• This record comes from PubMed

Transcriptional stimulation of rate-limiting components of the autophagic pathway improves plant fitness

. 2018 Mar 14 ; 69 (6) : 1415-1432.

Language English Country Great Britain, England Media print

Document type Journal Article, Research Support, Non-U.S. Gov't

Autophagy is a major catabolic process whereby autophagosomes deliver cytoplasmic content to the lytic compartment for recycling. Autophagosome formation requires two ubiquitin-like systems conjugating Atg12 with Atg5, and Atg8 with lipid phosphatidylethanolamine (PE), respectively. Genetic suppression of these systems causes autophagy-deficient phenotypes with reduced fitness and longevity. We show that Atg5 and the E1-like enzyme, Atg7, are rate-limiting components of Atg8-PE conjugation in Arabidopsis. Overexpression of ATG5 or ATG7 stimulates Atg8 lipidation, autophagosome formation, and autophagic flux. It also induces transcriptional changes opposite to those observed in atg5 and atg7 mutants, favoring stress resistance and growth. As a result, ATG5- or ATG7-overexpressing plants exhibit increased resistance to necrotrophic pathogens and oxidative stress, delayed aging and enhanced growth, seed set, and seed oil content. This work provides an experimental paradigm and mechanistic insight into genetic stimulation of autophagy in planta and shows its efficiency for improving plant productivity.

See more in PubMed

AbuQamar S, Chen X, Dhawan R, Bluhm B, Salmeron J, Lam S, Dietrich RA, Mengiste T. 2006. Expression profiling and mutant analysis reveals complex regulatory networks involved in Arabidopsis response to Botrytis infection. The Plant Journal 48, 28–44. PubMed

Avin-Wittenberg T, Bajdzienko K, Wittenberg G, Alseekh S, Tohge T, Bock R, Giavalisco P, Fernie AR. 2015. Global analysis of the role of autophagy in cellular metabolism and energy homeostasis in Arabidopsis seedlings under carbon starvation. The Plant Cell 27, 306–322. PubMed PMC

Bassham DC. 2015. Methods for analysis of autophagy in plants. Methods 75, 181–188. PubMed

Bassham DC, Laporte M, Marty F, Moriyasu Y, Ohsumi Y, Olsen LJ, Yoshimoto K. 2006. Autophagy in development and stress responses of plants. Autophagy 2, 2–11. PubMed

Bates PD, Stymne S, Ohlrogge J. 2013. Biochemical pathways in seed oil synthesis. Current Opinion in Plant Biology 16, 358–364. PubMed

Brown JK. 2002. Yield penalties of disease resistance in crops. Current Opinion in Plant Biology 5, 339–344. PubMed

Cabello JV, Lodeyro AF, Zurbriggen MD. 2014. Novel perspectives for the engineering of abiotic stress tolerance in plants. Current Opinion in Biotechnology 26, 62–70. PubMed

Chen Y, Klionsky DJ. 2011. The regulation of autophagy—unanswered questions. Journal of Cell Science 124, 161–170. PubMed PMC

Choquer M, Fournier E, Kunz C, Levis C, Pradier JM, Simon A, Viaud M. 2007. Botrytis cinerea virulence factors: new insights into a necrotrophic and polyphageous pathogen. FEMS Microbiology Letters 277, 1–10. PubMed

Chung T, Phillips AR, Vierstra RD. 2010. ATG8 lipidation and ATG8-mediated autophagy in Arabidopsis require ATG12 expressed from the differentially controlled ATG12A and ATG12B loci. The Plant Journal 62, 483–493. PubMed

Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735–743. PubMed

Dall’Armi C, Devereaux KA, Di Paolo G. 2013. The role of lipids in the control of autophagy. Current Biology 23, R33–R45. PubMed PMC

Doelling JH, Walker JM, Friedman EM, Thompson AR, Vierstra RD. 2002. The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. Journal of Biological Chemistry 277, 33105–33114. PubMed

Elander PH, Minina EA, Bozkov PV. 2018. Autophagy in turnover of lipid stores: trans-kingdom comparison. Journal of Experimental Botany 69, doi:10.1093/jxb/erx433. PubMed

Feng Y, Yao Z, Klionsky DJ. 2015. How to control self-digestion: transcriptional, post-transcriptional, and post-translational regulation of autophagy. Trends in Cell Biology 25, 354–363. PubMed PMC

