Mitochondrial signalling is critical for acclimation and adaptation to flooding in Arabidopsis thaliana

Abstract

SUMMARYMitochondria have critical functions in the acclimation to abiotic and biotic stresses. Adverse environmental conditions lead to increased demands in energy supply and metabolic intermediates, which are provided by mitochondrial ATP production and the tricarboxylic acid (TCA) cycle. Mitochondria also play a role as stress sensors to adjust nuclear gene expression via retrograde signalling with the transcription factor (TF) ANAC017 and the kinase CDKE1 key components to integrate various signals into this pathway. To determine the importance of mitochondria as sensors of stress and their contribution in the tolerance to adverse growth conditions, a comparative phenotypical, physiological and transcriptomic characterisation of Arabidopsis mitochondrial signalling mutants (cdke1/rao1 and anac017/rao2) and a set of contrasting accessions was performed after applying the complex compound stress of submergence. Our results showed that impaired mitochondrial retrograde signalling leads to increased sensitivity to the stress treatments. The multi‐factorial approach identified a network of 702 co‐expressed genes, including several WRKY TFs, overlapping in the transcriptional responses in the mitochondrial signalling mutants and stress‐sensitive accessions. Functional characterisation of two WRKY TFs (WRKY40 and WRKY45), using both knockout and overexpressing lines, confirmed their role in conferring tolerance to submergence. Together, the results revealed that acclimation to submergence is dependent on mitochondrial retrograde signalling, and underlying transcriptional re‐programming is used as an adaptation mechanism.

Differential submergence tolerance between juvenile and adult Arabidopsis plants involves the ANAC017 transcription factor

“…When challenged with submergence, a homozygous knockout ANAC017 mutant ( anac017‐1 ) exhibited significantly lower survival at the juvenile stage, as compared with wild‐type plants of the same age (Figure 7b), providing evidence for the involvement of this transcription factor in flooding tolerance. Similar observations were made for ANAC017 mutants at the adult stage (Meng et al ., 2020). Although a contribution by ANAC017 homologues to plant performance under submergence cannot be ruled out, the extent of reduction in flooding tolerance we observed in anac017 supports the hypothesis of a major role of this transcription tolerance in the response of juvenile Arabidopsis plants during the stress.…”

“…We showed that this tolerance mechanism is independent of the core‐anaerobic response (Figure 3), and rather relies on NAC transcription factors that mediate retrograde stress signalling (Figures 7b and 8). It should be observed that, in this context, ANAC017 anyway contributes positively to plant responses to submergence also at later vegetative stages (Meng et al ., 2020). The differential response between developmental stages seems to originate from the chromatin status of the loci targeted by ANAC017, rather than from its direct regulation by the stress.…”

Differential Expression of Maize and Teosinte microRNAs under Submergence, Drought, and Alternated Stress

“…Mitochondria and chloroplasts are the main compartments for energy production that are affected by low water and oxygen availability and may be a source of signals to integrate the cellular response [ 37 , 38 ]. A search was performed in the libraries with the objective of identifying small RNAs potentially originating from maize mitochondria or plastids.…”

Retrograde signals from endosymbiotic organelles: a common control principle in eukaryotic cells

“…This suggests that response to low oxygen, for instance during flooding or germination, may depend at least in part on mitochondrial plasticity controlled by ANAC017 [161,162]. Very recently, the protective role of ANAC017 in flooding tolerance was experimentally confirmed [163]. Conversely, ANAC017 may have a growth-limiting effect when expressed or active at high levels [164].…”