Physiology and transcriptomic analysis reveals new insights into thermotolerance difference between heat tolerant and...

Grapevine is one of the most economically important fruit crops cultivated worldwide. In recent decades, the increasing frequency and intensity of high temperature (HT) events have posed significant challenges to viticulture. However, previous researches have mostly focused on heat-sensitive cultivars response to HT, and were conducted in artificially controlled growth chamber, which limited deep understanding of thermotolerance mechanism of grape. In this study, we conducted physiological and transcriptomic analyses of berries and leaves at different development stages in 'Guipu No.1' (GP, a hybrid of wild V. quinquangularis and V. vinifera, heat tolerant) and 'Cabernet Sauvignon' (CS, a cultivar from V. vinifera, heat sensitive) grapevines exposed to natural subtropical HT. Under HT conditions, GP maintained higher total anthocyanins content and photosynthetic capacity compared to CS. Differential expression was observed in genes involved in both the light and dark reactions of photosynthesis, as well as in structural genes and transcript factors associated with anthocyanins biosynthesis. Notably, protein processing in endoplasmic reticulum emerged as a key biological process potentially underlying thermotolerance differences. Based on the above results, we also identified and characterized a class B Heat Shock Factor, HSFB3, which was significantly up-regulated in GP but not in CS under HT. The GP-derived VqHSFB3 and CS-derived VvHSFB3 differed by only one amino acid and exhibited similar transcriptional repression activity. Overexpression of HSFB3 in grapevines indicated that it acts as a negative regulator of thermotolerance. Together, these findings provide new insights into the molecular and physiological basis of grapevine thermotolerance and offer potential targets for breeding heat-tolerant cultivars.