Fleming A, Noda T, Yoshimori T, Rubinsztein DC. 2011. Chemical modulators of autophagy as biological probes and potential therapeutics. Nature Chemical Biology 7, 9–17. PubMed

Frankel LB, Lund AH. 2012. MicroRNA regulation of autophagy. Carcinogenesis 33, 2018–2025. PubMed

Füllgrabe J, Ghislat G, Cho DH, Rubinsztein DC. 2016. Transcriptional regulation of mammalian autophagy at a glance. Journal of Cell Science 129, 3059–3066. PubMed

Guiboileau A, Avila-Ospina L, Yoshimoto K, Soulay F, Azzopardi M, Marmagne A, Lothier J, Masclaux-Daubresse C. 2013. Physiological and metabolic consequences of autophagy deficiency for the management of nitrogen and protein resources in Arabidopsis leaves depending on nitrate availability. New Phytologist 199, 683–694. PubMed

Guiboileau A, Yoshimoto K, Soulay F, Bataillé MP, Avice JC, Masclaux-Daubresse C. 2012. Autophagy machinery controls nitrogen remobilization at the whole-plant level under both limiting and ample nitrate conditions in Arabidopsis. New Phytologist 194, 732–740. PubMed

Han S, Wang Y, Zheng X, Jia Q, Zhao J, Bai F, Hong Y, Liu Y. 2015. Cytoplastic glyceraldehyde-3-phosphate dehydrogenases interact with ATG3 to negatively regulate autophagy and immunity in Nicotiana benthamiana. The Plant Cell 27, 1316–1331. PubMed PMC

Hanaoka H, Noda T, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Ohsumi Y. 2002. Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiology 129, 1181–1193. PubMed PMC

Hofius D, Schultz-Larsen T, Joensen J et al. . 2009. Autophagic components contribute to hypersensitive cell death in Arabidopsis. Cell 137, 773–783. PubMed

Hothorn T, Bretz F, Westfall P. 2008. Simultaneous inference in general parametric models. Biometrical Journal J 50, 346–363. PubMed

Inskeep WP, Bloom PR. 1985. Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80% acetone. Plant Physiology 77, 483–485. PubMed PMC

Ishida H, Yoshimoto K, Izumi M, Reisen D, Yano Y, Makino A, Ohsumi Y, Hanson MR, Mae T. 2008. Mobilization of rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiology 148, 142–155. PubMed PMC

Kabbage M, Williams B, Dickman MB. 2013. Cell death control: the interplay of apoptosis and autophagy in the pathogenicity of Sclerotinia sclerotiorum. PLoS Pathogens 9, e1003287. PubMed PMC

Klionsky DJ, Abdelmohsen K, Abe A et al. . 2016. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 12, 1–222. PubMed PMC

Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685. PubMed

Lai Z, Wang F, Zheng Z, Fan B, Chen Z. 2011. A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. The Plant Journal 66, 953–968. PubMed

Lapierre LR, Kumsta C, Sandri M, Ballabio A, Hansen M. 2015. Transcriptional and epigenetic regulation of autophagy in aging. Autophagy 11, 867–880. PubMed PMC

Lee JM, Wagner M, Xiao R, Kim KH, Feng D, Lazar MA, Moore DD. 2014. Nutrient-sensing nuclear receptors coordinate autophagy. Nature 516, 112–115. PubMed PMC

Lenz HD, Haller E, Melzer E et al. . 2011. Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens. The Plant Journal 66, 818–830. PubMed

Levine B, Mizushima N, Virgin HW. 2011. Autophagy in immunity and inflammation. Nature 469, 323–335. PubMed PMC

Li F, Chung T, Pennington JG, Federico ML, Kaeppler HF, Kaeppler SM, Otegui MS, Vierstra RD. 2015. Autophagic recycling plays a central role in maize nitrogen remobilization. The Plant Cell 27, 1389–1408. PubMed PMC

Liu K, Czaja MJ. 2013. Regulation of lipid stores and metabolism by lipophagy. Cell Death and Differentiation 20, 3–11. PubMed PMC

Liu Y, Bassham DC. 2012. Autophagy: pathways for self-eating in plant cells. Annual Review of Plant Biology 63, 215–237. PubMed

Ma J, Jin R, Dobry CJ, Lawson SK, Kumar A. 2007. Overexpression of autophagy-related genes inhibits yeast filamentous growth. Autophagy 3, 604–609. PubMed

