The interplay between autophagy and chloroplast vesiculation pathways under dark‐induced senescence

• Published in: Plant, cell and environment Vol. 46; no. 12; pp. 3721 - 3736
• Main Authors: Barros, Jessica A. S., Cavalcanti, João Henrique F., Pimentel, Karla G., Magen, Sahar, Soroka, Yoram, Weiss, Shahar, Medeiros, David B., Nunes‐Nesi, Adriano, Fernie, Alisdair R., Avin‐Wittenberg, Tamar, Araújo, Wagner L.
• Format: Journal Article
• Language: English
• Published: Oxford Wiley Subscription Services, Inc 01-12-2023
• Subjects: Amino acids; Autophagy; Carbohydrates; Chloroplasts; Darkness; Degradation; Membrane structures; Metabolism; Mutants; Organic acids; Phenotypes; Proteins; Senescence; Substrates
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.14701

Abstract
In cellular circumstances where carbohydrates are scarce, plants can use alternative substrates for cellular energetic maintenance. In plants, the main protein reserve is present in the chloroplast, which contains most of the total leaf proteins and represents a rich source of nitrogen and amino acids. Autophagy plays a key role in chloroplast breakdown, a well‐recognised symptom of both natural and stress‐induced plant senescence. Remarkably, an autophagic‐independent route of chloroplast degradation associated with chloroplast vesiculation (CV) gene was previously demonstrated. During extended darkness, CV is highly induced in the absence of autophagy, contributing to the early senescence phenotype of
atg
mutants. To further investigate the role of CV under dark‐induced senescence conditions, mutants with low expression of CV (
amircv
) and double mutants
amircv1xatg5
were characterised. Following darkness treatment, no aberrant phenotypes were observed in
amircv
single mutants; however,
amircv1xatg5
double mutants displayed early senescence and altered dismantling of chloroplast and membrane structures under these conditions. Metabolic characterisation revealed that the functional lack of both CV and autophagy leads to higher impairment of amino acid release and differential organic acid accumulation during starvation conditions. The data obtained are discussed in the context of the role of CV and autophagy, both in terms of cellular metabolism and the regulation of chloroplast degradation.
Summary statement
Functional lack of both chloroplast vesiculation (CV) and autophagy leads to higher impairment of amino acid release and differential organic acid accumulation during extended darkness conditions. CV deficiency triggers minor energetic consequences when autophagy is still present and activated.