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Specific control of Arabidopsis BAK1/SERK4-regulated cell death by protein glycosylation

Nature Plants volume 2, Article number: 15218 (2016) Cite this article

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Abstract

Precise control of cell death is essential for the survival of all organisms. Arabidopsis thaliana BRASSINOSTEROID INSENSITIVE 1-associated receptor kinase 1 (BAK1) and somatic embryogenesis receptor kinase 4 (SERK4) redundantly and negatively regulate cell death through elusive mechanisms. By deploying a genetic screen for suppressors of cell death triggered by virus-induced gene silencing of BAK1/SERK4 on Arabidopsis knockout collections, we identified STT3a, a protein involved in N-glycosylation modification, as an important regulator of bak1/serk4 cell death. Systematic investigation of glycosylation pathway and endoplasmic reticulum (ER) quality control (ERQC) components revealed distinct and overlapping mechanisms of cell death regulated by BAK1/SERK4 and their interacting protein BIR1. Genome-wide transcriptional analysis revealed the activation of members of cysteine-rich receptor-like kinase (CRK) genes in the bak1/serk4 mutant. Ectopic expression of CRK4 induced STT3a/N-glycosylation-dependent cell death in Arabidopsis and Nicotiana benthamiana. Therefore, N-glycosylation and specific ERQC components are essential to activate bak1/serk4 cell death, and CRK4 is likely to be among client proteins of protein glycosylation involved in BAK1/SERK4-regulated cell death.

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Figure 1: The sobir1 mutant did not suppress bak1/serk4 cell death.
Figure 2: The stt3a mutants suppress BAK1/SERK4-regulated cell death.
Figure 3: Control of BAK1/SERK4-regulated cell death by protein N-glycosylation and specific components of ERQC.
Figure 4: Uncoupled BAK1 functions in cell death control, immunity and brassinosteroid signalling.
Figure 5: Members of CRK genes are upregulated in the bak1/serk4 mutant.
Figure 6: CRK4-induced cell death requires STT3a-mediated N-glycosylation.

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Acknowledgements

We thank S. H. Howell and the Arabidopsis Biological Resource Center for various Arabidopsis mutant seeds and transgenic plants, and members of the laboratories of L.S. and P.H. for discussions and comments about the experiments. The work was supported by grants from the National Institutes of Health (NIH) (R01GM092893) and the National Science Foundation (NSF) (IOS-1252539) to P.H., the NIH (R01GM097247) and the Robert A. Welch Foundation (A-1795) to L.S. and the NSF (IOS-1547551) to H.K. The Next-Generation Sequencing (NGS) was supported by a Texas AgriLife Genomics[JS(S6] Seed Grant. G.X. was partially supported by the China Scholarship Council (CSC). L.S.V. and S.A.S. were partially supported by the CAPES Foundation (Coordination for the Improvement of Higher Education Personnel), Brazil. A.C.I. was partially supported by the Rio de Janeiro State Research Foundation (FAPERJ), Brazil. A.B. was an undergraduate student supported by a NSF Research Experiences for Undergraduates (REU) programme.

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  1. Marcos V. V. de Oliveira, Guangyuan Xu and Bo Li: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Biochemistry & Biophysics, Institute for Plant Genomics & Biotechnology, Texas A&M University, College Station, 77843, Texas, USA

    Marcos V. V. de Oliveira, Guangyuan Xu, Xiangzong Meng & Ping He

  2. Department of Plant Pathology & Microbiology, Institute for Plant Genomics & Biotechnology, Texas A&M University, College Station, 77843, Texas, USA

    Marcos V. V. de Oliveira, Bo Li, Luciano de Souza Vespoli, Xin Chen, Xiao Yu, Suzane Ariádina de Souza, Aline C. Intorne, Ana Marcia E. de A. Manhães, Abbey L. Musinsky & Libo Shan

  3. Molecular and Environmental Plant Sciences, Texas A&M University, College Station, 77843, Texas, USA

    Guangyuan Xu, Hisashi Koiwa, Libo Shan & Ping He

  4. Center of Biosciences & Biotechnology, Darcy Ribeiro State University of North Rio de Janeiro, 28013-602, Brazil

    Luciano de Souza Vespoli, Suzane Ariádina de Souza, Aline C. Intorne, Ana Marcia E. de A. Manhães & Gonçalo A. de Souza Filho

  5. Medical Microbiology and Immunology Major, University of Wisconsin-Madison, Madison, 53706, Wisconsin, USA

    Abbey L. Musinsky

  6. Department of Horticultural Sciences, Texas A&M University, College Station, 77843, Texas, USA

    Hisashi Koiwa

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Contributions

M.V.V.O., G.X., B.L., L.S. and P.H. conceived and designed the experiments and wrote the manuscript with input from all co-authors. M.V.V.O., G.X., B.L., L.S.V., X.M., X.C., X.Y., S.A.S., A.C.I., A.M.M. and A.L.B performed the experiments; M.V.V.O., G.X., B.L., L.S.V., G.A.S.F., L.S. and P.H. analysed data; H.K. provided reagents.

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Correspondence to Libo Shan or Ping He.

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de Oliveira, M., Xu, G., Li, B. et al. Specific control of Arabidopsis BAK1/SERK4-regulated cell death by protein glycosylation. Nature Plants 2, 15218 (2016). https://doi.org/10.1038/nplants.2015.218

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