Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Effects of water stress on endogenous hormones and free polyamines in different tissues of grapevines (Vitis vinifera L. cv. ‘Merlot’)

Zhennan Zhan A , Ning Wang B , Zumin Chen B , Yanxia Zhang A , Kangqi Geng A , Dongmei Li https://orcid.org/0009-0000-3320-960X B * and Zhenping Wang https://orcid.org/0000-0002-8876-3664 A B *
+ Author Affiliations
- Author Affiliations

A School of Life Science, Ningxia University, Yinchuan, Ningxia 750021, People’s Republic of China.

B School of Agriculture, Ningxia University, Yinchuan, Ningxia 750021, People’s Republic of China.


Handling Editor: Manuela Chaves

Functional Plant Biology 50(12) 993-1009 https://doi.org/10.1071/FP22225
Submitted: 19 September 2022  Accepted: 30 August 2023  Published: 4 October 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Water stress can affect plant ecological distribution, crop growth and carbohydrate distribution, impacting berry quality. However, previous studies mainly focused on short-term water stress or osmotic stress and few studies paid attention to the responses of grape to long-term water stresses. Grapevines were subjected to no water stress (CK), mild water stress (T1) and moderate water stress (T2). Hundred-berry weight and malic acid content were reduced under T1 and T2; however, glucose and fructose content showed the opposite trend. Endogenous hormones and polyamines (PAs) can regulate plant growth and development as well as physiological metabolic processes. T1 and T2 could increase abscisic acid content, however, indole-3-acetic acid, jasmonate, gibberellins 3 and 4, cytokinin and trans-zeatin contents were slightly decreased. Three species of PAs (putrescine, spermidine and spermine) were detected, presenting obvious tissue specificity. Furthermore, there was a statistically positive correlation relating spermidine content in the pulp with glucose and fructose contents of grape berries; and a negative correlation with organic acid. In summary, water stress had a profound influence on hormonally-driven changes in physiology and berry quality, indicating that endogenous hormones and the PAs play a critical role in the development and ripening of grape berries under water stress.

Keywords: abscisic acid, berry quality, grapevines, hormones, polyamines, tissues, water status, water stress.

References

Agudelo-Romero P, Ali K, Choi YH, Sousa L, Verpoorte R, Tiburcio AF, Fortes AM (2014) Perturbation of polyamine catabolism affects grape ripening of Vitis vinifera cv. Trincadeira. Plant Physiology and Biochemistry 74, 141-155.
| Crossref | Google Scholar |

Alatzas A, Theocharis S, Miliordos D-E, Leontaridou K, Kanellis AK, Kotseridis Y, Hatzopoulos P, Koundouras S (2021) The effect of water deficit on two greek Vitis vinifera L. cultivars: physiology, grape composition and gene expression during berry development. Plants (Basel) 10, 1947.
| Crossref | Google Scholar |

Alcazar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231, 1237-1249.
| Crossref | Google Scholar | PubMed |

Alvarez-Florez F, Lopez-Cristoffanini C, Jauregui O, Melgarejo LM, Lopez-Carbonell M (2017) Changes in ABA, IAA and JA levels during calyx, fruit and leaves development in cape gooseberry plants (Physalis peruviana L.). Plant Physiology Biochemistry 115, 174-182.
| Crossref | Google Scholar | PubMed |

Antoln MC, Santesteban H, Santa Mara E, Aguirreolea J, Snchez-Daz M (2008) Involvement of abscisic acid and polyamines in berry ripening of Vitis vinifera (L.) subjected to water deficit irrigation. Australian Journal of Grape and Wine Research 14, 123-133.
| Crossref | Google Scholar |

Baeza P, Conde JR, Lissarrague JR, Junquera P (2005) Agronomic and ecophysiological responses of field-grown ‘Cabernet Sauvignon’ grapevines to three irrigation treatments. Acta Horticulturae 689, 373-380.
| Crossref | Google Scholar |

