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Curr Biol. 2019 Nov 18;29(22):3778-3790.e8. doi: 10.1016/j.cub.2019.09.018. Epub 2019 Oct 31.

The Receptor Kinases BAK1/SERK4 Regulate Ca2+ Channel-Mediated Cellular Homeostasis for Cell Death Containment.

Author information

1
Institute for Plant Genomics & Biotechnology, Texas A&M University, College Station, TX 77843, USA; Department of Plant Pathology & Microbiology, Texas A&M University, College Station, TX 77843, USA.
2
Institute for Plant Genomics & Biotechnology, Texas A&M University, College Station, TX 77843, USA; Department of Biochemistry & Biophysics, Texas A&M University, College Station, TX 77843, USA; College of Plant Protection, China Agricultural University, Beijing 100193, P.R. China.
3
Institute for Plant Genomics & Biotechnology, Texas A&M University, College Station, TX 77843, USA; Department of Plant Pathology & Microbiology, Texas A&M University, College Station, TX 77843, USA; Provincial Key Laboratory of Plant Pathology of Hubei Province, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, P.R. China.
4
College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, P. R. China.
5
Department of Cell and Systems Biology, Center for the Analysis of Genome Evolution and Function (CAGEF), University of Toronto, Toronto, ON M5S 3B2, Canada.
6
Department of Biology, Genetics Institute, Plant Molecular and Cellular Biology Program, University of Florida, Gainesville, FL 32610, USA.
7
Institute for Plant Genomics & Biotechnology, Texas A&M University, College Station, TX 77843, USA; Department of Biochemistry & Biophysics, Texas A&M University, College Station, TX 77843, USA.
8
Department of Plant Science and Landscape Architecture, University of Connecticut, Storrs, CT 06269, USA.
9
Institute for Plant Genomics & Biotechnology, Texas A&M University, College Station, TX 77843, USA; Department of Biochemistry & Biophysics, Texas A&M University, College Station, TX 77843, USA; College of Plant Protection, China Agricultural University, Beijing 100193, P.R. China. Electronic address: pinghe@tamu.edu.
10
Institute for Plant Genomics & Biotechnology, Texas A&M University, College Station, TX 77843, USA; Department of Plant Pathology & Microbiology, Texas A&M University, College Station, TX 77843, USA; College of Plant Protection, China Agricultural University, Beijing 100193, P.R. China. Electronic address: lshan@tamu.edu.

Abstract

Cell death is a vital and ubiquitous process that is tightly controlled in all organisms. However, the mechanisms underlying precise cell death control remain fragmented. As an important shared module in plant growth, development, and immunity, Arabidopsis thaliana BRASSINOSTEROID INSENSITIVE 1-associated receptor kinase 1 (BAK1) and somatic embryogenesis receptor kinase 4 (SERK4) redundantly and negatively regulate plant cell death. By deploying an RNAi-based genetic screen for bak1/serk4 cell death suppressors, we revealed that cyclic nucleotide-gated channel 20 (CNGC20) functions as a hyperpolarization-activated Ca2+-permeable channel specifically regulating bak1/serk4 cell death. BAK1 directly interacts with and phosphorylates CNGC20 at specific sites in the C-terminal cytosolic domain, which in turn regulates CNGC20 stability. CNGC19, the closest homolog of CNGC20 with a low abundance compared with CNGC20, makes a quantitative genetic contribution to bak1/serk4 cell death only in the absence of CNGC20, supporting the biochemical data showing homo- and heteromeric assembly of the CNGC20 and CNGC19 channel complexes. Transcripts of CNGC20 and CNGC19 are elevated in bak1/serk4 compared with wild-type plants, further substantiating a critical role of homeostasis of CNGC20 and CNGC19 in cell death control. Our studies not only uncover a unique regulation of ion channel stability by cell-surface-resident receptor kinase-mediated phosphorylation but also provide evidence for fine-tuning Ca2+ channel functions in maintaining cellular homeostasis by the formation of homo- and heterotetrameric complexes.

KEYWORDS:

Ca(2+)-permeable channel; cellular homeostasis; cyclic nucleotide-gated channel; phosphorylation; plant cell death; receptor kinase; virus-induced gene silencing

PMID:
31679931
DOI:
10.1016/j.cub.2019.09.018

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