Being unable to move, plants are regularly exposed to changing environmental conditions, among which various types of abiotic stress, such as heat, drought, salt, and so forth. These might have ...deleterious effects on plant performance and yield. Plants thus need to adapt using appropriate stress responses. One of the outcomes of abiotic stress is the need to degrade and recycle damaged proteins and organelles. Autophagy is a conserved eukaryotic mechanism functioning in the degradation of proteins, protein aggregates, and whole organelles. It was previously shown to have a role in plant abiotic stress. This review will describe the current knowledge regarding the involvement of autophagy in plant abiotic stress response, mechanisms functioning in autophagy induction during stress, and possible direction for future research.
Plants are regularly exposed to changing environmental conditions, among which various types of abiotic stress, damaging plant performance and yield. One of the outcomes of abiotic stress is the need to degrade and recycle damaged proteins and organelles. Autophagy is a conserved eukaryotic mechanism functioning in the degradation of proteins, protein aggregates, and whole organelles. The review describes the current knowledge regarding the involvement of autophagy in plant abiotic stress response, mechanisms functioning in autophagy induction during stress, and possible directions for future research.
Autophagy is a eukaryotic cellular transport mechanism that delivers intracellular macromolecules, proteins, and even organelles to a lytic organelle (vacuole in yeast and plants/lysosome in animals) ...for degradation and nutrient recycling. The process is mediated by highly conserved autophagy‐related (ATG) proteins. In plants, autophagy maintains cellular homeostasis under favorable conditions, guaranteeing normal plant growth and fitness. Severe stress such as nutrient starvation and plant senescence further induce it, thus ensuring plant survival under unfavorable conditions by providing nutrients through the removal of damaged or aged proteins, or organelles. In this article, we examine the interplay between metabolism and autophagy, focusing on the different aspects of this reciprocal relationship. We show that autophagy has a strong influence on a range of metabolic processes, whereas at the same time, even single metabolites can activate autophagy. We highlight the involvement of ATG genes in metabolism, examine the role of the macronutrients carbon and nitrogen, and various micronutrients, and take a closer look at how the interaction between autophagy and metabolism impacts on plant phenotypes and yield.
Autophagy is a degradation mechanism functioning in plant metabolism to sustain plant growth and development. Shortage of nutrients represents a stress that activates autophagy, which in turn balances nutrient homeostasis. We present a detailed overview of this reciprocal relationship using different nutrients as examples and highlight the implications of autophagy activity on plant fitness and yield during metabolic stress.
Autophagy is a major cellular degradation pathway in eukaryotes. Recent studies have revealed the importance of autophagy in many aspects of plant life, including seedling establishment, plant ...development, stress resistance, metabolism, and reproduction. This is manifested by the dual ability of autophagy to execute bulk degradation under severe environmental conditions, while simultaneously to be highly selective in targeting specific compartments and protein complexes to regulate key cellular processes, even during favorable growth conditions. Delivery of cellular components to the vacuole enables their recycling, affecting the plant metabolome, especially under stress. Recent research in Arabidopsis has further unveiled fundamental mechanistic aspects in autophagy which may have relevance in non-plant systems. We review the most recent discoveries concerning autophagy in plants, touching upon all these aspects.
Autophagy is involved in almost every aspect of plant life, including germination, seedling establishment, development, reproduction, metabolism, and stress tolerance.
Proteins that are involved in fundamental processes of autophagy, such as autophagosome biogenesis, were recently characterized in plants.
Autophagy is intimately associated with other intracellular trafficking pathways.
Several selective autophagy pathways were recently identified in Arabidopsis; most are common to all eukaryotes. Nevertheless, some pathways were initially discovered in plants and others are plant-specific.
As an intracellular recycling system, autophagy is highly important for proper plant metabolism and nutrient allocation, both during stress and favorable growth conditions.
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.
