TY - JOUR
T1 - Transcriptional stimulation of rate-limiting components of the autophagic pathway improves plant fitness
AU - Minina, Elena A.
AU - Moschou, Panagiotis N.
AU - Vetukuri, Ramesh R.
AU - Sanchez-Vera, Victoria
AU - Cardoso, Catarina
AU - Liu, Qinsong
AU - Elander, Pernilla H.
AU - Dalman, Kerstin
AU - Beganovic, Mirela
AU - Lindberg Yilmaz, Jenny
AU - Marmon, Sofia
AU - Shabala, Lana
AU - Suarez, Maria F.
AU - Ljung, Karin
AU - Novák, Ondřej
AU - Shabala, Sergey
AU - Stymne, Sten
AU - Hofius, Daniel
AU - Bozhkov, Peter V.
N1 - Funding Information:
This work was supported by grants from the Knut and Alice Wallenberg Foundation (to DH and PVB, 19679-006), the Swedish Research Council (to PVB, 20419-000), Pehrssons Fond (to PVB, 16406-000), the Swedish Foundation for Strategic Research (to StSt and PVB, 21236-000), Olle Engkvist Foundation (to PVB, 18510-000), Carl Tryggers Foundation (to EAM, 21196-000) and Trees and Crops for the Future Research Programme (to PVB). We would like to express our sincere gratitude to T. Johansen, Y. Ohsumi, and R. Vierstra for kindly providing us with the antibodies required for this study.
Publisher Copyright:
© The Author(s) 2018.
PY - 2018/3/14
Y1 - 2018/3/14
N2 - 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 Atg8PE 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.
AB - 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 Atg8PE 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.
KW - Aging
KW - ATG genes
KW - Autophagy
KW - Autophagy-related ubiquitin-like conjugation systems
KW - Biomass
KW - Oil content
KW - Ratelimiting components of autophagic flux
KW - Seed yield
KW - Stress resistance
KW - Transcriptional regulation
UR - http://www.scopus.com/inward/record.url?scp=85044200714&partnerID=8YFLogxK
U2 - 10.1093/jxb/ery010
DO - 10.1093/jxb/ery010
M3 - Article
C2 - 29365132
AN - SCOPUS:85044200714
SN - 0022-0957
VL - 69
SP - 1415
EP - 1432
JO - Journal of Experimental Botany
JF - Journal of Experimental Botany
IS - 6
ER -