PMID- 36852939
OWN - NLM
STAT- MEDLINE
DCOM- 20231019
LR  - 20240229
IS  - 1532-2548 (Electronic)
IS  - 0032-0889 (Print)
IS  - 0032-0889 (Linking)
VI  - 192
IP  - 2
DP  - 2023 May 31
TI  - Autophagy and multivesicular body pathways cooperate to protect sulfur 
      assimilation and chloroplast functions.
PG  - 886-909
LID - 10.1093/plphys/kiad133 [doi]
AB  - Autophagy and multivesicular bodies (MVBs) represent 2 closely related 
      lysosomal/vacuolar degradation pathways. In Arabidopsis (Arabidopsis thaliana), 
      autophagy is stress-induced, with deficiency in autophagy causing strong defects 
      in stress responses but limited effects on growth. LYST-INTERACTING PROTEIN 5 
      (LIP5) is a key regulator of stress-induced MVB biogenesis, and mutation of LIP5 
      also strongly compromises stress responses with little effect on growth in 
      Arabidopsis. To determine the functional interactions of these 2 pathways in 
      Arabidopsis, we generated mutations in both the LIP5 and AUTOPHAGY-RELATED 
      PROTEIN (ATG) genes. atg5/lip5 and atg7/lip5 double mutants displayed strong 
      synergistic phenotypes in fitness characterized by stunted growth, early 
      senescence, reduced survival, and greatly diminished seed production under normal 
      growth conditions. Transcriptome and metabolite analysis revealed that 
      chloroplast sulfate assimilation was specifically downregulated at early seedling 
      stages in the atg7/lip5 double mutant prior to the onset of visible phenotypes. 
      Overexpression of adenosine 5'-phosphosulfate reductase 1, a key enzyme in 
      sulfate assimilation, substantially improved the growth and fitness of the 
      atg7/lip5 double mutant. Comparative multi-omic analysis further revealed that 
      the atg7/lip5 double mutant was strongly compromised in other chloroplast 
      functions including photosynthesis and primary carbon metabolism. Premature 
      senescence and reduced survival of atg/lip5 double mutants were associated with 
      increased accumulation of reactive oxygen species and overactivation of 
      stress-associated programs. Blocking PHYTOALEXIN DEFICIENT 4 and salicylic acid 
      signaling prevented early senescence and death of the atg7/lip5 double mutant. 
      Thus, stress-responsive autophagy and MVB pathways play an important cooperative 
      role in protecting essential chloroplast functions including sulfur assimilation 
      under normal growth conditions to suppress salicylic-acid-dependent premature 
      cell-death and promote plant growth and fitness.
CI  - (c) American Society of Plant Biologists 2023. All rights reserved. For 
      permissions, please e-mail: journals.permissions@oup.com.
FAU - Fu, Yunting
AU  - Fu Y
AD  - College of Life Sciences, China Jiliang University, Hangzhou 310018, China.
FAU - Fan, Baofang
AU  - Fan B
AD  - Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 
      47907-2054, USA.
FAU - Li, Xifeng
AU  - Li X
AD  - College of Life Sciences, China Jiliang University, Hangzhou 310018, China.
FAU - Bao, Hexigeduleng
AU  - Bao H
AD  - College of Life Sciences, China Jiliang University, Hangzhou 310018, China.
AD  - Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 
      47907-2054, USA.
FAU - Zhu, Cheng
AU  - Zhu C
AD  - College of Life Sciences, China Jiliang University, Hangzhou 310018, China.
FAU - Chen, Zhixiang
AU  - Chen Z
AUID- ORCID: 0000-0002-5472-4560
AD  - College of Life Sciences, China Jiliang University, Hangzhou 310018, China.
AD  - Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 
      47907-2054, USA.
LA  - eng
PT  - Journal Article
PT  - Research Support, Non-U.S. Gov't
PT  - Research Support, U.S. Gov't, Non-P.H.S.
PL  - United States
TA  - Plant Physiol
JT  - Plant physiology
JID - 0401224
RN  - 0 (Arabidopsis Proteins)
RN  - 0 (Sulfates)
SB  - IM
MH  - *Arabidopsis/metabolism
MH  - *Arabidopsis Proteins/genetics/metabolism
MH  - Autophagy/genetics
MH  - *Chloroplasts/metabolism
MH  - Multivesicular Bodies/metabolism
MH  - Mutation/genetics
MH  - *Sulfates/metabolism
PMC - PMC10231471
COIS- Conflict of interest statement. None declared.
EDAT- 2023/03/01 06:00
MHDA- 2023/06/02 06:42
PMCR- 2024/02/28
CRDT- 2023/02/28 08:13
PHST- 2022/10/20 00:00 [received]
PHST- 2023/02/02 00:00 [accepted]
PHST- 2023/06/02 06:42 [medline]
PHST- 2023/03/01 06:00 [pubmed]
PHST- 2023/02/28 08:13 [entrez]
PHST- 2024/02/28 00:00 [pmc-release]
AID - 7059663 [pii]
AID - kiad133 [pii]
AID - 10.1093/plphys/kiad133 [doi]
PST - ppublish
SO  - Plant Physiol. 2023 May 31;192(2):886-909. doi: 10.1093/plphys/kiad133.