Spatiotemporal dynamics of the tomato fruit transcriptome under prolonged water stress

Authors: NICOLAS, PHILIPPE - Boyce Thompson Institute; SHINOZAKI, YOSHIHITO - Cornell University; POWELL, ADRIAN - Boyce Thompson Institute; PHILIPPE, GLEN - Cornell University; SNYDER, STEPHEN - Cornell University; GAO, KAN - Boyce Thompson Institute; ZHENG, YI - Boyce Thompson Institute; XU, YIMIN - Boyce Thompson Institute; COURTNEY, LANCE - Boyce Thompson Institute; VREBALOV, JULIA - Boyce Thompson Institute; CASTEEL, CLARE - Cornell University; MUELLER, LUKAS - Boyce Thompson Institute; FEI, ZHANGJUN - Boyce Thompson Institute; Giovannoni, James; ROSE, JOCELYN K C - Cornell University; CATALA, CARMEN - Boyce Thompson Institute

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/7/2022
Publication Date: 9/22/2022
Citation: Nicolas, P., Shinozaki, Y., Powell, A., Philippe, G., Snyder, S., Gao, K., Zheng, Y., Xu, Y., Courtney, L., Vrebalov, J., Casteel, C., Mueller, L., Fei, Z., Giovannoni, J.J., Rose, J., Catala, C. 2022. Spatiotemporal dynamics of the tomato fruit transcriptome under prolonged water stress. Plant Physiology. https://doi.org/10.1093/plphys/kiac445.
DOI: https://doi.org/10.1093/plphys/kiac445

Interpretive Summary: Environmental conditions have fundamental impacts on plant development and crop productivity, which will be amplified by climate change. Increased drought duration and an overall decrease in water availability are major contributors to plant stress and performance under changing environmental conditions . Thus, there is a pressing need to better understand the mechanisms employed by plants to adapt to drought and in all tissues and organs including the fruit. Development of the fruit, especially during its early stages, is particularly sensitive to water stress and this can be a major factor limiting crop yield. Surprisingly, to date, few studies on drought have centered on the fruit, rather such studies tend to focus on development of the leaves, stems, flowers and roots. Here we characterized the distribution and timing of gene expression shifts in response to water stress and revealed tissue-specific changes associated with the regulation of the fruit response to water deficit. We also collected expression data from tomato leaves for comparison and find distinct responses that help the fruit in coping with reduced water. This study expands our understanding of the molecular mechanisms involved in acclimation to water deficit and suggests genes that could be targeted by plant breeders for development of more climate resilient crops.

Technical Abstract: Water availability influences all aspects of plant growth and development; however, most studies of plant responses to drought have focused on vegetative organs, notably roots and leaves. Far less is known about the molecular bases of drought acclimation responses in fruits, which are complex organs with distinct tissue types. To obtain a more comprehensive picture of the molecular mechanisms governing fruit development under drought, we profiled the transcriptomes of a spectrum of fruit tissues from tomato (Solanum lycopersicum), spanning early growth through ripening and collected from plants grown under varying intensities of water stress. In addition, we compared transcriptional changes in fruit with those in leaves to highlight different and conserved transcriptome signatures in vegetative and reproductive organs. We observed extensive and diverse genetic reprogramming in different fruit tissues and leaves, each associated with a unique response to drought acclimation. These included major transcriptional shifts in the placenta of growing fruit and in the seeds of ripe fruit, related to cell growth and epigenetic regulation, respectively. Changes in metabolic and hormonal pathways, such as those related to starch, carotenoids, jasmonic acid and ethylene metabolism, were associated with distinct fruit tissues and developmental stages. Gene co-expression network analysis provided further insights into the tissue-specific regulation of distinct responses to water stress. Our data highlight the spatiotemporal specificity of drought responses in tomato fruit and indicate known and novel molecular regulatory mechanisms involved in drought acclimation, during both vegetative and reproductive stages of development.