Berahim Z, Dorairaj D, Omar MH, Saud HM, Ismail MR (2021) Spermine mediated improvements on stomatal features, growth, grain filling and yield of rice under differing water availability. Scientific Reports 11, 10669.
| Crossref | Google Scholar | PubMed |

Bernardo S, Dinis L-T, Machado N, Barros A, Pitarch-Bielsa M, Malheiro AC, Gómez-Cadenas A, Moutinho-Pereira J (2022) Uncovering the effects of kaolin on balancing berry phytohormones and quality attributes of Vitis vinifera grown in warm-temperate climate regions. Journal of the Science of Food and Agriculture 102, 782-793.
| Crossref | Google Scholar | PubMed |

Bottcher C, Keyzers RA, Boss PK, Davies C (2010) Sequestration of auxin by the indole-3-acetic acid-amido synthetase GH3-1 in grape berry (Vitis vinifera L.) and the proposed role of auxin conjugation during ripening. Journal of Experimental Botany 61, 3615-3625.
| Crossref | Google Scholar | PubMed |

Bottcher C, Boss PK, Davies C (2013) Increase in cytokinin levels during ripening in developing Vitis vinifera cv. Shiraz berries. American Journal of Enology and Viticulture 64, 527-531.
| Crossref | Google Scholar |

Bottcher C, Burbidge CA, Boss PK, Davies C (2015) Changes in transcription of cytokinin metabolism and signalling genes in grape (Vitis vinifera L.) berries are associated with the ripening-related increase in isopentenyladenine. BMC Plant Biology 15, 223.
| Crossref | Google Scholar | PubMed |

Bucchetti B, Matthews MA, Falginella L, Peterlunger E, Castellarin SD (2011) Effect of water deficit on Merlot grape tannins and anthocyanins across four seasons. Scientia Horticulturae 128, 297-305.
| Crossref | Google Scholar |

Buesa I, Pérez D, Castel J, Intrigliolo DS, Castel JR (2017) Effect of deficit irrigation on vine performance and grape composition of Vitis vinifera L. cv. Muscat of Alexandria. Australian Journal of Grape and Wine Research 23, 251-259.
| Crossref | Google Scholar |

Cardarelli M, Cecchetti V (2014) Auxin polar transport in stamen formation and development: how many actors? Frontiers in Plant Science 5, 333.
| Crossref | Google Scholar | PubMed |

Chaves MM, Santos TP, Souza CR, Ortuño MF, Rodrigues ML, Lopes CM, Maroco JP, Pereira JS (2007) Deficit irrigation in grapevine improves water-use efficiency while controlling vigour and production quality. Annals of Applied Biology 150, 237-252.
| Crossref | Google Scholar |

Coombe BG (1995) Growth stages of the grapevine: adoption of a system for identifying grapevine growth stages. Australian Journal of Grape and Wine Research 1, 104-110.
| Crossref | Google Scholar |

Demenkov PS, Oshchepkova ЕА, Ivanisenko TV, Ivanisenko VA (2021) Prioritization of biological processes based on the reconstruction and analysis of associative gene networks describing the response of plants to adverse environmental factors. Vavilov Journal of Genetics and Breeding 25, 580-592.
| Crossref | Google Scholar | PubMed |

Deluc LG, Quilici DR, Decendit A, Grimplet J, Wheatley MD, Schlauch KA, Mérillon J-M, Cushman JC, Cramer GR (2009) Water deficit alters differentially metabolic pathways affecting important flavor and quality traits in grape berries of Cabernet Sauvignon and Chardonnay. BMC Genomics 10, 212.
| Crossref | Google Scholar | PubMed |

Do PT, Degenkolbe T, Erban A, Heyer AG, Kopka J, Kohl KI, Hincha DK, Zuther E (2013) Dissecting rice polyamine metabolism under controlled long-term drought stress. PLoS ONE 8, e60325.
| Crossref | Google Scholar | PubMed |

Escalona JM, Fuentes S, Tomás M, Martorell S, Flexas J, Medrano H (2013) Responses of leaf night transpiration to drought stress in Vitis vinifera L. Agricultural Water Management 118, 50-58.
| Crossref | Google Scholar |

