Cargando…

Multiple variants of the fungal effector AVR-Pik bind the HMA domain of the rice protein OsHIPP19, providing a foundation to engineer plant defense

Microbial plant pathogens secrete effector proteins, which manipulate the host to promote infection. Effectors can be recognized by plant intracellular nucleotide-binding leucine-rich repeat (NLR) receptors, initiating an immune response. The AVR-Pik effector from the rice blast fungus Magnaporthe o...

Descripción completa

Detalles Bibliográficos
Autores principales: Maidment, Josephine H.R., Franceschetti, Marina, Maqbool, Abbas, Saitoh, Hiromasa, Jantasuriyarat, Chatchawan, Kamoun, Sophien, Terauchi, Ryohei, Banfield, Mark J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Biochemistry and Molecular Biology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7961100/
https://www.ncbi.nlm.nih.gov/pubmed/33548226
http://dx.doi.org/10.1016/j.jbc.2021.100371
_version_ 1783665184722649088
author Maidment, Josephine H.R.
Franceschetti, Marina
Maqbool, Abbas
Saitoh, Hiromasa
Jantasuriyarat, Chatchawan
Kamoun, Sophien
Terauchi, Ryohei
Banfield, Mark J.
author_facet Maidment, Josephine H.R.
Franceschetti, Marina
Maqbool, Abbas
Saitoh, Hiromasa
Jantasuriyarat, Chatchawan
Kamoun, Sophien
Terauchi, Ryohei
Banfield, Mark J.
author_sort Maidment, Josephine H.R.
collection PubMed
description Microbial plant pathogens secrete effector proteins, which manipulate the host to promote infection. Effectors can be recognized by plant intracellular nucleotide-binding leucine-rich repeat (NLR) receptors, initiating an immune response. The AVR-Pik effector from the rice blast fungus Magnaporthe oryzae is recognized by a pair of rice NLR receptors, Pik-1 and Pik-2. Pik-1 contains a noncanonical integrated heavy-metal-associated (HMA) domain, which directly binds AVR-Pik to activate plant defenses. The host targets of AVR-Pik are also HMA-domain-containing proteins, namely heavy-metal-associated isoprenylated plant proteins (HIPPs) and heavy-metal-associated plant proteins (HPPs). Here, we demonstrate that one of these targets interacts with a wider set of AVR-Pik variants compared with the Pik-1 HMA domains. We define the biochemical and structural basis of the interaction between AVR-Pik and OsHIPP19 and compare the interaction to that formed with the HMA domain of Pik-1. Using analytical gel filtration and surface plasmon resonance, we show that multiple AVR-Pik variants, including the stealthy variants AVR-PikC and AVR-PikF, which do not interact with any characterized Pik-1 alleles, bind to OsHIPP19 with nanomolar affinity. The crystal structure of OsHIPP19 in complex with AVR-PikF reveals differences at the interface that underpin high-affinity binding of OsHIPP19-HMA to a wider set of AVR-Pik variants than achieved by the integrated HMA domain of Pik-1. Our results provide a foundation for engineering the HMA domain of Pik-1 to extend binding to currently unrecognized AVR-Pik variants and expand disease resistance in rice to divergent pathogen strains.
format Online
Article
Text
id pubmed-7961100
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher American Society for Biochemistry and Molecular Biology
record_format MEDLINE/PubMed
spelling pubmed-79611002021-03-19 Multiple variants of the fungal effector AVR-Pik bind the HMA domain of the rice protein OsHIPP19, providing a foundation to engineer plant defense Maidment, Josephine H.R. Franceschetti, Marina Maqbool, Abbas Saitoh, Hiromasa Jantasuriyarat, Chatchawan Kamoun, Sophien Terauchi, Ryohei Banfield, Mark J. J Biol Chem Research Article Microbial plant pathogens secrete effector proteins, which manipulate the host to promote infection. Effectors can be recognized by plant intracellular nucleotide-binding leucine-rich repeat (NLR) receptors, initiating an immune response. The AVR-Pik effector from the rice blast fungus Magnaporthe oryzae is recognized by a pair of rice NLR receptors, Pik-1 and Pik-2. Pik-1 contains a noncanonical integrated heavy-metal-associated (HMA) domain, which directly