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Plants use leucine-rich repeat receptor kinases (LRR-RKs) to sense sequence diverse peptide hormones at the cell surface. A 3.0-Å crystal structure of the LRR-RK GSO1/SGN3 regulating Casparian strip formation in the endodermis reveals a large spiral-shaped ectodomain. The domain provides a binding platform for 21 amino acid CIF peptide ligands, which are tyrosine sulfated by the tyrosylprotein sulfotransferase TPST/SGN2. GSO1/SGN3 harbors a binding pocket for sulfotyrosine and makes extended backbone interactions with CIF2. Quantitative biochemical comparisons reveal that GSO1/SGN3-CIF2 represents one of the strongest receptor-ligand pairs known in plants. Multiple missense mutations are required to block CIF2 binding in vitro and GSO1/SGN3 function in vivo. Using structure-guided sequence analysis we uncover previously uncharacterized CIF peptides conserved among higher plants. Quantitative binding assays with known and novel CIFs suggest that the homologous LRR-RKs GSO1/SGN3 and GSO2 have evolved unique peptide binding properties to control different developmental processes. A quantitative biochemical interaction screen, a CIF peptide antagonist and genetic analyses together implicate SERK proteins as essential coreceptor kinases required for GSO1/SGN3 and GSO2 receptor activation. Our work provides a mechanistic framework for the recognition of sequence-divergent peptide hormones in plants.

Competing Interests: The authors declare no competing interest.

