Secondary metabolites in grapevine: crosstalk of transcriptional, metabolic and hormonal signals controlling stress defence responses in berries and vegetative organs

Abstract

Abiotic stresses, such as temperature, heat waves, water limitation, solar radiation and the increase in atmospheric CO2 concentration, significantly influence the accumulation of secondary metabolites in grapevine berries at different developmental stages, and in vegetative organs. Transcriptional reprogramming, miRNAs, epigenetic marks and hormonal crosstalk regulate the secondary metabolism of berries, mainly the accumulation of phenylpropanoids and of volatile organic compounds (VOCs). Currently, the biological mechanisms that control the plastic response of grapevine cultivars to environmental stress or that occur during berry ripening have been extensively studied in many worlds viticultural areas, in different cultivars and in vines grown under various agronomic managements. A novel frontier in the study of these mechanisms is the involvement of miRNAs whose target transcripts encode enzymes of the flavonoid biosynthetic pathway. Some miRNA-mediated regulatory cascades, post-transcriptionally control key MYB transcription factors, showing, for example, a role in influencing the anthocyanin accumulation in response to UV-B light during berry ripening. DNA methylation profiles partially affect the berry transcriptome plasticity of different grapevine cultivars, contributing to the modulation of berry qualitative traits. Numerous hormones (such as abscisic and jasmomic acids, strigolactones, gibberellins, auxins, cytokynins and ethylene) are involved in triggering the vine response to abiotic and biotic stress factors. Through specific signaling cascades, hormones mediate the accumulation of antioxidants that contribute to the quality of the berry and that intervene in the grapevine defense processes, highlighting that the grapevine response to stressors can be similar in different grapevine organs. The expression of genes responsible for hormone biosynthesis is largely modulated by stress conditions, thus resulting in the numeourous interactions between grapevine and the surrounding environment.

UV light and adaptive divergence of leaf physiology, anatomy, and ultrastructure drive heat stress tolerance in genetically distant grapevines

“…Regarding the genetic basis and phenotypical mechanisms activated in response to light, heat, and/or water stresses, many findings have been reported ( Wahid et al., 2007 ; Salem-Fnayou et al., 2011 ; Janni et al., 2020 ; Ferrandino et al., 2023 ), and different molecular mechanisms to keep leaf cell homeostasis and high physiological performances were identified in grapevine varieties adapted to different environmental conditions ( Pelsy, 2010 ; Carvalho et al., 2015a ). The main changes in plant anatomy are common to that observed under drought and include cell size reduction, enlarged xylem vessels, increased leaf blade thickness, stomatal and trichoma density, and a smaller proportion of palisade mesophyll ( Wahid et al., 2007 ; Salem-Fnayou et al., 2011 ).…”

“…At the cellular level, gradual exposure to heat determines enzymatic inactivation in chloroplasts and mitochondria, inhibition of protein synthesis, and enhanced plasma membrane permeability, whereas direct severe damages caused by very high temperature are related to increased lipid fluidity in membranes and protein denaturation, hence the loss of membrane integrity ( Haider et al., 2021 ). Grapevine responses and acclimation to heat stress, either caused by abrupt increases or gradual exposure to high temperatures, involve deep alteration in gene expression and transcript accumulation, coding for primary or secondary metabolism proteins and leading to the synthesis of different stress-related proteins that associate with cell wall, chloroplasts, ribosomes, and mitochondria, preserving their structural integrity and function and preventing other protein denaturation ( Wahid et al., 2007 ; Ferrandino et al., 2023 ). Different transcription factors and heat shock proteins may be involved in abiotic stress responses, therefore establishing different stress tolerance strategies ( Janni et al., 2020 ).…”

“…Different transcription factors and heat shock proteins may be involved in abiotic stress responses, therefore establishing different stress tolerance strategies ( Janni et al., 2020 ). Simultaneously, the complex hormonal signaling network (namely, abscisic acid, jasmonate, or carotenoid-derived hormone crosstalk pathways) triggers the activation of defense mechanisms, including enzymatic and non-enzymatic detoxification of reactive oxygen species to protect cells from oxidative injuries, including the synthesis of secondary metabolites such as flavonoids, glutathione, and ascorbic acid ( Chen et al., 2022 ; Ferrandino et al., 2023 ). Under diverse genotype–environmental stress combinations (e.g., heat, drought, and UV-B light), the expression of genotype-specific heat shock proteins (HSP) determine cell and tissue stress tolerance strategy and the accumulation of different compatible solutes like sugar, sugar-alcohols, proline, and other osmolytes that buffer cellular redox potential and mediate flavonoid biosynthesis.…”

“…Under diverse genotype–environmental stress combinations (e.g., heat, drought, and UV-B light), the expression of genotype-specific heat shock proteins (HSP) determine cell and tissue stress tolerance strategy and the accumulation of different compatible solutes like sugar, sugar-alcohols, proline, and other osmolytes that buffer cellular redox potential and mediate flavonoid biosynthesis. Therefore, genotype-specific HSP allow for the improvement of membrane stability, thus reducing the impact of high temperatures on leaf gas exchanges and water use efficiency as well as on nutrient and photosynthate partitioning and plant growth ( Wahid et al., 2007 ; Ferrandino et al., 2023 ). Plant exposure to high UV-B doses may lead to the excessive production of ROS and reduced photosynthesis, impairing photochemical efficiency, reducing photosynthetic pigment accumulation, and inducing the proteolytic degradation of Rubisco.…”

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“…The important role played by local biodiversity on vineyard plasticity in a changing climate must be further considered when evaluating the best viticulture strategies to cope with global warming since not only the local varieties have justified grapevine cultivation for centuries but they also guaranteed acclimation under local environments (Merrill et al, 2020;Antolıń et al, 2021;Naulleau et al, 2021). Therefore, other than the different plant agronomical traits and berry characteristics that determined vineyard resilience and wine typicity in distinct wine-producing areas, morpho-anatomical and physiological differences among cultivars should also be further explored, as they can give new insights on the extent of varietal resilience or tolerance to abiotic stress conditions, to better understand cultivar responses to the changing climate in order to support viticulture adaptation in arid and semiarid regions for the near future (Ferrandino et al, 2023).…”