binds AVR-Pik to activate plant defenses. The host targets of AVR-Pik are also HMA-domain-containing proteins, namely heavy-metal-associated isoprenylated plant proteins (HIPPs) and heavy-metal-associated plant proteins (HPPs). Here, we demonstrate that one of these targets interacts with a wider set of AVR-Pik variants compared with the Pik-1 HMA domains. We define the biochemical and structural basis of the interaction between AVR-Pik and OsHIPP19 and compare the interaction to that formed with the HMA domain of Pik-1. Using analytical gel filtration and surface plasmon resonance, we show that multiple AVR-Pik variants, including the stealthy variants AVR-PikC and AVR-PikF, which do not interact with any characterized Pik-1 alleles, bind to OsHIPP19 with nanomolar affinity. The crystal structure of OsHIPP19 in complex with AVR-PikF reveals differences at the interface that underpin high-affinity binding of OsHIPP19-HMA to a wider set of AVR-Pik variants than achieved by the integrated HMA domain of Pik-1. Our results provide a foundation for engineering the HMA domain of Pik-1 to extend binding to currently unrecognized AVR-Pik variants and expand disease resistance in rice to divergent pathogen strains. American Society for Biochemistry and Molecular Biology 2021-02-04 /pmc/articles/PMC7961100/ /pubmed/33548226 http://dx.doi.org/10.1016/j.jbc.2021.100371 Text en © 2021 The Authors https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Research Article
Maidment, Josephine H.R.
Franceschetti, Marina
Maqbool, Abbas
Saitoh, Hiromasa
Jantasuriyarat, Chatchawan
Kamoun, Sophien
Terauchi, Ryohei
Banfield, Mark J.
Multiple variants of the fungal effector AVR-Pik bind the HMA domain of the rice protein OsHIPP19, providing a foundation to engineer plant defense
title Multiple variants of the fungal effector AVR-Pik bind the HMA domain of the rice protein OsHIPP19, providing a foundation to engineer plant defense
title_full Multiple variants of the fungal effector AVR-Pik bind the HMA domain of the rice protein OsHIPP19, providing a foundation to engineer plant defense
title_fullStr Multiple variants of the fungal effector AVR-Pik bind the HMA domain of the rice protein OsHIPP19, providing a foundation to engineer plant defense
title_full_unstemmed Multiple variants of the fungal effector AVR-Pik bind the HMA domain of the rice protein OsHIPP19, providing a foundation to engineer plant defense
title_short Multiple variants of the fungal effector AVR-Pik bind the HMA domain of the rice protein OsHIPP19, providing a foundation to engineer plant defense
title_sort multiple variants of the fungal effector avr-pik bind the hma domain of the rice protein oshipp19, providing a foundation to engineer plant defense
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7961100/
https://www.ncbi.nlm.nih.gov/pubmed/33548226
http://dx.doi.org/10.1016/j.jbc.2021.100371
work_keys_str_mv AT maidmentjosephinehr multiplevariantsofthefungaleffectoravrpikbindthehmadomainofthericeproteinoshipp19providingafoundationtoengineerplantdefense
AT franceschettimarina multiplevariantsofthefungaleffectoravrpikbindthehmadomainofthericeproteinoshipp19providingafoundationtoengineerplantdefense
AT maqboolabbas multiplevariantsofthefungaleffectoravrpikbindthehmadomainofthericeproteinoshipp19providingafoundationtoengineerplantdefense
AT saitohhiromasa multiplevariantsofthefungaleffectoravrpikbindthehmadomainofthericeproteinoshipp19providingafoundationtoengineerplantdefense
AT jantasuriyaratchatchawan multiplevariantsofthefungaleffectoravrpikbindthehmadomainofthericeproteinoshipp19providingafoundationtoengineerplantdefense
AT kamounsophien multiplevariantsofthefungaleffectoravrpikbindthehmadomainofthericeproteinoshipp19providingafoundationtoengineerplantdefense
AT terauchiryohei multiplevariantsofthefungaleffectoravrpikbindthehmadomainofthericeproteinoshipp19providingafoundationtoengineerplantdefense
AT banfieldmarkj multiplevariantsofthefungaleffectoravrpikbindthehmadomainofthericeproteinoshipp19providingafoundationtoengineerplantdefense