Titel:	Molecular mechanism for the recognition of sequence-divergent CIF peptides by the plant receptor kinases GSO1/SGN3 and GSO2.
Autor/in / Beteiligte Person:	Okuda, S ; Fujita, S ; Moretti, A ; Hohmann, U ; Doblas, VG ; Ma, Y ; Pfister, A ; Brandt, B ; Geldner, N ; Hothorn, M
Link:	Full Text Finder (Volltext)
Zeitschrift:	Proceedings of the National Academy of Sciences of the United States of America, Jg. 117 (2020-02-04), Heft 5, S. 2693-2703
Veröffentlichung:	Washington, DC : National Academy of Sciences, 2020
Medientyp:	academicJournal
ISSN:	1091-6490 (electronic)
DOI:	10.1073/pnas.1911553117
Schlagwort:	Amino Acid Sequence Arabidopsis chemistry Arabidopsis enzymology Arabidopsis genetics Arabidopsis Proteins chemistry Arabidopsis Proteins genetics Kinetics Ligands Peptides chemistry Plant Growth Regulators chemistry Plant Growth Regulators metabolism Protein Binding Protein Kinases chemistry Protein Kinases genetics Arabidopsis metabolism Arabidopsis Proteins metabolism Peptides metabolism Protein Kinases metabolism
Sonstiges:	Nachgewiesen in: MEDLINE Sprachen: English Publication Type: Journal Article; Research Support, Non-U.S. Gov't Language: English [Proc Natl Acad Sci U S A] 2020 Feb 04; Vol. 117 (5), pp. 2693-2703. <i>Date of Electronic Publication: </i>2020 Jan 21. MeSH Terms: Arabidopsis / metabolism ; Arabidopsis Proteins / metabolism ; Peptides / metabolism ; Protein Kinases / metabolism ; Amino Acid Sequence ; Arabidopsis / chemistry ; Arabidopsis / enzymology ; Arabidopsis / genetics ; Arabidopsis Proteins / chemistry ; Arabidopsis Proteins / genetics ; Kinetics ; Ligands ; Peptides / chemistry ; Plant Growth Regulators / chemistry ; Plant Growth Regulators / metabolism ; Protein Binding ; Protein Kinases / chemistry ; Protein Kinases / genetics References: Science. 2010 Aug 27;329(5995):1065-7. (PMID: 20798316) ; Plant J. 2008 Apr;54(1):30-42. (PMID: 18088309) ; Science. 2016 Dec 23;354(6319):1594-1597. (PMID: 27940581) ; Plant Physiol. 2015 Jul;168(3):1106-21. (PMID: 25944825) ; Proc Natl Acad Sci U S A. 2006 Jun 27;103(26):10098-103. (PMID: 16785434) ; J Mol Biol. 2007 Sep 21;372(3):774-97. (PMID: 17681537) ; Proc Natl Acad Sci U S A. 2018 Mar 27;115(13):3488-3493. (PMID: 29531026) ; Proc Natl Acad Sci U S A. 2008 Jan 8;105(1):258-63. (PMID: 18172197) ; EMBO Rep. 2017 Aug;18(8):1367-1381. (PMID: 28607033) ; Nature. 2018 Jan 18;553(7688):342-346. (PMID: 29320478) ; Plant J. 2015 Apr;82(2):328-36. (PMID: 25754504) ; Acta Crystallogr D Struct Biol. 2019 May 1;75(Pt 5):488-497. (PMID: 31063151) ; Science. 2017 Jan 20;355(6322):284-286. (PMID: 28104889) ; BMC Plant Biol. 2007 Mar 30;7:16. (PMID: 17397538) ; Nucleic Acids Res. 2007 Jul;35(Web Server issue):W375-83. (PMID: 17452350) ; Plant Cell. 2018 Oct;30(10):2383-2401. (PMID: 30201822) ; Science. 2017 Jan 20;355(6322):280-284. (PMID: 28104888) ; Plant J. 2014 Jan;77(1):46-58. (PMID: 24147836) ; Curr Biol. 2007 Jul 3;17(13):1109-15. (PMID: 17600708) ; J Appl Crystallogr. 2011 Dec 1;44(Pt 6):1285-1287. (PMID: 22477786) ; Annu Rev Plant Biol. 2014;65:385-413. (PMID: 24779997) ; Proc Natl Acad Sci U S A. 2019 Apr 23;116(17):8525-8534. (PMID: 30948631) ; Plant J. 1999 May;18(3):265-76. (PMID: 10377992) ; Nat Chem Biol. 2009 Aug;5(8):578-80. (PMID: 19525968) ; Cell Res. 2016 Jun;26(6):674-85. (PMID: 27229311) ; Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32. (PMID: 15572765) ; Proc Natl Acad Sci U S A. 2009 Sep 1;106(35):15067-72. (PMID: 19666544) ; Elife. 2014 Sep 16;3:e03115. (PMID: 25233277) ; Acta Crystallogr D Biol Crystallogr. 2010 Feb;66(Pt 2):213-21. (PMID: 20124702) ; Plant Cell. 2005 Dec;17(12):3350-61. (PMID: 16284306) ; Science. 2013 Nov 1;342(6158):624-8. (PMID: 24114786) ; Mol Plant. 2016 Oct 10;9(10):1406-1414. (PMID: 27449136) ; Curr Biol. 2015 Sep 21;25(18):2361-72. (PMID: 26320950) ; Cell Res. 2015 Jan;25(1):110-20. (PMID: 25475059) ; Cell Res. 2016 May;26(5):543-55. (PMID: 27055373) ; Annu Rev Plant Biol. 2017 Apr 28;68:109-137. (PMID: 28125280) ; Curr Opin Plant Biol. 2017 Oct;39:136-143. (PMID: 28750257) ; Dev Dyn. 2014 Feb;243(2):257-78. (PMID: 24123341) ; J Appl Crystallogr. 2007 Aug 1;40(Pt 4):658-674. (PMID: 19461840) ; Proc Natl Acad Sci U S A. 2016 Apr 5;113(14):3897-902. (PMID: 27001831) ; Elife. 2016 Apr 08;5:. (PMID: 27058169) ; Nature. 2015 Sep 10;525(7568):265-8. (PMID: 26308901) ; Development. 2018 May 22;145(10):. (PMID: 29789310) ; Nat Plants. 2018 Apr;4(4):205-211. (PMID: 29581511) Grant Information: United States HHMI Howard Hughes Medical Institute Contributed Indexing: Keywords: Arabidopsis; coreceptor; peptide hormone; receptor kinase; root development Molecular Sequence: PDB 6S6Q Substance Nomenclature: 0 (Arabidopsis Proteins) ; 0 (Ligands) ; 0 (Peptides) ; 0 (Plant Growth Regulators) ; EC 2.7.- (Protein Kinases) ; EC 2.7.1.- (GASSHO1 protein, Arabidopsis) ; EC 2.7.1.- (GASSHO2 protein, Arabidopsis) Entry Date(s): Date Created: 20200123 Date Completed: 20200615 Latest Revision: 20200615 Update Code: 20240513 PubMed Central ID: PMC7007523

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Molecular mechanism for the recognition of sequence-divergent CIF peptides by the plant receptor kinases GSO1/SGN3 and GSO2.