Home LiteratureArticle Details
PMID: 21187394 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Conserved endoplasmic reticulum-associated degradation system to eliminate mutated receptor-like kinases in Arabidopsis.

Su W, Liu Y, Xia Y, Hong Z, Li J

Abstract

Endoplasmic reticulum (ER)-associated degradation (ERAD) is an integral part of the ER quality-control system that removes toxic misfolded proteins via ubiquitin/proteasome-mediated degradation. Most of our knowledge on ERAD comes from biochemical and genetic studies in yeast and mammalian cells. Although ERAD is known to operate in plant cells, little is known about its molecular components and its biochemical mechanism. A genetic screen for suppressors of the Arabidopsis bri1-9, a weak dwarf mutant caused by ER retention of a structurally defective yet biochemically competent brassinosteroid (BR) receptor BRI1, resulted in identification of the EMS-mutagenized bri1 suppressor 5 (EBS5) gene that encodes an Arabidopsis homolog of the yeast Hrd3/mammalian Sel1L protein known to be involved in ERAD. Loss-of-function ebs5 mutations block the ERAD of bri1-9 and bri1-5, another ER-retained BR receptor. We showed that EBS5 complemented the ERAD defect of the yeast Δhrd3 mutant and interacted with the two mutated BR receptors in plant cells. Using a reverse genetic approach, we discovered that two Arabidopsis homologs of the yeast/mammalian Hrd1, an ER membrane-localized ubiquitin ligase, function redundantly in the ERAD of bri1-9. Together, our results revealed functional roles of two conserved ERAD components in degrading mutated/misfolded receptor-like kinases in Arabidopsis.

