Autophagy regulates programmed cell death during the plant innate immune response.
The plant innate immune response includes the hypersensitive response (HR), a form of programmed cell death (PCD). PCD must be restricted to infection sites to prevent the HR from playing a pathologic rather than protective role. Here we show that plant BECLIN 1, an ortholog of the yeast and mammalian autophagy gene ATG6/VPS30/beclin 1, functions to restrict HR PCD to infection sites. Initiation of HR PCD is normal in BECLIN 1-deficient plants, but remarkably, healthy uninfected tissue adjacent to HR lesions and leaves distal to the inoculated leaf undergo unrestricted PCD. In the HR PCD response, autophagy is induced in both pathogen-infected cells and distal uninfected cells; this is reduced in BECLIN 1-deficient plants. The restriction of HR PCD also requires orthologs of other autophagy-related genes including PI3K/VPS34, ATG3, and ATG7. Thus, the evolutionarily conserved autophagy pathway plays an essential role in plant innate immunity and negatively regulates PCD.
Liu
Yule
Y
Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Connecticut 06520.
Schiff
Michael
M
Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Connecticut 06520.
Czymmek
Kirk
K
Department of Biological Sciences, Delaware Biotechnology Institute, University of Delaware, Newark, Delaware 19711.
Tallóczy
Zsolt
Z
Department of Medicine, Columbia University College of Physicians and Surgeons, New York, New York 10032.
Levine
Beth
B
Department of Medicine, Columbia University College of Physicians and Surgeons, New York, New York 10032; Department of Medicine, University of Texas Southwestern Medical Center, Dallas, Texas 75390.
Dinesh-Kumar
S P
SP
Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Connecticut 06520. Electronic address: savithramma.dinesh-kumar@yale.edu.
D000595:Amino Acid Sequence; D017209:Apoptosis / Q000502:physiology*; D051017:Apoptosis Regulatory Proteins; D001343:Autophagy / Q000502:physiology*; D000071193:Autophagy-Related Protein 7; D001483:Base Sequence; D000071186:Beclin-1; D018506:Gene Expression Regulation, Plant / Q000235:genetics; D007113:Immunity, Innate / Q000235:genetics / Q000502:physiology*; D008565:Membrane Proteins; D046529:Microscopy, Electron, Transmission; D008969:Molecular Sequence Data; D015388:Organelles / Q000378:metabolism / Q000648:ultrastructure; D019869:Phosphatidylinositol 3-Kinases / Q000235:genetics / Q000378:metabolism; D010940:Plant Proteins / Q000235:genetics / Q000302:isolation & purification / Q000378:metabolism*; D011506:Proteins / Q000235:genetics; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics / Q000378:metabolism; D014026:Nicotiana / Q000235:genetics / Q000378:metabolism* / Q000648:ultrastructure; D014027:Tobacco Mosaic Virus / Q000378:metabolism; D025521:Tumor Suppressor Proteins / Q000235:genetics / Q000302:isolation & purification / Q000378:metabolism*; D033921:Vesicular Transport Proteins
C114830:ATG7 protein, S cerevisiae; D051017:Apoptosis Regulatory Proteins; C491997:BECN1 protein, human; D000071186:Beclin-1; D008565:Membrane Proteins; D010940:Plant Proteins; D011506:Proteins; D029701:Saccharomyces cerevisiae Proteins; D025521:Tumor Suppressor Proteins; C402377:VPS30 protein, S cerevisiae; D033921:Vesicular Transport Proteins; D019869:Phosphatidylinositol 3-Kinases; D000071193:Autophagy-Related Protein 7