Masclaux-Daubresse C, Clément G, Anne P, Routaboul JM, Guiboileau A, Soulay F, Shirasu K, Yoshimoto K. 2014. Stitching together the multiple dimensions of autophagy using metabolomics and transcriptomics reveals impacts on metabolism, development, and plant responses to the environment in Arabidopsis. The Plant Cell 26, 1857–1877. PubMed PMC

Mathew R, White E. 2011. Autophagy in tumorigenesis and energy metabolism: friend by day, foe by night. Current Opinion in Genetics and Development 21, 113–119. PubMed PMC

Minina EA, Bozhkov PV, Hofius D. 2014. Autophagy as initiator or executioner of cell death. Trends in Plant Science 19, 692–697. PubMed

Minina EA, Filonova LH, Fukada K et al. . 2013. a Autophagy and metacaspase determine the mode of cell death in plants. Journal of Cell Biology 203, 917–927. PubMed PMC

Minina EA, Sanchez-Vera V, Moschou PN, Suarez MF, Sundberg E, Weih M, Bozhkov PV. 2013b Autophagy mediates caloric restriction-induced lifespan extension in Arabidopsis. Aging Cell 12, 327–329. PubMed

Mizushima N, Komatsu M. 2011. Autophagy: renovation of cells and tissues. Cell 147, 728–741. PubMed

Nair U, Thumm M, Klionsky DJ, Krick R. 2011. GFP–Atg8 protease protection as a tool to monitor autophagosome biogenesis. Autophagy 7, 1546–1550. PubMed PMC

Nakagawa T, Kurose T, Hino T et al. . 2007. Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. Journal of Bioscience and Bioengineering 104, 34–41. PubMed

Nakatogawa H. 2013. Two ubiquitin-like conjugation systems that mediate membrane formation during autophagy. Essays in Biochemistry 55, 39–50. PubMed

Parzych KR, Klionsky DJ. 2014. An overview of autophagy: morphology, mechanism, and regulation. Antioxidants and Redox Signaling 20, 460–473. PubMed PMC

Patel S, Dinesh-Kumar SP. 2008. Arabidopsis ATG6 is required to limit the pathogen-associated cell death response. Autophagy 4, 20–27. PubMed

Pyo JO, Yoo SM, Ahn HH, Nah J, Hong SH, Kam TI, Jung S, Jung YK. 2013. Overexpression of Atg5 in mice activates autophagy and extends lifespan. Nature Communications 4, 2300. PubMed PMC

Rabinowitz JD, White E. 2010. Autophagy and metabolism. Science 330, 1344–1348. PubMed PMC

Ren C, Liu J, Gong Q. 2014. Functions of autophagy in plant carbon and nitrogen metabolism. Frontiers in Plant Science 5, 301. PubMed PMC

Rubinsztein DC, Mariño G, Kroemer G. 2011. Autophagy and aging. Cell 146, 682–695. PubMed

Scott RC, Juhász G, Neufeld TP. 2007. Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Current Biology 17, 1–11. PubMed PMC

Seok S, Fu T, Choi SE et al. . 2014. Transcriptional regulation of autophagy by an FXR–CREB axis. Nature 516, 108–111. PubMed PMC

Shibata M, Oikawa K, Yoshimoto K et al. . 2013. Highly oxidized peroxisomes are selectively degraded via autophagy in Arabidopsis. The Plant Cell 25, 4967–4983. PubMed PMC

Shibutani ST, Yoshimori T. 2014. A current perspective of autophagosome biogenesis. Cell Research 24, 58–68. PubMed PMC

Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM, Czaja MJ. 2009. Autophagy regulates lipid metabolism. Nature 458, 1131–1135. PubMed PMC

Slavikova S, Ufaz S, Avin-Wittenberg T, Levanony H, Galili G. 2008. An autophagy-associated Atg8 protein is involved in the responses of Arabidopsis seedlings to hormonal controls and abiotic stresses. Journal of Experimental Botany 59, 4029–4043. PubMed PMC

Sun X, Wang P, Jia X, Huo L, Che R, Ma F. 2017. Improvement of drought tolerance by overexpressing MdATG18a is mediated by modified antioxidant system and activated autophagy in transgenic apple. Plant Biotechnology Journal. doi: 10.1111/pbi.12794 PubMed PMC