Fernandes JC, Cobb F, Tracana S, Costa GJ, Valente I, Goulao LF, Amâncio S (2015) Relating water deficiency to berry texture, skin cell wall composition, and expression of remodeling genes in two Vitis vinifera L. varieties. Journal of Agricultural and Food Chemistry 63, 3951-3961.
| Crossref | Google Scholar | PubMed |

Flexas J, Galmés J, Gallé A, Gulías J, Pou A, Ribas-Carbo M, Tomàs M, Medrano H (2010) Improving water use efficiency in grapevines: potential physiological targets for biotechnological improvement. Australian Journal of Grape and Wine Research 16, 106-121.
| Crossref | Google Scholar |

Fortes AM, Teixeira RT, Agudelo-Romero P (2015) Complex interplay of hormonal signals during grape berry ripening. Molecules 20, 9326-9343.
| Crossref | Google Scholar | PubMed |

Giacomelli L, Rota-Stabelli O, Masuero D, Acheampong AK, Moretto M, Caputi L, Vrhovsek U, Moser C (2013) Gibberellin metabolism in Vitis vinifera L. during bloom and fruit-set: functional characterization and evolution of grapevine gibberellin oxidases. Journal of Experimental Botany 64, 4403-4419.
| Crossref | Google Scholar | PubMed |

Gouthu S, Deluc LG (2015) Timing of ripening initiation in grape berries and its relationship to seed content and pericarp auxin levels. BMC Plant Biology 15, 46.
| Crossref | Google Scholar | PubMed |

Hatmi S, Villaume S, Trotel-Aziz P, Barka EA, Clement C, Aziz A (2018) Osmotic stress and ABA affect immune response and susceptibility of grapevine berries to gray mold by priming polyamine accumulation. Frontiers in Plant Science 9, 1010.
| Crossref | Google Scholar | PubMed |

Ismail A, Seo M, Takebayashi Y, Kamiya Y, Nick P (2015) A balanced JA/ABA status may correlate with adaptation to osmotic stress in Vitis cells. Journal of Plant Physiology 185, 57-64.
| Crossref | Google Scholar | PubMed |

Jing H, Strader LC (2019) Interplay of auxin and cytokinin in lateral root development. International Journal of Molecular Sciences 20, 486.
| Crossref | Google Scholar | PubMed |

Johnstone MMG, Reinecke DM, Ozga JA (2005) The auxins IAA and 4-Cl-IAA differentially modify gibberellin action via ethylene response in developing pea fruit. Journal of Plant Growth Regulation 24, 214-225.
| Crossref | Google Scholar |

Ke J, Ma H, Gu X, Thelen A, Brunzelle JS, Li J, Xu HE, Melcher K (2015) Structural basis for recognition of diverse transcriptional repressors by the TOPLESS family of corepressors. Science Advances 1, e1500107.
| Crossref | Google Scholar | PubMed |

Kondo S, Fukuda K (2001) Changes of jasmonates in grape berries and their possible roles in fruit development. Scientia Horticulturae 91, 275-288.
| Crossref | Google Scholar |

Kotakis C, Theodoropoulou E, Tassis K, Oustamanolakis C, Ioannidis NE, Kotzabasis K (2014) Putrescine, a fast-acting switch for tolerance against osmotic stress. Journal of Plant Physiology 171, 48-51.
| Crossref | Google Scholar | PubMed |

Koyama R, Roberto SR, de Souza RT, Borges WFS, Anderson M, Waterhouse AL, Cantu D, Fidelibus MW, Blanco-Ulate B (2018) Exogenous abscisic acid promotes anthocyanin biosynthesis and increased expression of flavonoid synthesis genes in Vitis vinifera × Vitis labrusca table grapes in a subtropical region. Frontiers in Plant Science 9, 323.
| Crossref | Google Scholar | PubMed |

Kühn N, Serrano A, Abello C, Arce A, Espinoza C, Gouthu S, Deluc L, Arce-johnson P (2016) Regulation of polar auxin transport in grapevine fruitlets (Vitis vinifera L.) and the proposed role of auxin homeostasis during fruit abscission. BMC Plant Biology 16, 234.
| Crossref | Google Scholar | PubMed |

Lauer H (2012) The effect of deficit irrigation on grape quality characteristics: an analysis of current literature. Master’s Thesis, Cornell University, Ithaca, NY, USA.

