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Abstract :

Viticulture covers a large part of the arable land in the Mediterranean regions. However, the maintenance of this emblematic crop in drought-prone environments is threatened by climate change. Exploring large genetic collections can help select more water-efficient cultivars. Stomata, tiny pores on the leaf epidermis bounded by guard cells that can open and close, play an essential role in this process as they regulate gas exchange - photosynthesis and transpiration - between the plant and the atmosphere. Due to stomatal behaviour, increased photosynthesis usually coincides with increased transpiration. Thus, reducing night transpiration appears to be a promising breeding strategy to reduce water loss without penalising photosynthesis. However, day and night transpiration are correlated to some extent. Here, we explored the genetic and physiological basis of the daily (24 h) dynamics of transpiration in grapevine (Vitis vinifera). A protocol was developed for high-throughput phenotyping of transpiration dynamics in detached leaves. This allowed genome-wide association studies (GWAS) to be carried out on a diversity panel of 279 cultivars, which generated candidate genes that were then studied using different approaches. Quantitative genetic analyses revealed several single nucleotide polymorphisms (SNPs) associated with different aspects of transpiration dynamics. In particular, we found an association for nocturnal transpiration that co-located with the abundance of recumbent trichomes and cuticular striae on the leaf epidermis. A MYB transcription factor was identified as a strong candidate involved in the production of both structures, showing a complex interaction with stomatal development. Based on genomic and coexpression analyses, we propose a new model of interacting genes involved in the development of epidermal structures and impacting on night transpiration. Unexpectedly, we also found an association for daytime transpiration close to a gene essential for nocturnal starch metabolism. The corresponding mutant in Arabidopsis thaliana was impaired in stomatal light opening and endogenous nighttime reopening. Comparison with other mutants in the pathway revealed that the role of this gene in the control of stomatal movements extends beyond starch metabolism. Its cell-autonomous action was studied, with equivocal conclusions. Overall, this work provided several interesting targets for night-time water saving and water use efficiency in grapevines.