Abstract
Climate change has increased the frequency and severity of flooding events, with significant negative impact on agricultural productivity. These events often submerge plant aerial organs and roots, limiting growth and survival due to a severe reduction in light reactions and gas exchange necessary for photosynthesis and respiration, respectively. To distinguish molecular responses to the compound stress imposed by submergence, we investigated transcriptomic adjustments to darkness in air and under submerged conditions using eight Arabidopsis (Arabidopsis thaliana) accessions differing significantly in sensitivity to submergence. Evaluation of root and rosette transcriptomes revealed an early transcriptional and posttranscriptional response signature that was conserved primarily across genotypes, although flooding susceptibility-associated and genotype-specific responses also were uncovered. Posttranscriptional regulation encompassed darkness- and submergence-induced alternative splicing of transcripts from pathways involved in the alternative mobilization of energy reserves. The organ-specific transcriptome adjustments reflected the distinct physiological status of roots and shoots. Root-specific transcriptome changes included marked up-regulation of chloroplast-encoded photosynthesis and redox-related genes, whereas those of the rosette were related to the regulation of development and growth processes. We identified a novel set of tolerance genes, recognized mainly by quantitative differences. These included a transcriptome signature of more pronounced gluconeogenesis in tolerant accessions, a response that included stress-induced alternative splicing. This study provides organ-specific molecular resolution of genetic variation in submergence responses involving interactions between darkness and low-oxygen constraints of flooding stress and demonstrates that early transcriptome plasticity, including alternative splicing, is associated with the ability to cope with a compound environmental stress.
Highlights
Climate change has increased the frequency and severity of flooding events, with significant negative impact on agricultural productivity
The decline in oxygen levels caused by submergence had stabilized in both the root and petiole, as shown by oxygen microelectrode measurements in submerged Arabidopsis (Col-0) plants (Lee et al, 2011)
Multidimensional scaling (MDS) of the samples demonstrated a strong difference between root and shoot transcriptomes (Fig. 1B)
Summary
Climate change has increased the frequency and severity of flooding events, with significant negative impact on agricultural productivity. This study provides organ-specific molecular resolution of genetic variation in submergence responses involving interactions between darkness and low-oxygen constraints of flooding stress and demonstrates that early transcriptome plasticity, including alternative splicing, is associated with the ability to cope with a compound environmental stress. Our understanding of the flooding-induced lowoxygen and low-energy signaling networks has benefited greatly from studies on flood-sensitive Arabidopsis (Arabidopsis thaliana) These investigations have identified the main players in energy and carbon signaling (Smeekens et al, 2010; Ljung et al, 2015) and revealed whole-plant and cell type-specific transcriptional and translational adjustments induced by lowoxygen stress (Mustroph et al, 2009; Juntawong et al, 2014). Recent studies have revealed how this molecular hypoxic response is highly regulated and fine-tuned to maintain cellular homeostasis during low-oxygen conditions (Gibbs et al, 2014; Giuntoli et al, 2014; Gonzali et al, 2015)
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