ARC3 Activation by PARC6 Promotes FtsZ-Ring Remodeling at the Chloroplast Division Site

Chen, Cheng; Cao, Lingyan; Yang, Yue; Porter, Katie J.; Osteryoung, Katherine W.

doi:10.1105/tpc.18.00948

Title: ARC3 Activation by PARC6 Promotes FtsZ-Ring Remodeling at the Chloroplast Division Site

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Abstract

Chloroplast division is initiated by assembly of the stromal Z ring, composed of cytoskeletal Filamenting temperature-sensitive Z (FtsZ) proteins. Midplastid Z-ring positioning is governed by the chloroplast Min (Minicell) system, which inhibits Z-ring assembly everywhere except the division site. The central Min-system player is the FtsZ-assembly inhibitor ACCUMULATION AND REPLICATION OF CHLOROPLASTS3 (ARC3). Here, we report Arabidopsis (Arabidopsis thaliana) chloroplasts contain two pools of ARC3: one distributed throughout the stroma, which presumably fully inhibits Z-ring assembly at nondivision sites, and the other localized to a midplastid ring-like structure. We show that ARC3 is recruited to the middle of the plastid by the inner envelope membrane protein PARALOG OF ARC6 (PARC6). ARC3 bears a C-terminal Membrane Occupation and Recognition Nexus (MORN) domain; previous yeast two-hybrid experiments with full-length and MORN-truncated ARC3 showed the MORN domain mediates ARC3-PARC6 interaction but prevents ARC3-FtsZ interaction. Using yeast three-hybrid experiments, we demonstrate that the MORN-dependent ARC3-PARC6 interaction enables full-length ARC3 to bind FtsZ. The resulting PARC6/ARC3/FtsZ complex enhances the dynamics of Z rings reconstituted in a heterologous system. In conclusion, our findings lead to a model whereby activation of midplastid-localized ARC3 by PARC6 facilitates Z-ring remodeling during chloroplast division by promoting Z-ring dynamics and revealmore »« less

Authors:

^[1];

^[1]

Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824

Publication Date:: Fri Mar 01 00:00:00 EST 2019

Research Org.:: Michigan State Univ., East Lansing, MI (United States)

Sponsoring Org.:: USDOE Office of Science (SC); National Science Foundation (NSF)

OSTI Identifier:: 1497732

Alternate Identifier(s):: OSTI ID: 1609711

Grant/Contract Number:: FG02-06ER15808; 1719376

Resource Type:: Published Article

Journal Name:: The Plant Cell

Additional Journal Information:: Journal Name: The Plant Cell Journal Volume: 31 Journal Issue: 4; Journal ID: ISSN 1040-4651

Publisher:: American Society of Plant Biologists

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; Biochemistry & Molecular Biology; Plant Sciences; Cell Biology

Citation Formats


                    Chen, Cheng, Cao, Lingyan, Yang, Yue, Porter, Katie J., and Osteryoung, Katherine W. ARC3 Activation by PARC6 Promotes FtsZ-Ring Remodeling at the Chloroplast Division Site.  United States: N. p., 2019. 
Web.  doi:10.1105/tpc.18.00948.

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                    Chen, Cheng, Cao, Lingyan, Yang, Yue, Porter, Katie J., & Osteryoung, Katherine W. ARC3 Activation by PARC6 Promotes FtsZ-Ring Remodeling at the Chloroplast Division Site.  United States.  https://doi.org/10.1105/tpc.18.00948

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                    Chen, Cheng, Cao, Lingyan, Yang, Yue, Porter, Katie J., and Osteryoung, Katherine W. Fri .  
"ARC3 Activation by PARC6 Promotes FtsZ-Ring Remodeling at the Chloroplast Division Site".  United States.  https://doi.org/10.1105/tpc.18.00948.

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@article{osti_1497732,

  title        = {ARC3 Activation by PARC6 Promotes FtsZ-Ring Remodeling at the Chloroplast Division Site},

  author       = {Chen, Cheng and Cao, Lingyan and Yang, Yue and Porter, Katie J. and Osteryoung, Katherine W.},

  abstractNote = {Chloroplast division is initiated by assembly of the stromal Z ring, composed of cytoskeletal Filamenting temperature-sensitive Z (FtsZ) proteins. Midplastid Z-ring positioning is governed by the chloroplast Min (Minicell) system, which inhibits Z-ring assembly everywhere except the division site. The central Min-system player is the FtsZ-assembly inhibitor ACCUMULATION AND REPLICATION OF CHLOROPLASTS3 (ARC3). Here, we report Arabidopsis (Arabidopsis thaliana) chloroplasts contain two pools of ARC3: one distributed throughout the stroma, which presumably fully inhibits Z-ring assembly at nondivision sites, and the other localized to a midplastid ring-like structure. We show that ARC3 is recruited to the middle of the plastid by the inner envelope membrane protein PARALOG OF ARC6 (PARC6). ARC3 bears a C-terminal Membrane Occupation and Recognition Nexus (MORN) domain; previous yeast two-hybrid experiments with full-length and MORN-truncated ARC3 showed the MORN domain mediates ARC3-PARC6 interaction but prevents ARC3-FtsZ interaction. Using yeast three-hybrid experiments, we demonstrate that the MORN-dependent ARC3-PARC6 interaction enables full-length ARC3 to bind FtsZ. The resulting PARC6/ARC3/FtsZ complex enhances the dynamics of Z rings reconstituted in a heterologous system. In conclusion, our findings lead to a model whereby activation of midplastid-localized ARC3 by PARC6 facilitates Z-ring remodeling during chloroplast division by promoting Z-ring dynamics and reveal a novel function for MORN domains in regulating protein–protein interactions.},

  doi          = {10.1105/tpc.18.00948},

  journal      = {The Plant Cell},

  number       = 4,

  volume       = 31,

  place        = {United States},

  year         = {Fri Mar 01 00:00:00 EST 2019},

  month        = {Fri Mar 01 00:00:00 EST 2019}

}

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