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

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.

References

  1. 1

    Shiu, S. H. & Bleecker, A. B. Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol. 132, 530–543 (2003).

    CAS  Article  Google Scholar 

  2. 2

    Belkhadir, Y., Yang, L., Hetzel, J., Dangl, J. L. & Chory, J. The growth-defense pivot: crisis management in plants mediated by LRR-RK surface receptors. Trends Biochem. Sci. 39, 447–456 (2014).

    CAS  Article  Google Scholar 

  3. 3

    Li, J. & Chory, J. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90, 929–938 (1997).

    CAS  Article  Google Scholar 

  4. 4

    Gomez-Gomez, L. & Boller, T. FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5, 1003–1011 (2000).

    CAS  Article  Google Scholar 

  5. 5

    Gou, X. et al. Genetic evidence for an indispensable role of somatic embryogenesis receptor kinases in brassinosteroid signaling. PLoS Genet. 8, e1002452 (2012).

    CAS  Article  Google Scholar 

  6. 6

    Aan den Toorn, M., Albrecht, C. & de Vries, S. On the origin of SERKs: bioinformatics analysis of the somatic embryogenesis receptor kinases. Mol. Plant 8, 762–782 (2015).

    CAS  Article  Google Scholar 

  7. 7

    Albrecht, C., Russinova, E., Hecht, V., Baaijens, E. & de Vries, S. The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES 1 and 2 control male sporogenesis. Plant Cell 17, 3337–3349 (2005).

    CAS  Article  Google Scholar 

  8. 8

    Colcombet, J., Boisson-Dernier, A., Ros-Palau, R., Vera, C. E. & Schroeder, J. I. Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES 1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17, 3350–3361 (2005).

    CAS  Article  Google Scholar 

  9. 9

    Chinchilla, D. et al. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497–U412 (2007).

    CAS  Article  Google Scholar 

  10. 10

    Heese, A. et al. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl Acad. Sci. USA 104, 12217–12222 (2007).

    CAS  Article  Google Scholar 

  11. 11

    Postel, S. et al. The multifunctional leucine-rich repeat receptor kinase BAK1 is implicated in Arabidopsis development and immunity. Eur. J. Cell Biol. 89, 169–174 (2010).

    CAS  Article  Google Scholar 

  12. 12

    Roux, M. et al. The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23, 2440–2455 (2011).

    CAS  Article  Google Scholar 

  13. 13

    Li, J. et al. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110, 213–222 (2002).

    CAS  Article  Google Scholar 

  14. 14

    Nam, K. H. & Li, J. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110, 203–212 (2002).

    CAS  Article  Google Scholar 

  15. 15

    Meng, X. et al. Differential function of Arabidopsis SERK family receptor-like kinases in stomatal patterning. Curr. Biol. 25, 2361–2372 (2015).

    CAS  Article  Google Scholar 

  16. 16

    Wang, J. et al. Allosteric receptor activation by the plant peptide hormone phytosulfokine. Nature 525, 265–268 (2015).

    CAS  Article  Google Scholar 

  17. 17

    Ladwig, F. et al. Phytosulfokine regulates growth in Arabidopsis through a response module at the plasma membrane that includes CYCLIC NUCLEOTIDE-GATED CHANNEL17, H+-ATPase, and BAK1. Plant Cell 27, 1718–1729 (2015).

    CAS  Article  Google Scholar 

  18. 18

    He, K. et al. BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Curr. Biol. 17, 1109–1115 (2007).

    CAS  Article  Google Scholar 

  19. 19

    Kemmerling, B. et al. The BRI1-associated kinase 1, BAK1, has a brassinolide-independent role in plant cell-death control. Curr. Biol. 17, 1116–1122 (2007).

    CAS  Article  Google Scholar 

  20. 20

    Gao, M. et al. Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe 6, 34–44 (2009).

    CAS  Article  Google Scholar 

  21. 21

    Burch-Smith, T. M., Schiff, M., Liu, Y. & Dinesh-Kumar, S. P. Efficient virus-induced gene silencing in Arabidopsis. Plant Physiol. 142, 21–27 (2006).

    CAS  Article  Google Scholar 

  22. 22

    Gao, M. H. et al. MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res. 18, 1190–1198 (2008).

    CAS  Article  Google Scholar 

  23. 23

    Zhang, Q., Sun, T. & Zhang, Y. ER quality control components UGGT and STT3a are required for activation of defense responses in Bir1-1. PLoS ONE 10, e0120245 (2015).

    Article  Google Scholar 

  24. 24

    Hua, J. Modulation of plant immunity by light, circadian rhythm, and temperature. Curr. Opin. Plant Biol. 16, 406–413 (2013).

    CAS  Article  Google Scholar 

  25. 25

    Koiwa, H. et al. The STT3a subunit isoform of the Arabidopsis oligosaccharyltransferase controls adaptive responses to salt/osmotic stress. Plant Cell 15, 2273–2284 (2003).

    CAS  Article  Google Scholar 

  26. 26

    Farid, A. et al. Specialized roles of the conserved subunit OST3/6 of the oligosaccharyltransferase complex in innate immunity and tolerance to abiotic stresses. Plant Physiol. 162, 24–38 (2013).

    CAS  Article  Google Scholar 

  27. 27

    Liu, Y. & Li, J. Endoplasmic reticulum-mediated protein quality control in Arabidopsis. Front. Plant Sci. 5, 162 (2014).

