54] Van Leeuwen C, Trégoat O, Choné X. et al. Vine water status is a key factor in grape ripening and vintage quality for red Bordeaux wine. How can it be assessed for vineyard manage-ment purposes? OENO One. 2009;43:121

[55] López-Hidalgo C, Meijón M, Lamelas L. et al. The rainbow pro-tocol: a sequential method for quantifying pigments, sugars, free amino acids, phenolics, flavonoids and MDA from a small amount of sample. Plant Cell Environ. 2021;44:1977-86

[56] Choi YH, Tapias EC, Kim HK. et al. Metabolic discrimination of Catharanthus roseus leaves infected by Phytoplasma using 1 H-NMR spectroscopy and multivariate data analysis. Plant Physiol. 2004;135:2398-410

[57] Reid KE, Olsson N, Schlosser J. et al. An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biol. 2006;6:27

[58] Velt A, Frommer B, Blanc S. et al. An improved refer-ence of the grapevine genome reasserts the origin of the PN40024 highly homozygous genotype. G3 (Bethesda). 2023;13:jkad067

[59] Costa-Silva J, Domingues D, Lopes FM. RNA-Seq differential expression analysis: an extended review and a software tool. PLoS One. 2017;12:e0190152

[60] Navarro-Payá D, Santiago A, Orduña L. et al. The grape gene reference catalogue as a standard resource for gene selection and genetic improvement. Front Plant Sci. 2022;12:803977