Spatiotemporal dynamics of the tomato fruit transcriptome under prolonged water stress

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 unrevealed molecular regulatory mechanisms involved in drought acclimation, during both vegetative and reproductive stages of development.

Transcriptomic analysis reveals the gene regulatory networks involved in leaf and root response to osmotic stress in tomato

“…Since many molecular factors may operate regardless of organ specificity, leaf and root organs should not be considered separately from the whole plant to understand the complex molecular network of drought response and its regulatory mechanisms. Finally, very few studies described GCNs involved in water stress response in tomato (Nicolas et al, 2022;Wei et al, 2023).…”

Integrative analysis of the methylome and transcriptome of tomato fruit (Solanum lycopersicum L.) induced by postharvest handling

“…This may underscore the significance of fruit photosynthetic activity during ripening. A recent study reported that fruit photosynthetic gene expression is upregulated in both green and ripened fruit under water stress when source capacity is constrained [ 71 ], indicating a dynamic tradeoff between source and sink photosynthesis to support organ development.…”

Integrative analysis of the methylome and transcriptome of tomato fruit (Solanum lycopersicumL.) induced by postharvest handling

“…SGR1 is reported to be activated by fruit development and cold temperature 71 , suggesting our postharvest treatments may not have direct effect on chlorophyll degradation. A recent study reported that fruit photosynthetic gene expression is upregulated in both green and ripened fruit under water stress when source capacity is constrained 72 . This indicates a dynamic tradeoff between source and sink photosynthesis to support organ development.…”