Revolutionizing tomato fruit development: Unveiling the role of autophagy in metabolism and growth
image: ATG4 RNAi plants display induce senescence and reduce fruit yield in comparison to wild-type plants.
Credit: Horticulture Research
Autophagy, a eukaryotic mechanism for breaking down cellular components, is a vital process in lytic organelles such as vacuoles in yeast and plants, and lysosomes in animals. Research has predominantly focused on the model plant Arabidopsis, revealing the conservation of autophagy-related genes across various plant species. Recent studies highlight autophagy's crucial role in plant responses to nutrient scarcity, stress management, and pathogen interactions, and its influence on plant yield and metabolism. However, while autophagy's impact on lipid,primary and secondary metabolism in crops like rice and Arabidopsis is documented, its role in tomato cellular metabolism remains underexplored.
In June 2022, Horticulture Research published a research article entitled by “Autophagy modulates the metabolism and growth of tomato fruit during development”.
In this study, researchers employed RNA interference (RNAi) to specifically target and reduce the expression of the autophagy-regulating protease ATG4 gene. This approach led to the generation of tomato plants with distinct early senescence phenotypes and reduced fruit yields(Fig.1). To analyze the effects of ATG4 downregulation, researchers conducted a series of experiments encompassing metabolite profiling, transcriptome analysis, and proteomics. In ATG4-RNAi tomato leaves, only observed minor alterations in the levels of certain primary and secondary metabolites, such as citric acid, glycerate, and quercetin derivatives. However, in the fruit, more pronounced changes were evident. Primary metabolites like proline, tryptophan, and phenylalanine showed decreased levels in ATG4-RNAi lines, while secondary metabolites such as quinic acid and 3-trans-caffeoylquinic acid were substantially increased in ATG4-RNAi green fruits compared to wild type (WT).
Transcriptome analysis revealed significant upregulation of genes involved in organelle degradation and chloroplast vesiculation pathways in ATG4-RNAi lines. This was further corroborated by proteomics data, which indicated reduced levels of chloroplastic proteins. These findings suggest that ATG4 plays a critical role in regulating chloroplast function and metabolism in tomato fruit. Additionally, lipid profiling demonstrated significant changes in lipid compounds in ATG4-RNAi lines, particularly at the green fruit stage. A correlation network analysis of omics data pointed to strong associations between lipids, genes, and proteins involved in lipid metabolism, chlorophyll binding, and chloroplast biosynthesis. Finally, metabolic flux analysis using 14C- or 13C glucose in red ripe fruits showed decreasing rate of protein synthesis alongside the 14CO2 evolution on lack of autophagy in Arabidopsis. However, there are few significant changes in the redistribution of metabolites, indicating that the absence of autophagy primarily affected specific metabolic pathways rather than causing widespread metabolic disruption.
In conclusion, this study reveals a key role for ATG4-dependent autophagy in tomato physiology. This is the first report linking autophagy to metabolic content in tomato pericarp, differing from previous studies focusing on foliar metabolism in Arabidopsis and maize. This research provides a more comprehensive understanding of autophagy in tomato, and highlights the potential of targeting autophagy for future crop improvement and breeding strategies.
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References
Authors
Saleh Alseekh1,2,†, Feng Zhu1,3,†, José G. Vallarino1, Ewelina M. Sokolowska1, Takuya Yoshida1, Susan Bergmann1, Regina Wendenburg1, Antje Bolze1, Aleksandra Skirycz1,4, Tamar Avin-Wittenberg1,5,* and Alisdair R. Fernie1,2,*
†Contributed equally to the research described.
Affiliations
1Max-Planck-Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany
2Center of Plant Systems Biology and Biotechnology, 4000 Plovdiv, Bulgaria
3National R&D Center for Citrus Preservation, Key Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, 430070 Wuhan, China
4Boyce Thompson Institute, 14850, Ithaca, US
5Current Address: Department of Plant and Environmental Sciences, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Givat Ram, Jerusalem, 9190401.
About Tamar Avin-Wittenberg & Alisdair R. Fernie
Tamar Avin-Wittenberg: She is an associate professor in the Department of Plant and Environmental Sciences at the Alexander Silberman Institute of Life Sciences at The Hebrew University of Jerusalem. The Avin-Wittenberg lab focuses on understanding how plants break down cellular components to obtain nutrients for energy during stress and development. By using molecular and metabolic techniques, they aim to unravel the mechanisms behind this process.
Alisdair R. Fernie: He is Group Leader (group Central Metabolism) at the Max Planck Institute of Molecular Plant Physiology (MPG), Potsdam-Golm, Germany. Early work of Prof. Fernie focused on the metabolic regulation of photosynthetic and heterotrophic carbon metabolism. Prof. Fernie has developed extensive expertise in metabolomics and flux profiling as well as studying the genetic control of metabolism with a particular focus on crop species. His studies now embrace both primary and intermediary metabolism.