A Single Nonsynonymous Substitution in the RNA-Dependent RNA Polymerase of <i>Potato virus Y</i> Allows the Simultaneous Breakdown of Two Different Forms of Antiviral Resistance in <i>Capsicum annuum</i>

The dominant <i>Pvr4</i> gene in pepper (<i>Capsicum annuum</i>) confers resistance to members of six potyvirus species, all of which belong to the <i>Potato virus Y</i> (PVY) phylogenetic group. The corresponding avirulence factor in the PVY genome is the NIb cis...

Full description

Bibliographic Details
Main Authors: Benoît Moury, Thierry Michon, Vincent Simon, Alain Palloix
Format: Article
Language:English
Published: MDPI AG 2023-04-01
Series:Viruses
Subjects:
Online Access:https://www.mdpi.com/1999-4915/15/5/1081
_version_ 1797598059897552896
author Benoît Moury
Thierry Michon
Vincent Simon
Alain Palloix
author_facet Benoît Moury
Thierry Michon
Vincent Simon
Alain Palloix
author_sort Benoît Moury
collection DOAJ
description The dominant <i>Pvr4</i> gene in pepper (<i>Capsicum annuum</i>) confers resistance to members of six potyvirus species, all of which belong to the <i>Potato virus Y</i> (PVY) phylogenetic group. The corresponding avirulence factor in the PVY genome is the NIb cistron (i.e., RNA-dependent RNA polymerase). Here, we describe a new source of potyvirus resistance in the Guatemalan accession <i>C. annuum</i> cv. PM949. PM949 is resistant to members of at least three potyvirus species, a subset of those controlled by <i>Pvr4</i>. The F<sub>1</sub> progeny between PM949 and the susceptible cultivar Yolo Wonder was susceptible to PVY, indicating that the resistance is recessive. The segregation ratio between resistant and susceptible plants observed in the F<sub>2</sub> progeny matched preferably with resistance being determined by two unlinked recessive genes independently conferring resistance to PVY. Inoculations by grafting resulted in the selection of PVY mutants breaking PM949 resistance and, less efficiently, <i>Pvr4</i>–mediated resistance. The codon substitution E<sub>472</sub>K in the NIb cistron of PVY, which was shown previously to be sufficient to break <i>Pvr4</i> resistance, was also sufficient to break PM949 resistance, a rare example of cross-pathogenicity effect. In contrast, the other selected NIb mutants showed specific infectivity in PM949 or <i>Pvr4</i> plants. Comparison of <i>Pvr4</i> and PM949 resistance, which share the same target in PVY, provides interesting insights into the determinants of resistance durability.
first_indexed 2024-03-11T03:14:03Z
format Article
id doaj.art-07132da6e3b949b09a7aae5b4a56796e
institution Directory Open Access Journal
issn 1999-4915
language English
last_indexed 2024-03-11T03:14:03Z
publishDate 2023-04-01
publisher MDPI AG
record_format Article
series Viruses
spelling doaj.art-07132da6e3b949b09a7aae5b4a56796e2023-11-18T03:38:41ZengMDPI AGViruses1999-49152023-04-01155108110.3390/v15051081A Single Nonsynonymous Substitution in the RNA-Dependent RNA Polymerase of <i>Potato virus Y</i> Allows the Simultaneous Breakdown of Two Different Forms of Antiviral Resistance in <i>Capsicum annuum</i>Benoît Moury0Thierry Michon1Vincent Simon2Alain Palloix3INRAE, Pathologie Végétale, 84140 Montfavet, FranceUMR Biologie du Fruit et Pathologie, INRAE, Université de Bordeaux, CS 20032, 33882 Villenave d’Ornon, FranceINRAE, Pathologie Végétale, 84140 Montfavet, FranceINRAE, GAFL, 84140 Montfavet, FranceThe dominant <i>Pvr4</i> gene in pepper (<i>Capsicum annuum</i>) confers resistance to members of six potyvirus species, all of which belong to the <i>Potato virus Y</i> (PVY) phylogenetic group. The corresponding avirulence factor in the PVY genome is the NIb cistron (i.e., RNA-dependent RNA polymerase). Here, we describe a new source of potyvirus resistance in the Guatemalan accession <i>C. annuum</i> cv. PM949. PM949 is resistant to members of at least three potyvirus species, a subset of those controlled by <i>Pvr4</i>. The F<sub>1</sub> progeny between PM949 and the susceptible cultivar Yolo Wonder was susceptible to PVY, indicating that the resistance is recessive. The segregation ratio between resistant and susceptible plants observed in the F<sub>2</sub> progeny matched preferably with resistance