The blast pathogen effector AVR-Pik binds and stabilizes rice heavy metal-associated (HMA) proteins to co-opt their function in immunity.

Publisher: Public Library of Science Country of Publication: United States NLM ID: 101238921 Publication Model: eCollection Cited Medium: Internet ISSN: 1553-7374 (Electronic) Linking ISSN: 15537366 NLM ISO Abbreviation: PLoS Pathog Subsets: MEDLINE

Original Publication: San Francisco, CA : Public Library of Science, c2005-

Oryza*/microbiology ; Oryza*/metabolism ; Oryza*/immunology ; Plant Diseases*/microbiology ; Plant Diseases*/immunology ; Plant Proteins*/metabolism ; Plant Immunity*; Disease Resistance ; Fungal Proteins/metabolism ; Host-Pathogen Interactions/immunology ; Metals, Heavy/metabolism ; NLR Proteins/metabolism ; Ascomycota/metabolism

Intracellular nucleotide-binding domain and leucine-rich repeat-containing (NLR) receptors play crucial roles in immunity across multiple domains of life. In plants, a subset of NLRs contain noncanonical integrated domains that are thought to have evolved from host targets of pathogen effectors to serve as pathogen baits. However, the functions of host proteins with similarity to NLR integrated domains and the extent to which they are targeted by pathogen effectors remain largely unknown. Here, we show that the blast fungus effector AVR-Pik binds a subset of related rice proteins containing a heavy metal-associated (HMA) domain, one of the domains that has repeatedly integrated into plant NLR immune receptors. We find that AVR-Pik binding stabilizes the rice small HMA (sHMA) proteins OsHIPP19 and OsHIPP20. Knockout of OsHIPP20 causes enhanced disease resistance towards the blast pathogen, indicating that OsHIPP20 is a susceptibility gene (S-gene). We propose that AVR-Pik has evolved to bind HMA domain proteins and co-opt their function to suppress immunity. Yet this binding carries a trade-off, it triggers immunity in plants carrying NLR receptors with integrated HMA domains.
Competing Interests: The authors have declared that no competing interests exist.
(Copyright: © 2024 Oikawa et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