Li X, Zhang L-P, Zhang L, Yan P, Ahammed GJ, Han W-Y (2019) Methyl salicylate enhances flavonoid biosynthesis in tea leaves by stimulating the phenylpropanoid pathway. Molecules 24, 362.
| Crossref | Google Scholar | PubMed |

Li Z, Hou J, Zhang Y, Zeng W, Cheng B, Hassan MJ, Zhang Y, Pu Q, Peng Y (2020) Spermine regulates water balance associated with Ca2+-dependent aquaporin (TrTIP2-1, TrTIP2-2 and TrPIP2-7) expression in plants under water stress. Plant and Cell Physiology 61, 1576-1589.
| Crossref | Google Scholar | PubMed |

Lian TT, Moe MM, Kim YJ, Bang KS (2019) Effects of different colored leds on the enhancement of biologically active ingredients in callus cultures of Gynura procumbens (lour.) merr. Molecules 24, 4336.
| Crossref | Google Scholar | PubMed |

Lin M, Pang C, Fan S, Song M, Wei H, Yu S (2015) Global analysis of the Gossypium hirsutum L. transcriptome during leaf senescence by RNA-Seq. BMC Plant Biology 15, 43.
| Crossref | Google Scholar | PubMed |

Menéndez AB, Calzadilla PI, Sansberro PA, Espasandin FD, Gazquez A, Bordenave CD, Maiale SJ, Rodríguez AA, Maguire VG, Campestre MP, Garriz A, Rossi FR, Romero FM, Solmi L, Salloum MS, Monteoliva MI, Debat JH, Ruiz OA (2019) Polyamines and legumes: joint stories of stress, nitrogen fixation and environment. Frontiers in Plant Science 10, 1415.
| Crossref | Google Scholar | PubMed |

Mens C, Li D, Haaima LE, Gresshoff PM, Ferguson BJ (2018) Local and systemic effect of cytokinins on Soybean nodulation and regulation of their isopentenyl transferase (IPT) biosynthesis genes following rhizobia inoculation. Frontiers in Plant Science 9, 1150.
| Crossref | Google Scholar | PubMed |

Min Z, Li R, Chen L, Zhang Y, Li Z, Liu M, Ju Y, Fang Y (2019) Alleviation of drought stress in grapevine by foliar-applied strigolactones. Plant Physiology and Biochemistry 135, 99-110.
| Crossref | Google Scholar |

Minocha R, Majumdar R, Minocha SC (2014) Polyamines and abiotic stress in plants: a complex relationship. Frontiers in Plant Science 5, 175.
| Crossref | Google Scholar | PubMed |

Nadarajah K, Abdul Hamid NW, Abdul Rahman NSN (2021) SA-mediated regulation and control of abiotic stress tolerance in rice. International Journal of Molecular Sciences 22, 5591.
| Crossref | Google Scholar | PubMed |

Nambara E, Kuchitsu K (2011) Opening a new era of ABA research. Journal of Plant Research 124, 431-435.
| Crossref | Google Scholar | PubMed |

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. Journal of Plant Growth Regulation 32, 551-563.
| Crossref | Google Scholar |

Nishiyama R, Watanabe Y, Fujita Y, Le DT, Kojima M, Werner T, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Kakimoto T, Sakakibara H, Schmülling T, Tran L-SP (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. The Plant Cell 23(6), 2169-2183.
| Crossref | Google Scholar | PubMed |

Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Current Opinion in Plant Biology 14, 290-295.
| Crossref | Google Scholar |

Pérez FJ, Viani C, Retamales J (2000) Bioactive gibberellins in seeded and seedless grapes: identification and changes in content during berry development. American Journal of Enology and Viticulture 51, 315.
| Crossref | Google Scholar |