being determined by two unlinked recessive genes independently conferring resistance to PVY. Inoculations by grafting resulted in the selection of PVY mutants breaking PM949 resistance and, less efficiently, <i>Pvr4</i>–mediated resistance. The codon substitution E<sub>472</sub>K in the NIb cistron of PVY, which was shown previously to be sufficient to break <i>Pvr4</i> resistance, was also sufficient to break PM949 resistance, a rare example of cross-pathogenicity effect. In contrast, the other selected NIb mutants showed specific infectivity in PM949 or <i>Pvr4</i> plants. Comparison of <i>Pvr4</i> and PM949 resistance, which share the same target in PVY, provides interesting insights into the determinants of resistance durability.https://www.mdpi.com/1999-4915/15/5/1081plant resistanceresistance durability<i>Potyvirus</i><i>Capsicum annuum</i>cross-pathogenicityvirulence determinant
spellingShingle Benoît Moury
Thierry Michon
Vincent Simon
Alain Palloix
A Single Nonsynonymous Substitution in the RNA-Dependent RNA Polymerase of <i>Potato virus Y</i> Allows the Simultaneous Breakdown of Two Different Forms of Antiviral Resistance in <i>Capsicum annuum</i>
Viruses
plant resistance
resistance durability
<i>Potyvirus</i>
<i>Capsicum annuum</i>
cross-pathogenicity
virulence determinant
title A Single Nonsynonymous Substitution in the RNA-Dependent RNA Polymerase of <i>Potato virus Y</i> Allows the Simultaneous Breakdown of Two Different Forms of Antiviral Resistance in <i>Capsicum annuum</i>
title_full A Single Nonsynonymous Substitution in the RNA-Dependent RNA Polymerase of <i>Potato virus Y</i> Allows the Simultaneous Breakdown of Two Different Forms of Antiviral Resistance in <i>Capsicum annuum</i>
title_fullStr A Single Nonsynonymous Substitution in the RNA-Dependent RNA Polymerase of <i>Potato virus Y</i> Allows the Simultaneous Breakdown of Two Different Forms of Antiviral Resistance in <i>Capsicum annuum</i>
title_full_unstemmed A Single Nonsynonymous Substitution in the RNA-Dependent RNA Polymerase of <i>Potato virus Y</i> Allows the Simultaneous Breakdown of Two Different Forms of Antiviral Resistance in <i>Capsicum annuum</i>
title_short A Single Nonsynonymous Substitution in the RNA-Dependent RNA Polymerase of <i>Potato virus Y</i> Allows the Simultaneous Breakdown of Two Different Forms of Antiviral Resistance in <i>Capsicum annuum</i>
title_sort single nonsynonymous substitution in the rna dependent rna polymerase of i potato virus y i allows the simultaneous breakdown of two different forms of antiviral resistance in i capsicum annuum i
topic plant resistance
resistance durability
<i>Potyvirus</i>
<i>Capsicum annuum</i>
cross-pathogenicity
virulence determinant
url https://www.mdpi.com/1999-4915/15/5/1081
work_keys_str_mv AT benoitmoury asinglenonsynonymoussubstitutioninthernadependentrnapolymeraseofipotatovirusyiallowsthesimultaneousbreakdownoftwodifferentformsofantiviralresistanceinicapsicumannuumi
AT thierrymichon asinglenonsynonymoussubstitutioninthernadependentrnapolymeraseofipotatovirusyiallowsthesimultaneousbreakdownoftwodifferentformsofantiviralresistanceinicapsicumannuumi
AT vincentsimon asinglenonsynonymoussubstitutioninthernadependentrnapolymeraseofipotatovirusyiallowsthesimultaneousbreakdownoftwodifferentformsofantiviralresistanceinicapsicumannuumi
AT alainpalloix asinglenonsynonymoussubstitutioninthernadependentrnapolymeraseofipotatovirusyiallowsthesimultaneousbreakdownoftwodifferentformsofantiviralresistanceinicapsicumannuumi
AT benoitmoury singlenonsynonymoussubstitutioninthernadependentrnapolymeraseofipotatovirusyiallowsthesimultaneousbreakdownoftwodifferentformsofantiviralresistanceinicapsicumannuumi
AT thierrymichon singlenonsynonymoussubstitutioninthernadependentrnapolymeraseofipotatovirusyiallowsthesimultaneousbreakdownoftwodifferentformsofantiviralresistanceinicapsicumannuumi
AT vincentsimon singlenonsynonymoussubstitutioninthernadependentrnapolymeraseofipotatovirusyiallowsthesimultaneousbreakdownoftwodifferentformsofantiviralresistanceinicapsicumannuumi
AT alainpalloix singlenonsynonymoussubstitutioninthernadependentrnapolymeraseofipotatovirusyiallowsthesimultaneousbreakdownoftwodifferentformsofantiviralresistanceinicapsicumannuumi