PLoS Pathog. 2015 Oct 27;11(10):e1005228. (PMID: 26506000)
Biochem Biophys Res Commun. 2007 Mar 9;354(2):385-90. (PMID: 17223078)
Nat Biotechnol. 2015 Mar;33(3):290-5. (PMID: 25690850)
Front Plant Sci. 2014 Nov 25;5:606. (PMID: 25506347)
PLoS One. 2008;3(11):e3647. (PMID: 18985154)
Science. 1997 Oct 31;278(5339):853-6. (PMID: 9346482)
Nat Methods. 2017 Jun;14(6):587-589. (PMID: 28481363)
Clin Chem. 1996 Sep;42(9):1518-26. (PMID: 8787723)
Front Plant Sci. 2015 Mar 05;6:134. (PMID: 25798142)
Mol Plant Microbe Interact. 2019 Jun;32(6):740-749. (PMID: 30601714)
New Phytol. 2009;181(1):89-102. (PMID: 18823312)
Plant Physiol. 2018 Mar;176(3):2052-2070. (PMID: 29374107)
Cell. 2015 May 21;161(5):1074-1088. (PMID: 26000483)
Genetics. 2008 Dec;180(4):2267-76. (PMID: 18940787)
PLoS Pathog. 2022 Sep 29;18(9):e1010792. (PMID: 36173975)
FEBS J. 2013 Apr;280(7):1604-16. (PMID: 23368984)
Front Plant Sci. 2016 Nov 21;7:1712. (PMID: 27917181)
Mol Biol Evol. 2013 Apr;30(4):772-80. (PMID: 23329690)
Elife. 2015 Aug 25;4:. (PMID: 26304198)
Plant Mol Biol. 1999 Sep;41(1):139-50. (PMID: 10561075)
Nat Commun. 2017 Oct 17;8(1):1004. (PMID: 29042542)
New Phytol. 2016 Apr;210(2):618-26. (PMID: 26848538)
Nat Methods. 2022 Jun;19(6):679-682. (PMID: 35637307)
Cell. 2015 May 21;161(5):1089-1100. (PMID: 26000484)
BMC Biol. 2016 Feb 19;14:8. (PMID: 26891798)
Cell. 1994 Jan 28;76(2):403-10. (PMID: 8293473)
Mol Plant Pathol. 2018 Feb 22;:. (PMID: 29470862)
Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):14652-7. (PMID: 12409616)
Plant Biol (Stuttg). 2015 Nov;17(6):1176-86. (PMID: 25951496)
Mol Plant Microbe Interact. 2009 Feb;22(2):115-22. (PMID: 19132864)
Science. 2014 Apr 18;344(6181):299-303. (PMID: 24744375)
PLoS Biol. 2008 Jan;6(1):e7. (PMID: 18215111)
Nat Protoc. 2010 Feb;5(2):227-38. (PMID: 20134421)
Plant Cell. 2009 May;21(5):1573-91. (PMID: 19454732)
Plant J. 2006 Sep;47(6):969-76. (PMID: 16961734)
J Biol Chem. 2021 Jan-Jun;296:100371. (PMID: 33548226)
Nat Plants. 2016 May 27;2(6):16075. (PMID: 27255839)
Elife. 2019 Sep 19;8:. (PMID: 31535976)
J Biol Chem. 2001 Mar 16;276(11):8415-26. (PMID: 11083871)
Rice (N Y). 2013 Feb 06;6(1):4. (PMID: 24280374)
Elife. 2023 May 18;12:. (PMID: 37199729)
Curr Opin Chem Biol. 2000 Apr;4(2):140-7. (PMID: 10742187)
Plant J. 2024 May;118(3):839-855. (PMID: 38271178)
Curr Opin Plant Biol. 2017 Aug;38:59-67. (PMID: 28494248)
Mol Biol Evol. 2018 Feb 1;35(2):518-522. (PMID: 29077904)
Plant Cell. 2013 Apr;25(4):1463-81. (PMID: 23548743)
Mol Biol Evol. 2015 Jan;32(1):268-74. (PMID: 25371430)
Plant J. 2012 Dec;72(6):894-907. (PMID: 22805093)
Proc Natl Acad Sci U S A. 2018 Nov 6;115(45):11637-11642. (PMID: 30355769)
Plant Mol Biol. 2009 Jan;69(1-2):213-26. (PMID: 18974936)
Nat Methods. 2015 Apr;12(4):357-60. (PMID: 25751142)
Nat Plants. 2018 Aug;4(8):576-585. (PMID: 29988155)
FEBS Lett. 2008 Jan 23;582(2):221-8. (PMID: 18082144)
Science. 2009 Aug 21;325(5943):998-1001. (PMID: 19696351)
Plant Physiol. 1998 Aug;117(4):1227-34. (PMID: 9701579)
Plant Mol Biol. 2015 Aug;88(6):561-72. (PMID: 26188471)
Nat Methods. 2012 Jul;9(7):671-5. (PMID: 22930834)
Protein Sci. 2022 Aug;31(8):e4379. (PMID: 35900023)
Plant Physiol. 2012 Jul;159(3):1099-110. (PMID: 22555879)
Plant J. 2011 May;66(3):467-79. (PMID: 21251109)
Genome Biol. 2018 Feb 19;19(1):23. (PMID: 29458393)
Mol Plant Microbe Interact. 2018 Jan;31(1):34-45. (PMID: 29144205)
Plant Physiol. 2019 Apr;179(4):1227-1235. (PMID: 30530739)
Trends Genet. 1994 Jul;10(7):246-52. (PMID: 8091505)

0 (Plant Proteins)
0 (Fungal Proteins)
0 (Metals, Heavy)
0 (NLR Proteins)

Date Created: 20241118 Date Completed: 20241202 Latest Revision: 20241204

20241204

PMC11611257

10.1371/journal.ppat.1012647

39556648