Global transcriptome and gene co-expression network analyses reveal regulatory and non-additive effects of drought and heat stress in grapevine

Abstract

Despite frequent co-occurrence of drought and heat stress, the molecular mechanisms governing plant responses to these stresses in combination have not often been studied. This is particularly evident in non-model, perennial plants. We conducted large scale physiological and transcriptome analyses to identify genes and pathways associated with grapevine response to drought and/or heat stress during stress progression and recovery. We identified gene clusters with expression correlated to leaf temperature and water stress and five hub genes for the combined stress co-expression network. Several differentially expressed genes were common to the individual and combined stresses, but the majority were unique to the individual or combined stress treatments. These included heat-shock proteins, mitogen-activated kinases, sugar metabolizing enzymes, and transcription factors, while phenylpropanoid biosynthesis and histone modifying genes were unique to the combined stress treatment. Following physiological recovery, differentially expressed genes were found only in plants under heat stress, both alone and combined with drought. Taken collectively, our results suggest that the effect of the combined stress on physiology and gene expression is more severe than that of individual stresses, but not simply additive, and that epigenetic chromatin modifications may play an important role in grapevine responses to combined drought and heat stress.

Transcriptome Analysis Reveals Long-Term Somatic Memory of Stress in The Woody Perennial Crop, GrapevineVitis Viniferacv. Cabernet Sauvignon

“…GO analysis of naïve plant exclusive DEGs showed enrichment in histone methylation, covalent chromatin modification, and histone lysine methylation (Table S3A). Similar GO terms were observed in first-year plants by Tan et al (2023b) under combined treatment. DEGs exclusive to primed plants exposed to a second stress were enriched for anatomical structure development and developmental process and GO terms associated with methylation were also identified (Table S3B).…”

“…This comparison served two functions, first to identify the genes differentially expressed by naïve plants when exposed to a first stress event. Secondly, these results also served as validation of the results presented by Tan et al (2023b) for season 1, as the naïve plants priming state and growing conditions replicated those in that experiment. In this comparison, 176 genes were found to be up-regulated, and 431 were down-regulated (Figure 1A) in naïve plants grown under stress conditions (ST4 2 03), compared to naïve plants grown under control conditions (ST4 2 00).…”

“…To test the establishment, maintenance, and priming effect of long-term memory of stress in V. vinifera, a two-growing seasons experiment was carried out during 2016, 2017, and 2018 (Figure 6). Plant material and growth conditions during the first growing season are described in detail in Tan et al (2023b). In short, 64 propagated dormant cuttings obtained from six donor vines ( V. vinifera L. Cabernet Sauvignon) were randomly allocated into two different groups (i.e., control and combined drought and heat stress (T0 and T3 respectively hereafter)), and randomly divided into five replicate plots.…”

“…In short, 64 propagated dormant cuttings obtained from six donor vines ( V. vinifera L. Cabernet Sauvignon) were randomly allocated into two different groups (i.e., control and combined drought and heat stress (T0 and T3 respectively hereafter)), and randomly divided into five replicate plots. Plants were then exposed to combined drought and heat stress as described in Tan et al (2023b). Briefly, the experimental design incorporated drought and high temperature stresses in a factorial design as in Edwards et al (2011).…”

“…Water stress was imposed by removing drippers and monitoring stress using measurements of stomatal conductance (g s ), with small amounts of additional water provided as required to maintain g s in the 50-75 mmol/m -2 /s -1 range. The water stress treatment started on 23/1/2018, with heat stress generated for two days using natural insolation, as in Tan et al (2023b), on 4-5/2/2018. On the second day of combined stress of year 2, g s was measured on every vine (64 in total) at approximately 4 PM, then a single set of measurements (stem water potential (Ψs), leaf temperature, g s and leaf sampling (snap-frozen leaves for DNA and RNA analysis) was undertaken (Figure 6B), as described in Tan et al (2023b), with the exception that it was not possible to take g s measurements on every leaf (2-3 reps per 2017/2018 treatment).…”