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.

Departamento de Biologia Molecular y Bioquimica Facultad de Ciencias Universidad de Malaga Campus de Teatinos Malaga Spain

Department of Molecular Sciences Uppsala BioCenter Swedish University of Agricultural Sciences and Linnean Center for Plant Biology Uppsala Sweden

Department of Plant Biology Uppsala BioCenter Swedish University of Agricultural Sciences and Linnean Center for Plant Biology Uppsala Sweden

Department of Plant Biology Uppsala BioCenter Swedish University of Agricultural Sciences and Linnean Center for Plant Biology Uppsala Sweden Department of Plant Protection Biology Swedish University of Agricultural Sciences Alnarp Sweden

Department of Plant Breeding Swedish University of Agricultural Sciences Alnarp Sweden

Laboratory of Growth Regulators Centre of the Region Haná for Biotechnological and Agricultural Research Institute of Experimental Botany Academy of Sciences of the Czech Republic Olomouc Czech Republic Faculty of Science Palacký University Olomouc Czech Republic

ScanBiRes AB Alnarp Sweden

School of Land and Food University of Tasmania Private Bag Hobart TAS Australia

Umeå Plant Science Centre Department of Forest Genetics and Plant Physiology Swedish University of Agricultural Sciences Umea Sweden

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$a Minina, Elena A $u Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, Uppsala, Sweden.

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$a Transcriptional stimulation of rate-limiting components of the autophagic pathway improves plant fitness / $c EA. Minina, PN. Moschou, RR. Vetukuri, V. Sanchez-Vera, C. Cardoso, Q. Liu, PH. Elander, K. Dalman, M. Beganovic, J. Lindberg Yilmaz, S. Marmon, L. Shabala, MF. Suarez, K. Ljung, O. Novák, S. Shabala, S. Stymne, D. Hofius, PV. Bozhkov,

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$a 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.

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$a Moschou, Panagiotis N $u Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, Uppsala, Sweden.

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$a Vetukuri, Ramesh R $u Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, Uppsala, Sweden. Department of Plant Protection Biology, Swedish University of Agricultural Sciences, Alnarp, Sweden.

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$a Sanchez-Vera, Victoria $u Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, Uppsala, Sweden.

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$a Cardoso, Catarina $u Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, Uppsala, Sweden.

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$a Liu, Qinsong $u Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, Uppsala, Sweden.

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$a Elander, Pernilla H $u Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, Uppsala, Sweden.

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$a Dalman, Kerstin $u Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, Uppsala, Sweden.

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$a Beganovic, Mirela $u Department of Plant Breeding, Swedish University of Agricultural Sciences, Alnarp, Sweden.

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$a Shabala, Lana $u School of Land and Food, University of Tasmania, Private Bag, Hobart, TAS, Australia.

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$a Suarez, Maria F $u Departamento de Biologia Molecular y Bioquimica, Facultad de Ciencias, Universidad de Malaga, Campus de Teatinos, Malaga, Spain.

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$a Ljung, Karin $u Umeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umea, Sweden.

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$a Novák, Ondrej $u Laboratory of Growth Regulators, Centre of the Region Haná for Biotechnological and Agricultural Research, Institute of Experimental Botany Academy of Sciences of the Czech Republic (AS CR), Olomouc, Czech Republic. Faculty of Science, Palacký University, Olomouc, Czech Republic.

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$a Shabala, Sergey $u School of Land and Food, University of Tasmania, Private Bag, Hobart, TAS, Australia.

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$a Stymne, Sten $u Department of Plant Breeding, Swedish University of Agricultural Sciences, Alnarp, Sweden.

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$a Hofius, Daniel $u Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, Uppsala, Sweden.

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$a Bozhkov, Peter V $u Department of Molecular Sciences, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, Uppsala, Sweden.

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