    PubMed  PubMed Central  Google Scholar 

  28. 28

    Pattison, R. J. & Amtmann, A. N-glycan production in the endoplasmic reticulum of plants. Trends Plant Sci. 14, 92–99 (2009).

    CAS  Article  Google Scholar 

  29. 29

    Farid, A. et al. Arabidopsis thaliana alpha1,2-glucosyltransferase (ALG10) is required for efficient N-glycosylation and leaf growth. Plant J. 68, 314–325 (2011).

    CAS  Article  Google Scholar 

  30. 30

    Hong, Z. et al. Evolutionarily conserved glycan signal to degrade aberrant brassinosteroid receptors in Arabidopsis. Proc. Natl Acad. Sci. USA 109, 11437–11442 (2012).

    CAS  Article  Google Scholar 

  31. 31

    Howell, S. H. Endoplasmic reticulum stress responses in plants. Annu. Rev. Plant Biol. 64, 477–499 (2013).

    CAS  Article  Google Scholar 

  32. 32

    Sun, T., Zhang, Q., Gao, M. & Zhang, Y. Regulation of SOBIR1 accumulation and activation of defense responses in bir1-1 by specific components of ER quality control. Plant J. 77, 748–756 (2014).

    CAS  Article  Google Scholar 

  33. 33

    Nekrasov, V. et al. Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity. EMBO J. 28, 3428–3438 (2009).

    CAS  Article  Google Scholar 

  34. 34

    Saijo, Y. et al. Receptor quality control in the endoplasmic reticulum for plant innate immunity. EMBO J. 28, 3439–3449 (2009).

    CAS  Article  Google Scholar 

  35. 35

    Lu, X. et al. Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele. Proc. Natl Acad. Sci. USA 106, 22522–22527 (2009).

    CAS  Article  Google Scholar 

  36. 36

    Li, J. et al. Specific ER quality control components required for biogenesis of the plant innate immune receptor EFR. Proc. Natl Acad. Sci. USA 106, 15973–15978 (2009).

    CAS  Article  Google Scholar 

  37. 37

    Haweker, H. et al. Pattern recognition receptors require N-glycosylation to mediate plant immunity. J. Biol. Chem. 285, 4629–4636 (2010).

    Article  Google Scholar 

  38. 38

    von Numers, N. et al. Requirement of a homolog of glucosidase II beta-subunit for EFR-mediated defense signaling in Arabidopsis thaliana. Mol. Plant 3, 740–750 (2010).

    CAS  Article  Google Scholar 

  39. 39

    Jin, H., Yan, Z., Nam, K. H. & Li, J. Allele-specific suppression of a defective brassinosteroid receptor reveals a physiological role of UGGT in ER quality control. Mol. Cell 26, 821–830 (2007).

    CAS  Article  Google Scholar 

  40. 40

    Jin, H., Hong, Z., Su, W. & Li, J. M. A plant-specific calreticulin is a key retention factor for a defective brassinosteroid receptor in the endoplasmic reticulum. Proc. Natl Acad. Sci. USA 106, 13612–13617 (2009).

    CAS  Article  Google Scholar 

  41. 41

    Kang, J. S. et al. Salt tolerance of Arabidopsis thaliana requires maturation of N-glycosylated proteins in the Golgi apparatus. Proc. Natl Acad. Sci. USA 105, 5933–5938 (2008).

    CAS  Article  Google Scholar 

  42. 42

    Deng, Y., Srivastava, R. & Howell, S. H. Protein kinase and ribonuclease domains of IRE1 confer stress tolerance, vegetative growth, and reproductive development in Arabidopsis. Proc. Natl Acad. Sci. USA 110, 19633–19638 (2013).

    CAS  Article  Google Scholar 

  43. 43

    Wu, S., Shan, L. & He, P. Microbial signature-triggered plant defense responses and early signaling mechanisms. Plant Sci. 228C, 118–126 (2014).

    Article  Google Scholar 

  44. 44

    Chen, K., Fan, B., Du, L. & Chen, Z. Activation of hypersensitive cell death by pathogen-induced receptor-like protein kinases from Arabidopsis. Plant Mol. Biol. 56, 271–283 (2004).

    CAS  Article  Google Scholar 

  45. 45

    Chen, K., Du, L. & Chen, Z. Sensitization of defense responses and activation of programmed cell death by a pathogen-induced receptor-like protein kinase in Arabidopsis. Plant Mol. Biol. 53, 61–74 (2003).

    CAS  Article  Google Scholar 

  46. 46

    Acharya, B. R. et al. Overexpression of CRK13, an Arabidopsis cysteine-rich receptor-like kinase, results in enhanced resistance to Pseudomonas syringae. Plant J. 50, 488–499 (2007).

    CAS  Article  Google Scholar 

  47. 47

    Liebrand, T. W. H., van den Burg, H. A. & Joosten, M. H. A. J. Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci. 19, 123–132 (2014).

    CAS  Article  Google Scholar 

  48. 48

    Schwessinger, B. et al. Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLoS Genet. 7, e1002046 (2011).

    CAS  Article  Google Scholar 

  49. 49

    Yeh, Y. H., Chang, Y. H., Huang, P. Y., Huang, J. B. & Zimmerli, L. Enhanced Arabidopsis pattern-triggered immunity by overexpression of cysteine-rich receptor-like kinases. Frontiers in plant science 6, 322 (2015).

    Article  Google Scholar 

  50. 50

    Gao, X. Q. et al. Bifurcation of Arabidopsis NLR immune signaling via Ca2+- dependent protein kinases. PLoS Pathog. 9, 14 (2013).

    Article  Google Scholar 

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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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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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