Elsevier

Food Chemistry

Volume 212, 1 December 2016, Pages 828-836
Food Chemistry

Polyphenolic responses of grapevine berries to light, temperature, oxidative stress, abscisic acid and jasmonic acid show specific developmental-dependent degrees of metabolic resilience to perturbation

https://doi.org/10.1016/j.foodchem.2016.05.164Get rights and content

Highlights

  • The extent of metabolite alteration in response to stress was developmental stage-dependent.

  • Greater magnitudes of metabolite fluctuations characterize the pre-veraison berries.

  • Flavonoid accumulation at veraison stage enhanced the berry resilience to the cue-induced changes.

Abstract

Grape-berries are exposed to a plethora of abiotic and biotic stimuli during their development. The developmental and temporal regulation of grape berry polyphenol metabolism in response to various cues was investigated using LC-QTOF-MS based metabolite profiling. High light (2500 μmol m−2 s−1), high temperature (40 °C), jasmonic acid (200 μM), menadione (120 μM) and abscisic acid (3.026 mM) treatments were applied to detached berries. Greater magnitudes of metabolite fluctuations characterize the pre-veraison berries than the veraison stage in response to the treatments. Furthermore, a tighter co-response of metabolic processes was shown at veraison, likely supporting the resilience to change in response to stress. High temperature and ABA treatments led to greater magnitudes of change during the course of the experiment. The present study demonstrates the occurrence of differential patterns of metabolic responses specific to individual cues and berry developmental stage, which in the field are commonly associated and thus hardly discernable.

Introduction

Global warming is becoming a challenge for the viticulture industry and, in the past 55 years, it has already affected most grape growing areas (Jones, White, Cooper, & Storchmann, 2005) due to major shifts in temperature, precipitation, and CO2 concentration. This trend is affecting grape berry metabolite composition and the final wine quality; for example, there are increases in sugar levels and thus in the alcohol percent of the wine. In the field, grape berry development is under the regulation of complex factors with very different outcomes depending on the timing of the stress, from fruit abortion to earlier maturation (Webb, Whetton, & Barlow, 2007), and on the variety (Degu et al., 2014). The reoccurrence of combined multiple environmental stresses poses a risk to the crop yield and quality. Excessive temperature (>35 °C) during the growing season can severely damage leaf photosynthetic efficiency and berry metabolism (Chuine et al., 2004). Water deficit affects berry quality in a developmental manner (Matthews & Anderson, 1988) as well as canopy development, thus exposing the clusters to other environmental hazards, e.g. heat, wind and solar radiation.

Stress response involves the biosynthesis and delivery of related endogenous hormones such as jasmonic acid and ABA, which mediate the plant physiology and metabolism (Lurie et al., 2009). Oxygen-derived free radicals are associated with environmental stresses and function also as signaling molecules to induce cellular changes and respond to the environment (Vranova, Inzé, & Van Breusegem, 2002). For instance, the signaling role of ROS under stress and its association with ABA and calcium mobilization (Verslues & Zhu, 2005) suggest its involvement in triggering a plant stress response. However, excessive ROS production due to prolonged stress poses a cellular hazard (Smirnoff, 1993).

At the cellular level, plants react to stress related stimuli by mediating the biosynthesis of a wide range of chemical species with diverse properties, from compatible solutes (Xiong & Zhu, 2002) to complex phytochemicals (Apel & Hirt, 2004). Among the metabolic pathways involved in stress responses in grape-berries, polyphenol metabolism is highly relevant to fruit quality as it is composed of flavonoid classes, such as anthocyanins, flavonols, flavanones and flavanols. The expression of polyphenol biosynthetic genes characterized in grapevine is dependent on developmental stage, tissue type, cultivar (Sparvoli, Martin, Scienza, Gavazzi, & Tonelli, 1994) and their interaction with the environment (Deluc et al., 2009).

These responses are accompanied by a change in expression of a plethora of genes (Cramer et al., 2007). Nevertheless, dissecting the effect of individual environmental signals on fruits in the field is challenging, as they appear concomitantly and pose confounding or synergetic effects. Pedicel bearing detached berry has been used as a model system to study berry maturation processes (Lurie et al., 2009) and can be handled under a controlled environment in the lab to investigate the effect of individual and combined environmental cues.

In the present study, detached berries of Shiraz grapevine were exposed to individual stresses or stress signals to explore their effect on berry phenolic biosynthesis. Previously it has been confirmed that Shiraz vines are more responsive to environmental perturbation, particularly to water stress, than are Cabernet Sauvignon vines (Hochberg, Degu, Cramer, Rachmilevitch, & Fait, 2015). In light of these results, detached berries of Shiraz at the hard-green stage (pre-veraison) and veraison stage (90% color change) were used as a model system in order to gain insights into developmental stage-dependent berry skin metabolic perturbation in response to individual environmental cues: high light (HL), high temperature (HT), ABA, jasmonic acid (JA) and menadione (Mn) (as oxidative stress inducer). Exogenous applications of menadione have been used to mimic the effect of ROS at the molecular level (Schwarzländer, Fricker, & Sweetlove, 2009). The results are discussed within the frame of the current knowledge on the regulation of polyphenol metabolism.

Section snippets

Plant material and experimental conditions

Shiraz grape berries grown at Ramat Hanegev Research center vineyard were excised for experiments at two phenological stages, at green (pre-veraison – 62 days after anthesis (DAA)) and veraison stages (75 DAA) (Supplementary Fig. 1) during the 2014 growing season. The vines were trained in a vertical shoot position (VSP) trellis system and oriented in N-S position. The entire bunch cluster (Supplementary Fig. 1) was taken from the east side (sun-exposed) of the vine. The pre-veraison stage

Metabolite changes in response to different environmental cues

The metabolite changes in response to the cues were measured at 6 h, 12 h, 24 h and 48 h. The unsupervised multivariate data analysis using PCA plot based on metabolite response values clearly separated the treatments with distinct projections. Particularly samples exposed to HT were separated from the rest of the treatments in both pre-veraison and veraison stages. To aid in exploring the results, PCA was re-run on the treatments not including HT. On the first principal components (PC1) samples

Discussion

In red grapevine cultivars, berries undergo a series of developmental phases, beginning with the photosynthetically active green stage, through veraison, to the red-pigmented berry. Each developmental phase, is characterized by a berry’s unique metabolite composition (Deluc et al., 2007). Thus, environmental perturbations at different developmental stages will affect the berry metabolism differently due to variations in metabolic composition and will lead to diverse outputs at harvest,

Conclusion

The present study reveals the occurrence of developmental and time-mediated regulation of the metabolic response to stress in polyphenol metabolism. The detached berry approach used aided in discriminating metabolic responses amongst the stresses that in the field are usually combined. The metabolic responses were greater in pre-veraison than veraison-stage berries. The exogenous cues applied and their modulation over time indicated repartitioning within the polyphenol branching pathways,

Competing interests

The authors declare that they have no competing interests.

Acknowledgments

This research was supported by the Binational Agricultural Research and Development Fund (BARD) (grant number IS-4325-10) and partly funded by the Israeli Ministry of Agriculture (grant number 857-0614-09). We acknowledge the Ramat haNegev research and developmental station for the maintenance of the vines.

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