Specific ABA‐independent tomato transcriptome reprogramming under abiotic stress combination

Abstract

SUMMARYCrops often have to face several abiotic stresses simultaneously, and under these conditions, the plant's response significantly differs from that observed under a single stress. However, up to the present, most of the molecular markers identified for increasing plant stress tolerance have been characterized under single abiotic stresses, which explains the unexpected results found when plants are tested under real field conditions. One important regulator of the plant's responses to abiotic stresses is abscisic acid (ABA). The ABA signaling system engages many stress‐responsive genes, but many others do not respond to ABA treatments. Thus, the ABA‐independent pathway, which is still largely unknown, involves multiple signaling pathways and important molecular components necessary for the plant's adaptation to climate change. In the present study, ABA‐deficient tomato mutants (flacca, flc) were subjected to salinity, heat, or their combination. An in‐depth RNA‐seq analysis revealed that the combination of salinity and heat led to a strong reprogramming of the tomato transcriptome. Thus, of the 685 genes that were specifically regulated under this combination in our flc mutants, 463 genes were regulated by ABA‐independent systems. Among these genes, we identified six transcription factors (TFs) that were significantly regulated, belonging to the R2R3‐MYB family. A protein–protein interaction network showed that the TFs SlMYB50 and SlMYB86 were directly involved in the upregulation of the flavonol biosynthetic pathway‐related genes. One of the most novel findings of the study is the identification of the involvement of some important ABA‐independent TFs in the specific plant response to abiotic stress combination. Considering that ABA levels dramatically change in response to environmental factors, the study of ABA‐independent genes that are specifically regulated under stress combination may provide a remarkable tool for increasing plant resilience to climate change.

Multi-Omics Exploration of ABA Involvement in Identifying Unique Molecular Markers for Single and Combined Stresses in tomato plants

“…Romero et al (2012) demonstrated that the application of ABA in sweet orange plant fruits from ABA-deficient mutant plants under dehydration condition did not produce a recovery at the transcriptomic level with respect to WT, supporting the results found in these experiments (Romero et al ., 2012). This was observed with 903 DEGs compared to WT under control conditions and it was also noted in a previous work of our group (Pardo-Hernández et al ., 2024). On the other hand, a certain number of DEGs were treatment-specific, obtaining 117, 567, 774 and 1426 DEGs specifically regulated under control, salinity, heat and stress combination respectively.…”

“…Our research group has been demonstrating for more than a decade that the combination of abiotic stresses produces a specific response in plants that cannot be deduced from the application of the stresses separately. In addition, we have recently demonstrated that, although ABA is an essential hormone in these stress responses, there are certain genetic markers that are regulated independently of ABA and some of them are specific to the combination of salinity and heat (Pardo-Hernández et al ., 2024). Thus, this work was designed to further investigate the relationship between ABA and the possible coordination of the stress responses of tomato plants at different levels: phenomics, ionomics, transcriptomics, and metabolomics.…”

“…Throughout their whole life cycle, plants have to face different abiotic and biotic stresses, which often act simultaneously rather than independently (Husaini, 2022; López-Valdez et al ., 2022). Studies over the last decade have shown that plant responses to the combination of two or more abiotic stresses are unique and cannot be inferred from the study of plants exposed to each stress separately (Zandalinas et al ., 2021; Pascual et al ., 2022; Rivero et al ., 2022; Pardo-Hernández et al ., 2024). In addition, climate change and global warming are influencing crop yield via exacerbated biotic and abiotic stresses, and therefore, many scientists are investigating how to mitigate climate change effects or enhance the stress tolerance of plants (Shahzad et al ., 2022; Asif et al ., 2023).…”

“…Nevertheless, plants can also respond to stresses in an ABA-independent way. Our research group recently demonstrated that under abiotic stress combination and ABA-deficiency, an ABA-independent regulation of certain genes encoding for transcription factors or proteins involved in the stress response of plants occurs (Pardo-Hernández et al ., 2024). For instance, other researchers have showed that ubiquitin ligases ATL31 and ATL6 in Arabidopsis and choline monoooxygenase in Kochia scoparia regulate plant response to salt stress through an ABA-independent pathway (Kalinina et al ., 2012; Du et al ., 2023).…”

Arabidopsis ubiquitin ligase PUB41 is a positive regulator of the ABA response

“…Although ABA signaling results in a global change of gene expression (Rock 2000), the hormone does not affect the expression of genes involved in the response to ABA itself (for example, see (Pardo-Hernández et al 2024)). We thus treated seedlings with ABA and assayed the effect on AtPUB41 expression.…”