Sun X, Jia X, Huo L, Che R, Gong X, Wang P, Ma F. 2018. MdATG18a overexpression improves tolerance to nitrogen deficiency and regulates anthocyanin accumulation through increased autophagy in transgenic apple. Plant, Cell and Environment 41: 469–480. PubMed

Svenning S, Lamark T, Krause K, Johansen T. 2011. Plant NBR1 is a selective autophagy substrate and a functional hybrid of the mammalian autophagic adapters NBR1 and p62/SQSTM1. Autophagy 7, 993–1010. PubMed PMC

Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue BPA, Broekaert WF. 1998. Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proceedings of the National Academy of Sciences, USA 95, 15107–15111. PubMed PMC

Thompson AR, Doelling JH, Suttangkakul A, Vierstra RD. 2005. Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiology 138, 2097–2110. PubMed PMC

Wada S, Hayashida Y, Izumi M et al. . 2015. Autophagy supports biomass production and nitrogen use efficiency at the vegetative stage in rice. Plant Physiology 168, 60–73. PubMed PMC

Wada S, Ishida H, Izumi M, Yoshimoto K, Ohsumi Y, Mae T, Makino A. 2009. Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiology 149, 885–893. PubMed PMC

Wang P, Sun X, Jia X, Ma F. 2017. Apple autophagy-related protein MdATG3s afford tolerance to multiple abiotic stresses. Plant Science 256, 53–64. PubMed

Wang P, Sun X, Wang N, Jia X, Ma F. 2016. Ectopic expression of an autophagy-associated MdATG7b gene from apple alters growth and tolerance to nutrient stress in Arabidopsis thaliana. Plant Cell, Tissue and Organ Culture 1–15.

Wang Y, Yu B, Zhao J et al. . 2013. Autophagy contributes to leaf starch degradation. The Plant Cell 25, 1383–1399. PubMed PMC

Wingenter K, Schulz A, Wormit A et al. . 2010. Increased activity of the vacuolar monosaccharide transporter TMT1 alters cellular sugar partitioning, sugar signaling, and seed yield in Arabidopsis. Plant Physiology 154, 665–677. PubMed PMC

Wuyts N, Palauqui JC, Conejero G, Verdeil JL, Granier C, Massonnet C. 2010. High-contrast three-dimensional imaging of the Arabidopsis leaf enables the analysis of cell dimensions in the epidermis and mesophyll. Plant Methods 6, 17. PubMed PMC

Xia T, Xiao D, Liu D, Chai W, Gong Q, Wang NN. 2012. Heterologous expression of ATG8c from soybean confers tolerance to nitrogen deficiency and increases yield in Arabidopsis. PLoS One 7, e37217. PubMed PMC

Xie Q, Michaeli S, Peled-Zehavi H, Galili G. 2015. Chloroplast degradation: one organelle, multiple degradation pathways. Trends in Plant Science 20, 264–265. PubMed

Xiong Y, Contento AL, Nguyen PQ, Bassham DC. 2007. Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiology 143, 291–299. PubMed PMC

Yang Z, Klionsky DJ. 2010. Eaten alive: a history of macroautophagy. Nature Cell Biology 12, 814–822. PubMed PMC

Yoshimoto K, Hanaoka H, Sato S, Kato T, Tabata S, Noda T, Ohsumi Y. 2004. Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. The Plant Cell 16, 2967–2983. PubMed PMC

Yoshimoto K, Jikumaru Y, Kamiya Y, Kusano M, Consonni C, Panstruga R, Ohsumi Y, Shirasu K. 2009. Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. The Plant Cell 21, 2914–2927. PubMed PMC

Zhang Y, Goldman S, Baerga R, Zhao Y, Komatsu M, Jin SK. 2009. Adipose-specific deletion of autophagy-related gene 7 (atg7) in mice reveals a role in adipogenesis. Proceedings of the National Academy of Sciences, USA 106, 19860–19865. PubMed PMC

Zhou J, Wang J, Cheng Y, Chi YJ, Fan B, Yu JQ, Chen Z. 2013. NBR1-mediated selective autophagy targets insoluble ubiquitinated protein aggregates in plant stress responses. PLoS Genetics 9, e1003196. PubMed PMC

Zhou J, Yu JQ, Chen Z. 2014. The perplexing role of autophagy in plant innate immune responses. Molecular Plant Pathology 15, 637–645. PubMed PMC

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...