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. 2022 Nov 25:13:974048.
doi: 10.3389/fpls.2022.974048. eCollection 2022.

Transcriptomic and splicing changes underlying tomato responses to combined water and nutrient stress

Alessandra Ruggiero  1 , Paola Punzo  1 , Michael James Van Oosten  2 , Valerio Cirillo  2 , Salvatore Esposito  3 , Antonello Costa  1 , Albino Maggio  2 , Stefania Grillo  1 , Giorgia Batelli  1
Affiliations

Transcriptomic and splicing changes underlying tomato responses to combined water and nutrient stress

Alessandra Ruggiero et al. Front Plant Sci. .

Abstract

Tomato is a horticultural crop of high economic and nutritional value. Suboptimal environmental conditions, such as limited water and nutrient availability, cause severe yield reductions. Thus, selection of genotypes requiring lower inputs is a goal for the tomato breeding sector. We screened 10 tomato varieties exposed to water deficit, low nitrate or a combination of both. Biometric, physiological and molecular analyses revealed different stress responses among genotypes, identifying T270 as severely affected, and T250 as tolerant to the stresses applied. Investigation of transcriptome changes caused by combined stress in roots and leaves of these two genotypes yielded a low number of differentially expressed genes (DEGs) in T250 compared to T270, suggesting that T250 tailors changes in gene expression to efficiently respond to combined stress. By contrast, the susceptible tomato activated approximately one thousand and two thousand genes in leaves and roots respectively, indicating a more generalized stress response in this genotype. In particular, developmental and stress-related genes were differentially expressed, such as hormone responsive factors and transcription factors. Analysis of differential alternative splicing (DAS) events showed that combined stress greatly affects the splicing landscape in both genotypes, highlighting the important role of AS in stress response mechanisms. In particular, several stress and growth-related genes as well as transcription and splicing factors were differentially spliced in both tissues. Taken together, these results reveal important insights into the transcriptional and post-transcriptional mechanisms regulating tomato adaptation to growth under reduced water and nitrogen inputs.

Keywords: differential alternative splicing; differential gene expression; leaf; low nitrate; root; tolerant and sensitive genotypes; water deficit.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Biometric parameters measured at the end of the experiment in the four treatments in all genotypes. (A) Height; (B) Leaf area; (C) Shoot fresh weight; (D) Shoot dry weight. Values indicate mean ± SE (n≥6). Different letters indicate significant difference within each genotype at p< 0.05 (Duncan test).
Figure 2
Figure 2
Heatmap constructed through ClustVis (http://biit.cs.ut.ee/clustvis/) of percentage differences in physiological and biometric parameters measured in plants of the 10 genotypes analysed (See Supplementary Datasheet S1 ) subjected to combined stress versus control condition. The red-blue color gradient scaling is indicated, where red and blue colors indicate highest and lowest variations in values measured in stressed plants compared to controls, respectively. Rows and columns are clustered through correlation distance and average linkage. RootDW, Root Dry Weight; gs, Stomatal Conductance; ShootFW, Shoot Fresh Weight; ShootDW, Shoot Dry Weight; RWC, Leaf Relative Water Content; SPAD, Leaf SPAD Values.
Figure 3
Figure 3
Representative plants of genotypes T250 (left) and T270 (right) grown for 24 days in Control (Ct), Low Nutrient (LN), Drought (Dr) or Combined stress (Cm) condition.
Figure 4
Figure 4
Differentially expressed genes (DEGs) and enriched Gene Ontology terms in leaves of T250 and T270 subjected to combined stress. (A) MA plots depicting the distribution of DEGs (green dots, down-regulated, red dots, up-regulated) in T270 (left) and T250 (right) leaves. X-axis: log2 mean expression across treatments; Y-axis: log2 expression fold change in combined stress vs. control treatments. (B) Venn diagrams depicting number and overlap of up-regulated (upper panel) and down-regulated (lower panel) DEGs in leaves of combined stress-treated T250 and T270. The diagrams were drawn using the online tool Venny (Oliveros, 2007-2015); (C, D) Plots showing enriched GO terms in leaf DEGs up (C) or down-regulated (D) in T270 (left) or T250 (right). Symbols indicate GO categories: MF, Molecular Function; CC, cellular compartment, BP, biological process. Symbol sizes are proportional to the gene count, whereas colors represent FDR values< 0.05. X-axis: enrichment score. Categories with ES> 5 and gene count > 4 are shown.
Figure 5
Figure 5
Differentially expressed genes (DEGs) and enriched Gene Ontology terms in roots of T250 and T270 subjected to combined stress. (A) MA plots depicting the distribution of DEGs (green dots, down-regulated, red dots, up-regulated) in T270 (left) and T250 (right) roots. X-axis: log2 mean expression across treatments; Y-axis: log2 expression fold change in combined stress vs. control treatments. (B) Venn diagrams depicting number and overlap of up-regulated (upper panel) and down-regulated (lower panel) DEGs in roots of combined stress-treated T250 and T270. The diagrams were drawn using the online tool Venny (Oliveros, 2007-2015); (C, D) Plots showing enriched GO terms in root DEGs up (C) or down-regulated (D) in T270 (left) or T250 (right). Symbols indicate GO categories: MF, Molecular Function; CC, cellular compartment, BP, biological process. Symbol sizes are proportional to the gene count, whereas colors represent FDR values< 0.05. X-axis: enrichment score. Categories with ES> 5 and gene count > 4 are shown.
Figure 6
Figure 6
Alternative splicing (AS) regulation in root and leaf of T250 and T270 under combined stress condition. (A, B) Bar graph of the number of differential up- (A) and down-regulated (B) AS events. (C) Number of genes concerned by DAS (left) and DAS events (right). (D) Venn diagram depicting the number of genotype-specific and common (DAS) genes.
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