Pilati S, Bagagli G, Sonego P, Moretto M, Brazzale D, Castorina G, Simoni L, Tonelli C, Guella G, Engelen K, Galbiati M, Moser C (2017) Abscisic acid is a major regulator of grape berry ripening onset: new insights into ABA signaling network. Frontiers in Plant Science 8, 1093.
| Crossref | Google Scholar | PubMed |

Podlesakova K, Ugena L, Spichal L, Dolezal K, De Diego N (2019) Phytohormones and polyamines regulate plant stress responses by altering GABA pathway. New Biotechnology 48, 53-65.
| Crossref | Google Scholar | PubMed |

Qin L, Zhang X, Yan J, Fan L, Rong C, Mo C, Zhang M (2019) Effect of exogenous spermidine on floral induction, endogenous polyamine and hormone production, and expression of related genes in ‘Fuji’ apple (Malus domestica Borkh.). Scientific Reports 9, 12777.
| Crossref | Google Scholar | PubMed |

Raspor M, Motyka V, Ninković S, Dobrev PI, Malbeck J, Ćosić T, Cingel A, Savić J, Tadić V, Dragićević IČ (2020) Endogenous levels of cytokinins, indole-3-acetic acid and abscisic acid in in vitro grown potato: a contribution to potato hormonomics. Scientific Reports 10, 3437.
| Crossref | Google Scholar | PubMed |

Ribalta-Pizarro C, Munoz P, Munne-Bosch S (2021) Tissue-Specific hormonal variations in grapes of irrigated and non-irrigated grapevines (Vitis vinifera cv. “Merlot”) growing under mediterranean field conditions. Frontiers in Plant Science 12, 621587.
| Crossref | Google Scholar | PubMed |

Romero P, Gil-Muñoz R, del Amor FM, Valdés E, Fernández JI, Martinez-Cutillas A (2013) Regulated deficit irrigation based upon optimum water status improves phenolic composition in Monastrell grapes and wines. Agricultural Water Management 121, 85-101.
| Crossref | Google Scholar |

Salvi P, Manna M, Kaur H, Thakur T, Gandass N, Bhatt D, Muthamilarasan M (2021) Phytohormone signaling and crosstalk in regulating drought stress response in plants. Plant Cell Reports 40, 1305-1329.
| Crossref | Google Scholar | PubMed |

Seo SY, Kim YJ, Park KY (2019) Increasing polyamine contents enhances the stress tolerance via reinforcement of antioxidative properties. Frontiers in Plant Science 10, 1331.
| Crossref | Google Scholar | PubMed |

Sharma A, Sidhu GPS, Araniti F, Bali AS, Shahzad B, Tripathi DK, Brestic M, Skalicky M, Landi M (2020) The role of salicylic acid in plants exposed to heavy metals. Molecules 25, 540.
| Crossref | Google Scholar | PubMed |

Shellie KC, Bowen P (2014) Isohydrodynamic behavior in deficit-irrigated Cabernet Sauvignon and Malbec and its relationship between yield and berry composition. Irrigation Science 32, 87-97.
| Crossref | Google Scholar |

Shemi R, Wang R, Gheith EMS, Hussain HA, Hussain S, Irfan M, Cholidah L, Zhang K, Zhang S, Wang L (2021) Effects of salicylic acid, zinc and glycine betaine on morpho-physiological growth and yield of maize under drought stress. Scientific Reports 11, 3195.
| Crossref | Google Scholar | PubMed |

Shukla A, Srivastava S, Suprasanna P (2017) Genomics of metal stress-mediated signalling and plant adaptive responses in reference to phytohormones. Current Genomics 18, 512-522.
| Crossref | Google Scholar | PubMed |

Sugiura T, Hayashi T, Kawai S, Ohno T (1975) High-speed liquid chromatographic determination of putrescine, spermidine and spermine. Journal of Chromatography A 110, 385-388.
| Crossref | Google Scholar |

