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. 2023 May 8:14:1182461.
doi: 10.3389/fpls.2023.1182461. eCollection 2023.

Drought-triggered leaf transcriptional responses disclose key molecular pathways underlying leaf water use efficiency in sugarcane (Saccharum spp.)

Affiliations

Drought-triggered leaf transcriptional responses disclose key molecular pathways underlying leaf water use efficiency in sugarcane (Saccharum spp.)

Danyel F Contiliani et al. Front Plant Sci. .

Abstract

Drought is a major constraint to sugarcane (Saccharum spp.) production and improving the water use efficiency (WUE) is a critical trait for the sustainability of this bioenergy crop. The molecular mechanism underlying WUE remains underexplored in sugarcane. Here, we investigated the drought-triggered physiological and transcriptional responses of two sugarcane cultivars contrasting for drought tolerance, 'IACSP97-7065' (sensitive) and 'IACSP94-2094' (tolerant). After 21 days without irrigation (DWI), only 'IACSP94-2094' exhibited superior WUE and instantaneous carboxylation efficiency, with the net CO2 assimilation being less impacted when compared with 'IACSP97-7065'. RNA-seq of sugarcane leaves at 21 DWI revealed a total of 1,585 differentially expressed genes (DEGs) for both genotypes, among which 'IACSP94-2094' showed 617 (38.9%) exclusive transcripts (212 up- and 405 down-regulated). Functional enrichment analyses of these unique DEGs revealed several relevant biological processes, such as photosynthesis, transcription factors, signal transduction, solute transport, and redox homeostasis. The better drought-responsiveness of 'IACSP94-2094' suggested signaling cascades that foster transcriptional regulation of genes implicated in the Calvin cycle and transport of water and carbon dioxide, which are expected to support the high WUE and carboxylation efficiency observed for this genotype under water deficit. Moreover, the robust antioxidant system of the drought-tolerant genotype might serve as a molecular shield against the drought-associated overproduction of reactive oxygen species. This study provides relevant data that may be used to develop novel strategies for sugarcane breeding programs and to understand the genetic basis of drought tolerance and WUE improvement of sugarcane.

Keywords: abiotic stress; antioxidant mechanism; carboxylation efficiency; transcriptome; water use efficiency.

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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
Physiological changes in drought-stressed sugarcane genotypes. Drought-sensitive (‘IACSP97-7065’) and -tolerant (‘IACSP94-2094’) sugarcane genotypes were physiologically evaluated at 21 days without water (21 DWI) and rehydration (recovery) for irrigated (control) and drought groups. The physiological parameters examined were: (A) CO2 assimilation (PN), (B) transpiration (E), (C) water use efficiency (WUE, PN/E), (D) instantaneous carboxylation efficiency (CEi), (E) stomatal conductance (gs), (F) non-photochemical quenching (NPQ), (G) maximum (Fv/Fm) and (H) effective (ΦPSII) quantum efficiency of photosystem II. Data represent the means ± SE (n = 3 biological replicates) and statistical differences are represented as *P<0.05, **P<0.01, and ***P<0.001.
Figure 2
Figure 2
RNA-Seq results and RT-qPCR validation. (A) the Venn diagram represents the distribution of exclusive and shared up- and down-regulated DEGs between sugarcane genotypes. (B) Overall annotation of leaf sugarcane DEGs against monocots protein databases. (C) Validation of the expression profiles of 15 selected genes from ‘IACSP97-7065’ (red) and ‘IACSP94-2094’ (blue) at 21 DWI, in which relative expression levels (drought vs. irrigated) are represented as log2Fold-change. Error bars represent standard deviations.
Figure 3
Figure 3
Gene ontology (GO) functional classification of sugarcane DEGs. GO terms are divided into ‘molecular function’ and ‘biological process’ categories, which are represented by up- (right) and down-regulated (left) genes from ‘IACSP97-7065’ (red) and ‘IACSP94-2094’ (blue) sugarcane genotypes.
Figure 4
Figure 4
Enriched KEGG pathway categories. KOBAS analysis of sugarcane DEGs enriched the responsive biological pathways for drought-stressed (A) ‘IACSP97-7065’ and (B) ‘IACSP94-2094’ genotypes. Gene counts for each pathway are represented by the X-axis. The significantly enriched pathways represent their corrected p-values according to the color spectrum (from red to blue).
Figure 5
Figure 5
Mapman annotation of gene expression profiles. Functional classes (indicated in bold within boxes) comprise transcriptional profiles of ‘IACSP97-7065’ (left) and ‘IACSP94-2094’ (right) sugarcane genotypes. Each mapped gene is displayed in square within heatmaps, and the color scale indicates its relative expression (log2Fold-change). Up-regulated DEGs are represented in red, whereas down-regulated ones are represented in green.
Figure 6
Figure 6
Expression-based heatmaps of drought-responsive sugarcane genes. Transcriptional profiles of sugarcane genotypes are represented in four functional categories: transcription factor, photosynthesis, redox homeostasis, and solute transport. Color scale indicates relative gene expression (log2Fold-change), ranging from down- (green) to up-regulated (red). Non-significant gene expression is colored in white.

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