New insights into the heat responses of grape leaves via combined phosphoproteomic and acetylproteomic analyses

Abstract

Heat stress is a serious and widespread threat to the quality and yield of many crop species, including grape (Vitis vinifera L.), which is cultivated worldwide. Here, we conducted phosphoproteomic and acetylproteomic analyses of leaves of grape plants cultivated under four distinct temperature regimes. The phosphorylation or acetylation of a total of 1011 phosphoproteins with 1828 phosphosites and 96 acetyl proteins with 148 acetyl sites changed when plants were grown at 35 °C, 40 °C, and 45 °C in comparison with the proteome profiles of plants grown at 25 °C. The greatest number of changes was observed at the relatively high temperatures. Functional classification and enrichment analysis indicated that phosphorylation, rather than acetylation, of serine/arginine-rich splicing factors was involved in the response to high temperatures. This finding is congruent with previous observations by which alternative splicing events occurred more frequently in grapevine under high temperature. Changes in acetylation patterns were more common than changes in phosphorylation patterns in photosynthesis-related proteins at high temperatures, while heat-shock proteins were associated more with modifications involving phosphorylation than with those involving acetylation. Nineteen proteins were identified with changes associated with both phosphorylation and acetylation, which is consistent with crosstalk between these posttranslational modification types.

Identification and Characterization of Contrasting Genotypes/Cultivars for Developing Heat Tolerance in Agricultural Crops: Current Status and Prospects

“…Post-pollination events that are highly susceptible to heat stress are (1) pollen load (Prasad et al, 1999b(Prasad et al, , 2006, (2) pollen germination (Prasad et al, 2001), (3) pollen tube growth (Prasad et al, 2001), and (4) fertilization (Prasad et al, 2001;Barnabás et al, 2008;Hedhly, 2011;Sita et al, 2017b). The development of male gametophyte under high temperature is more susceptible than female gametophyte (Djanaguiraman et al, 2018a;Liu et al, 2019). However, in peal millet (Pennisetum glaucum), the female gametophyte was more sensitive than male gameophyte (Djanaguiraman et al, 2018b).…”

“…Considering contributory role of proteins adapting roots under heat stress, Valdes-Lopez et al (2016) reported the involvement of both up and down regulatory proteins contributing to heat tolerance in soybean root. Recently, proteomics analysis deduced that protein phosphorylation and protein acetylation could regulate heat tolerance by modulating photosynthesis protein in grape (Liu et al, 2019). The proteins involved in heat tolerance elucidated through proteomics analysis could serve as biomarkers for identifying heat tolerant cultivars in various crop plants.…”

Molecular Tools for Adapting Viticulture to Climate Change

“…In grapevine, application of a heat shock (35–45°C) greatly modified the leaf transcriptome, AS pattern, and proteome ( Jiang et al, 2017 ). In particular, the transcription level of several SR proteins, as well as their phosphorylation status, a marker of functionality, significantly increased with temperature, showing that the whole splicing machinery was modulated ( Jiang et al, 2017 ; Liu et al, 2019 ). Because transcription and translation are energy costly, the strong induction of AS under stress conditions is suspected to be a means for reducing the amount and diversity of translatable transcripts ( Chaudhary et al, 2019 ).…”

Protein phosphorylation associated with drought priming-enhanced heat tolerance in a temperate grass species

“…Previous researches have shown that rapid accumulation of heat shock proteins is critically important for drought- and heat-priming of plants 9 , 10 . In addition to modification at gene transcript and protein levels, drought priming may affect protein post-translational modifications (PTMs) which affect the structure, localization, and activity of proteins, ultimately regulating plant growth and development, and mediating plant responses to environmental stimulus 11 , 12 . Protein phosphorylation in the process of PTMs plays crucial roles in plant stress tolerance by transmitting intracellular signals from the cell surface to the nucleus to regulate cellular functions of proteins 13 .…”

“…For example, large-scale quantitative phosphoproteome analysis in tomato ( Solanum lycopersicum ) plants identified novel signaling cascades involving different kinases that regulate cold acclimation 15 . Several studies reported phosphoproteins responsive to drought or heat stress individually 12 , 16 . For example, Liu et al 12 identified up-regulated phosphoproteins of SR-rich splicing factors and heat shock proteins involved in heat stress responses in grape ( Vitis vinifera ) leaves.…”