Teribia N, Tijero V, Munne-Bosch S (2016) Linking hormonal profiles with variations in sugar and anthocyanin contents during the natural development and ripening of sweet cherries. New Biotechnology 33, 824-833.
| Crossref | Google Scholar | PubMed |

Upreti KK, Murti GSR (2010) Response of grape rootstocks to salinity: changes in root growth, polyamines and abscisic acid. Biologia Plantarum 54, 730-734.
| Crossref | Google Scholar |

Wang W, Liu J-H (2016) CsPAO4 of Citrus sinensis functions in polyamine terminal catabolism and inhibits plant growth under salt stress. Scientific Reports 6, 31384.
| Crossref | Google Scholar | PubMed |

Wang H, Wu T, Liu J, Cong L, Zhu Y, Zhai R, Yang C, Wang Z, Ma F, Xu L (2020) PbGA20ox2 regulates fruit set and induces parthenocarpy by enhancing GA4 content. Frontiers in Plant Science 11, 113.
| Crossref | Google Scholar | PubMed |

Xu L, Yue Q, Bian F, Sun H, Zhai H, Yao Y (2017) Melatonin enhances phenolics accumulation partially via ethylene signaling and resulted in high antioxidant capacity in grape berries. Frontiers in Plant Science 8, 1426.
| Crossref | Google Scholar | PubMed |

Yang B, Yao H, Zhang JX, Li Y, Ju Y, Zhao X, Sun X, Fang Y (2020a) Effect of regulated deficit irrigation on the content of soluble sugars, organic acids and endogenous hormones in Cabernet Sauvignon in the Ningxia region of China. Food Chemistry 312, 126020.
| Crossref | Google Scholar | PubMed |

Yang B, He S, Liu Y, Liu B, Ju Y, Kang D, Sun X, Fang Y (2020b) Transcriptomics integrated with metabolomics reveals the effect of regulated deficit irrigation on anthocyanin biosynthesis in Cabernet Sauvignon grape berries. Food Chemistry 314, 126170.
| Crossref | Google Scholar | PubMed |

Yu R, Fidelibus MW, Kennedy JA, Kurtural SK (2021) Precipitation before flowering determined effectiveness of leaf removal timing and irrigation on wine composition of Merlot Grapevine. Plants (Basel) 10, 1865.
| Crossref | Google Scholar |

Yuzikhin OS, Shaposhnikov AI, Konnova TA, Syrova DS, Hamo H, Ermekkaliev TS, Shevchenko VP, Shevchenko KV, Gogoleva NE, Nizhnikov AA, Safronova VI, Kamnev AA, Belimov AA, Gogolev YV (2022) Isolation and characterization of 1-hydroxy-2,6,6-trimethyl-4-oxo-2-cyclohexene-1-acetic acid, a metabolite in bacterial transformation of abscisic acid. Biomolecules 12(10), 1508.
| Crossref | Google Scholar |

Zafar Z, Rasheed F, Atif RM, Javed MA, Maqsood M, Gailing O (2021) Foliar application of salicylic acid improves water stress tolerance in Conocarpus erectus L. and Populus deltoides L. saplings: evidence from morphological, physiological, and biochemical changes. Plants (Basel) 10, 1242.
| Crossref | Google Scholar | PubMed |

Zhang X, Luo G, Wang R, Wang J, Himelrick DG (2003) Growth and developmental responses of seeded and seedless grape berries to shoot girdlin. Journal of the American Society for Horticultural Science 128, 316-323.
| Crossref | Google Scholar |

Zhang Y, Li Y, Hassan MJ, Li Z, Peng Y (2020) Indole-3-acetic acid improves drought tolerance of white clover via activating auxin, abscisic acid and jasmonic acid related genes and inhibiting senescence genes. BMC Plant Biology 20, 150.
| Crossref | Google Scholar | PubMed |

Zsófi Z, Villangó S, Pálfi Z, Tóth E, Bálo B (2014) Texture characteristics of the grape berry skin and seed (Vitis vinifera L. cv. Kékfrankos) under postveraison water deficit. Scientia Horticulturae 172, 176-182.
| Crossref | Google Scholar |