Plants are constantly exposed to environmental changes that affect their performance. Metabolic adjustments are crucial to controlling energy homoeostasis and plant survival, particularly during ...stress. Under carbon starvation, coordinated reprogramming is initiated to adjust metabolic processes, which culminate in premature senescence. Notwithstanding, the regulatory networks that modulate transcriptional control during low energy remain poorly understood. Here, we show that the WRKY45 transcription factor is highly induced during both developmental and dark‐induced senescence. The overexpression of Arabidopsis WRKY45 resulted in an early senescence phenotype characterized by a reduction of maximum photochemical efficiency of photosystem II and chlorophyll levels in the later stages of darkness. The detailed metabolic characterization showed significant changes in amino acids coupled with the accumulation of organic acids in WRKY45 overexpression lines during dark‐induced senescence. Furthermore, the markedly upregulation of alternative oxidase (AOX1a, AOX1d) and electron transfer flavoprotein/ubiquinone oxidoreductase (ETFQO) genes suggested that WRKY45 is associated with a dysregulation of mitochondrial signalling and the activation of alternative respiration rather than amino acids catabolism regulation. Collectively our results provided evidence that WRKY45 is involved in the plant metabolic reprogramming following carbon starvation and highlight the potential role of WRKY45 in the modulation of mitochondrial signalling pathways.
The WRKY45 transcription factor mediates metabolic reprogramming during carbon starvation. The overexpression of WRKY45 triggered a differential accumulation of amino acids, organic acids and respiratory adjustments through the regulation of mitochondrial signalling and alternative respiration.
Germination and early seedling establishment are developmental stages in which plants face limited nutrient supply as their photosynthesis mechanism is not yet active. For this reason, the plant must ...mobilize the nutrient reserves provided by the mother plant in order to facilitate growth. Autophagy is a catabolic process enabling the bulk degradation of cellular constituents in the vacuole. The autophagy mechanism is conserved among eukaryotes, and homologs of many autophagy-related (ATG) genes have been found in Arabidopsis thaliana. T-DNA insertion mutants (atg mutants) of these genes display higher sensitivity to various stresses, particularly nutrient starvation. However, the direct impact of autophagy on cellular metabolism has not been well studied. In this work, we used etiolated Arabidopsis seedlings as a model system for carbon starvation. atg mutant seedlings display delayed growth in response to carbon starvation compared with wild-type seedlings. High-throughput metabolomic, lipidomic, and proteomic analyses were performed, as well as extensive flux analyses, in order to decipher the underlying causes of the phenotype. Significant differences between atg mutants and wild-type plants have been demonstrated, suggesting global effects of autophagy on central metabolism during carbon starvation as well as severe energy deprivation, resulting in a morphological phenotype.
Seeds are the major organs responsible for the evolutionary upkeep of angiosperm plants. Seeds accumulate significant amounts of storage compounds used as nutrients and energy reserves during the ...initial stages of seed germination. The accumulation of storage compounds requires significant amounts of energy, the generation of which can be limited due to reduced penetration of oxygen and light particularly into the inner parts of seeds. In this review, we discuss the adjustment of seed metabolism to limited energy production resulting from the suboptimal penetration of oxygen into the seed tissues. We also discuss the role of photosynthesis during seed development and its contribution to the energy status of developing seeds. Finally, we describe the contribution of amino acid metabolism to the seed energy status, focusing on the Asp-family pathway that leads to the synthesis and catabolism of Lys, Thr, Met, and Ile.
