Background Mitochondria play a diversity of physiological and metabolic roles under conditions of abiotic or biotic stress. They may be directly subjected to physico-chemical constraints, and they are also involved in integrative responses to environmental stresses through their central position in cell nutrition, respiration, energy balance and biosyntheses. In plant cells, mitochondria present various biochemical peculiarities, such as cyanide-insensitive alternative respiration, and, besides integration with ubiquitous eukaryotic compartments, their functioning must be coupled with plastid functioning. Moreover, given the sessile lifestyle of plants, their relative lack of protective barriers and present threats of climate change, the plant cell is an attractive model to understand the mechanisms of stress/organelle/cell integration in the context of environmental stress responses. Scope The involvement of mitochondria in this integration entails a complex network of signalling, which has not been fully elucidated, because of the great diversity of mitochondrial constituents (metabolites, reactive molecular species and structural and regulatory biomolecules) that are linked to stress signalling pathways. The present review analyses the complexity of stress signalling connexions that are related to the mitochondrial electron transport chain and oxidative phosphorylation system, and how they can be involved in stress perception and transduction, signal amplification or cell stress response modulation. Conclusions Plant mitochondria are endowed with a diversity of multi-directional hubs of stress signalling that lead to regulatory loops and regulatory rheostats, whose functioning can amplify and diversify some signals or, conversely, dampen and reduce other signals. Involvement in a wide range of abiotic and biotic responses also implies that mitochondrial stress signalling could result in synergistic or conflicting outcomes during acclimation to multiple and complex stresses, such as those arising from climate change.
During leaf senescence, nitrogen is remobilized and carbon backbones are replenished by amino acid catabolism, with many of the key reactions occurring in mitochondria. The intermediate Δ1‐pyrroline‐5‐carboxylate (P5C) is common to some catabolic pathways, thus linking the metabolism of several amino acids, including proline and arginine. Specifically, mitochondrial proline catabolism involves sequential action of proline dehydrogenase (ProDH) and P5C dehydrogenase (P5CDH) to produce P5C and then glutamate. Arginine catabolism produces urea and ornithine, the latter in the presence of α‐ketoglutarate being converted by ornithine δ‐aminotransferase (OAT) into P5C and glutamate. Metabolic changes during dark‐induced leaf senescence (DIS) were studied in Arabidopsis thaliana leaves of Col‐0 and in prodh1prodh2, p5cdh and oat mutants. Progression of DIS was followed by measuring chlorophyll and proline contents for 5 days. Metabolomic profiling of 116 compounds revealed similar profiles of Col‐0 and oat metabolism, distinct from prodh1prodh2 and p5cdh metabolism. Metabolic dynamics were accelerated in p5cdh by 1 day. Notably, more P5C and proline accumulated in p5cdh than in prodh1prodh2. ProDH1 enzymatic activity and protein amount were significantly down‐regulated in p5cdh mutant at Day 4 of DIS. Mitochondrial P5C levels appeared critical in determining the flow through interconnected amino acid remobilization pathways to sustain senescence.
Proline is an amino acid which is degraded in the mitochondrion by the sequential action of Proline Dehydrogenase (ProDH) and Pyrroline-5-Carboxylate Dehydrogenase (P5CDH) to form glutamate. We investigated the phenotypes of Arabidopsis wildtype plants, knockout prodh1prodh2 double mutant and knockout p5cdh allelic mutants grown at low and high nitrate supplies. Surprisingly, only p5cdh presented lower seed yield and produced lighter seeds. Elementary analyses in above ground organs revealed lower C concentrations in the p5cdh seeds. The computing of C, N, and dry matter partitioning between the above ground organs revealed a major defect in stem to seed resource allocations in p5cdh. Surprisingly defects in C, N and biomass allocation to seeds dramatically increased in high N conditions. 15N-labbeling consistently confirmed the defect of N remobilization from rosette and stem to seeds in p5cdh. Consequently, p5cdh mutants produced morphologically abnormal C-depleted seeds that displayed very low germination rates. The most striking result is the strong amplification of the N remobilization defects in p5cdh by high nitrate supply. Interestingly, such phenotype was not observed in prodh1prodh2 mutant irrespective of nitrate supply. This study reveals an essential role of p5cdh in carbon and nitrogen remobilization for reserve accumulation during seed development in Arabidopsis.
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