MeSH Terms
Arabidopsis/metabolism Arabidopsis Proteins/genetics Cloning, Molecular Cycloheximide/pharmacology Endoplasmic Reticulum/metabolism Genetic Complementation Test Glycoproteins/chemistry Immunoprecipitation Mutation Protein Denaturation Protein Folding Receptors, Steroid/metabolism Time Factors Transgenes Ubiquitin-Protein Ligases/metabolism
Chemicals
Arabidopsis Proteins Glycoproteins Receptors, Steroid Cycloheximide Ubiquitin-Protein Ligases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Su Wei
Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, MI 48109-1048, USA.
Liu Yidan
Xia Yang
Hong Zhi
Li Jianming
References (46)
46 references, click to expand
  1. ER quality control can lead to retrograde transport from the ER lumen to the cytosol and the nucleoplasm in plants.
    Plant J. 2003 May;34(3):269-81 PMID: 12713534
  2. Allele-specific suppression of a defective brassinosteroid receptor reveals a physiological role of UGGT in ER quality control.
    Mol Cell. 2007 Jun 22;26(6):821-30 PMID: 17588517
  3. Stringent requirement for HRD1, SEL1L, and OS-9/XTP3-B for disposal of ERAD-LS substrates.
    J Cell Biol. 2010 Jan 25;188(2):223-35 PMID: 20100910
  4. In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration.
    Methods Mol Biol. 1998;82:259-66 PMID: 9664431
  5. Intracellular signaling by the unfolded protein response.
    Annu Rev Cell Dev Biol. 2006;22:487-508 PMID: 16822172
  6. Defining the glycan destruction signal for endoplasmic reticulum-associated degradation.
    Mol Cell. 2008 Dec 26;32(6):870-7 PMID: 19111666
  7. A complex of Yos9p and the HRD ligase integrates endoplasmic reticulum quality control into the degradation machinery.
    Nat Cell Biol. 2006 Aug;8(8):849-54 PMID: 16845381
  8. BIN2, a new brassinosteroid-insensitive locus in Arabidopsis.
    Plant Physiol. 2001 Sep;127(1):14-22 PMID: 11553730
  9. Quality control in the endoplasmic reticulum.
    Nat Rev Mol Cell Biol. 2003 Mar;4(3):181-91 PMID: 12612637
  10. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction.
    Cell. 1997 Sep 5;90(5):929-38 PMID: 9298904
  11. Multiprotein complexes that link dislocation, ubiquitination, and extraction of misfolded proteins from the endoplasmic reticulum membrane.
    Proc Natl Acad Sci U S A. 2005 Oct 4;102(40):14296-301 PMID: 16186509
  12. ER quality control of immune receptors and regulators in plants.
    Cell Microbiol. 2010 Jun;12(6):716-24 PMID: 20408850
  13. Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes.
    Plant Cell. 2003 Feb;15(2):561-76 PMID: 12566592
  14. Deficiency of suppressor enhancer Lin12 1 like (SEL1L) in mice leads to systemic endoplasmic reticulum stress and embryonic lethality.
    J Biol Chem. 2010 Apr 30;285(18):13694-703 PMID: 20197277
  15. The recognition and retrotranslocation of misfolded proteins from the endoplasmic reticulum.
    Traffic. 2008 Jun;9(6):861-70 PMID: 18315532
  16. A plant-specific calreticulin is a key retention factor for a defective brassinosteroid receptor in the endoplasmic reticulum.
    Proc Natl Acad Sci U S A. 2009 Aug 11;106(32):13612-7 PMID: 19597144
  17. Role of 26S proteasome and HRD genes in the degradation of 3-hydroxy-3-methylglutaryl-CoA reductase, an integral endoplasmic reticulum membrane protein.
    Mol Biol Cell. 1996 Dec;7(12):2029-44 PMID: 8970163
  18. Specific ER quality control components required for biogenesis of the plant innate immune receptor EFR.
    Proc Natl Acad Sci U S A. 2009 Sep 15;106(37):15973-8 PMID: 19717464
  19. Identification and characterization of endoplasmic reticulum-associated degradation proteins differentially affected by endoplasmic reticulum stress.
    Plant Physiol. 2005 May;138(1):218-31 PMID: 15849299
  20. Two putative BIN2 substrates are nuclear components of brassinosteroid signaling.
    Plant Physiol. 2002 Nov;130(3):1221-9 PMID: 12427989
  21. Mutations of an alpha1,6 mannosyltransferase inhibit endoplasmic reticulum-associated degradation of defective brassinosteroid receptors in Arabidopsis.
    Plant Cell. 2009 Dec;21(12):3792-802 PMID: 20023196
  22. The EDEM and Yos9p families of lectin-like ERAD factors.
    Semin Cell Dev Biol. 2007 Dec;18(6):743-50 PMID: 17945519
  23. A luminal surveillance complex that selects misfolded glycoproteins for ER-associated degradation.
    Cell. 2006 Jul 28;126(2):349-59 PMID: 16873065
  24. Nuclear protein phosphatases with Kelch-repeat domains modulate the response to brassinosteroids in Arabidopsis.
    Genes Dev. 2004 Feb 15;18(4):448-60 PMID: 14977918
  25. Genome-wide insertional mutagenesis of Arabidopsis thaliana.
    Science. 2003 Aug 1;301(5633):653-7 PMID: 12893945
  26. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus.
    Plant J. 2003 Mar;33(5):949-56 PMID: 12609035
  27. Endoplasmic reticulum degradation requires lumen to cytosol signaling. Transmembrane control of Hrd1p by Hrd3p.
    J Cell Biol. 2000 Oct 2;151(1):69-82 PMID: 11018054
  28. The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation.
    Plant Mol Biol. 1994 Sep;25(6):989-94 PMID: 7919218
  29. Ubiquitin receptors and ERAD: a network of pathways to the proteasome.
    Semin Cell Dev Biol. 2007 Dec;18(6):780-91 PMID: 17942349
  30. Assembly of ER-associated protein degradation in vitro: dependence on cytosol, calnexin, and ATP.
    J Cell Biol. 1996 Feb;132(3):291-8 PMID: 8636208
  31. Sel1-like repeat proteins in signal transduction.
    Cell Signal. 2007 Jan;19(1):20-31 PMID: 16870393
  32. One step at a time: endoplasmic reticulum-associated degradation.
    Nat Rev Mol Cell Biol. 2008 Dec;9(12):944-57 PMID: 19002207
  33. Multiple mechanism-mediated retention of a defective brassinosteroid receptor in the endoplasmic reticulum of Arabidopsis.
    Plant Cell. 2008 Dec;20(12):3418-29 PMID: 19060110
  34. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation.
    Cell. 2006 May 19;125(4):749-60 PMID: 16713565
  35. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes.
    Nature. 2000 Apr 13;404(6779):770-4 PMID: 10783891
  36. Endoplasmic reticulum quality control and the unfolded protein response: insights from plants.
    Traffic. 2008 Sep;9(10):1581-8 PMID: 18557840
  37. Mapping the Arabidopsis organelle proteome.
    Proc Natl Acad Sci U S A. 2006 Apr 25;103(17):6518-23 PMID: 16618929
  38. Conserved ERAD-like quality control of a plant polytopic membrane protein.
    Plant Cell. 2005 Jan;17(1):149-63 PMID: 15598804
  39. Ubiquitin ligases, critical mediators of endoplasmic reticulum-associated degradation.
    Semin Cell Dev Biol. 2007 Dec;18(6):770-9 PMID: 17950636
  40. ER degradation of a misfolded luminal protein by the cytosolic ubiquitin-proteasome pathway.
    Science. 1996 Sep 20;273(5282):1725-8 PMID: 8781238
  41. Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1.
    Nature. 2005 Jan 13;433(7022):167-71 PMID: 15650741
  42. Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity.
    EMBO J. 2009 Nov 4;28(21):3428-38 PMID: 19763086
  43. A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development.
    Plant Physiol. 1996 Jul;111(3):671-8 PMID: 8754677
  44. Heat shock response relieves ER stress.
    EMBO J. 2008 Apr 9;27(7):1049-59 PMID: 18323774
  45. Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana.
    FEBS J. 2005 Jul;272(13):3461-76 PMID: 15978049
  46. Misfolded proteins are sorted by a sequential checkpoint mechanism of ER quality control.
    J Cell Biol. 2004 Apr;165(1):41-52 PMID: 15078901
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2011-01-11
Epub
2010-00-27
Pages
870-5
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3021050
Subset
IM
Grants
NIGMS NIH HHS · R01 GM060519 · United States
NIGMS NIH HHS · GM060519 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com