SUMMARY
The importance of the alternative donation of electrons to the ubiquinol pool via the electron‐transfer flavoprotein/electron‐transfer flavoprotein:ubiquinone oxidoreductase (ETF/ETFQO) ...complex has been demonstrated. However, the functional significance of this pathway during seed development and germination remains to be elucidated. To assess the function of this pathway, we performed a detailed metabolic and transcriptomic analysis of Arabidopsis mutants to test the molecular consequences of a dysfunctional ETF/ETFQO pathway. We demonstrate that the disruption of this pathway compromises seed germination in the absence of an external carbon source and also impacts seed size and yield. Total protein and storage protein content is reduced in dry seeds, whilst sucrose levels remain invariant. Seeds of ETFQO and related mutants were also characterized by an altered fatty acid composition. During seed development, lower levels of fatty acids and proteins accumulated in the etfqo‐1 mutant as well as in mutants in the alternative electron donors isovaleryl‐CoA dehydrogenase (ivdh‐1) and d‐2‐hydroxyglutarate dehydrogenase (d2hgdh1‐2). Furthermore, the content of several amino acids was increased in etfqo‐1 mutants during seed development, indicating that these mutants are not using such amino acids as alternative energy source for respiration. Transcriptome analysis revealed alterations in the expression levels of several genes involved in energy and hormonal metabolism. Our findings demonstrated that the alternative pathway of respiration mediated by the ETF/ETFQO complex affects seed germination and development by directly adjusting carbon storage during seed filling. These results indicate a role for the pathway in the normal plant life cycle to complement its previously defined roles in the response to abiotic stress.
Significance Statement
The importance of the alternative donation of electrons to the ubiquinol pool via the electron‐transfer flavoprotein/electron‐transfer flavoprotein:ubiquinone oxidoreductase (ETF/ETFQO) complex during normal seed development and germination is presented. Our results provide compelling evidence for a pivotal role of the alternative ETF/ETFQO respiration pathway in the normal life cycle of a plant in addition to its previously defined roles in response the to abiotic stress.
Atg8 is a central protein in bulk starvation-induced autophagy, but it is also specifically associated with multiple protein targets under various physiological conditions to regulate their selective ...turnover by the autophagy machinery. Here, we describe two new closely related Arabidopsis thaliana Atge-interacting proteins (ATI1 and ATI2) that are unique to plants. We show that under favorable growth conditions, ATI1 and ATI2 are partially associated with the endoplasmic reticulum (ER) membrane network, whereas upon exposure to carbon starvation, they become mainly associated with newly identified spherical compartments that dynamically move along the ER network. These compartments are morphologically distinct from previously reported spindle-shaped ER bodies and, in contrast to them, do not contain ER-lumenal markers possessing a C-terminal HDEL sequence. Organelle and autophagosome-specific markers show that the bodies containing ATM are distinct from Golgi, mitochondria, peroxisomes, and classical autophagosomes. The final destination of the ATI1 bodies is the central vacuole, indicating that they may operate in selective turnover of specific proteins. ATI1 and ATI2 gene expression is elevated during late seed maturation and desiccation. We further demonstrate that ATI1 overexpression or suppression of both ATM and ATI2, respectively, stimulate or inhibit seed germination in the presence of the germinationinhibiting hormone abscisic acid.
Summary
Plants need to continuously adjust their transcriptome in response to various stresses that lead to inhibition of photosynthesis and the deprivation of cellular energy. This adjustment is ...triggered in part by a coordinated re‐programming of the energy‐associated transcriptome to slow down photosynthesis and activate other energy‐promoting gene networks. Therefore, understanding the stress‐related transcriptional networks of genes belonging to energy‐associated pathways is of major importance for engineering stress tolerance. In a bioinformatics approach developed by our group, termed ‘gene coordination’, we previously divided genes encoding for enzymes and transcription factors in Arabidopsis thaliana into three clusters, displaying altered coordinated transcriptional behaviors in response to multiple biotic and abiotic stresses (Plant Cell, 23, 2011, 1264). Enrichment analysis indicated further that genes controlling energy‐associated metabolism operate as a compound network in response to stress. In the present paper, we describe in detail the network association of genes belonging to six central energy‐associated pathways in each of these three clusters described in our previous paper. Our results expose extensive stress‐associated intra‐ and inter‐pathway interactions between genes from these pathways, indicating that genes encoding proteins involved in energy‐associated metabolism are expressed in a highly coordinated manner. We also provide examples showing that this approach can be further utilized to elucidate candidate genes for stress tolerance and functions of isozymes.
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