Barberry plays an active role as an alternate host of Puccinia graminis in Spain

Dolors Villegas; Radhika Bartaula; Carlos Cantero-Martínez; Douglas Luster; Les J Szabo; Pablo Olivera; Anna Berlin; Julian Rodriguez-Algaba; Mogens S. Hovmøller; Robert McIntosh; Yue Jin

doi:10.1111/ppa.13540

Barberry plays an active role as an alternate host of Puccinia graminis in Spain

Dolors Villegas, Radhika Bartaula, Carlos Cantero-Martínez, Douglas Luster, Les J Szabo, Pablo Olivera, Anna Berlin, Julian Rodriguez-Algaba, Mogens S. Hovmøller, Robert McIntosh, Yue Jin

Plant Pathology

Research output: Contribution to journal › Article › peer-review

7 Scopus citations

Abstract

Stem rust, caused by Puccinia graminis, is a destructive group of diseases. The pathogen uses Berberis species as alternate hosts to complete its life cycle. B. vulgaris and the endemic species B. hispanica and B. garciae are present in Spain. The objective of this study was to investigate the functionality of the indigenous barberry as alternate hosts. Field surveys were conducted in 2018 and 2019 in Huesca, Teruel and Albacete provinces of Spain. Aecial samples on barberry were analysed via infection assays and DNA analysis. B. garciae was predominant in Huesca and Teruel provinces, often found in the field margins of cereal crops. Aecial infections on B. garciae were observed in May and uredinial infections on cereal crops in June. Scattered B. hispanica bushes were occasionally found near cereal crops in Albacete, where aecial infections on B. hispanica were observed in June when most cereal crops were mature. Infection assays using aeciospores resulted in stem rust infections on susceptible genotypes of wheat, barley, rye and oat, indicating the presence of the sexual cycle for P. graminis f. sp. tritici, f. sp. secalis and f. sp. avenae. Sequence analyses from aecial samples supported this finding as well as the presence of Puccinia brachypodii. This study provides the first evidence that indigenous Berberis species play an active role in the sexual cycle of P. graminis under natural conditions in Spain.

Original language	English (US)
Pages (from-to)	1174-1184
Number of pages	11
Journal	Plant Pathology
Volume	71
Issue number	5
DOIs	https://doi.org/10.1111/ppa.13540
State	Published - Jun 2022

Bibliographical note

Funding Information:
The research was supported by the United States Department of Agriculture‐Agricultural Research Service, the Bill and Melinda Gates Foundation and the United Kingdom Department for International Development managed by Cornell University, USA, grant number: DGGW‐OPP1133199, and the State Research Agency (AEI), Spain, project PID2020‐118650RR‐C31. Thanks to Dr Fanny Álvaro for the initial observation and sampling of aecial infection on barberry. The assistance of Dr Joan Pedrol and Dr Rosario Fanlo (University of Lleida, Spain) in grass species identification is gratefully acknowledged. We thank the assistance of Amparo López Olmeda (Teruel Plant Health Service), Gloria Herrero Sánchez (Cereales Teruel Sociedad Cooperativa) and Vicente Lozano Herrera (farmer cereal producer). Meteorological data from the El Ballestero site (Albacete province) were kindly provided by Manuel Fernández. Data from surface cropping area of Aragón have been provided by Sección de estadística del Departamento de Agricultura, Ganadería y Medio Ambiente del Gobierno de Aragón (Silvia Quílez‐Domingo). The support of Daniel Gómez and Alberto Pastoriza (Herbarium curators in the Pyrenean Institute of Ecology, IPE‐CSIC, Jaca) is thankfully acknowledged. Technical assistance of Melissa Carter, Jerry Johnson and Kim‐Phuong Nguyen from USDA‐ARS is acknowledged. Dr Villegas acknowledges the contribution of the CERCA program (Generalitat de Catalunya, Spain).

Funding Information:
The research was supported by the United States Department of Agriculture-Agricultural Research Service, the Bill and Melinda Gates Foundation and the United Kingdom Department for International Development managed by Cornell University, USA, grant number: DGGW-OPP1133199, and the State Research Agency (AEI), Spain, project PID2020-118650RR-C31. Thanks to Dr Fanny ?lvaro for the initial observation and sampling of aecial infection on barberry. The assistance of Dr Joan Pedrol and Dr Rosario Fanlo (University of Lleida, Spain) in grass species identification is gratefully acknowledged. We thank the assistance of Amparo L?pez Olmeda (Teruel Plant Health Service), Gloria Herrero S?nchez (Cereales Teruel Sociedad Cooperativa) and Vicente Lozano Herrera (farmer cereal producer). Meteorological data from the El Ballestero site (Albacete province) were kindly provided by Manuel Fern?ndez. Data from surface cropping area of Arag?n have been provided by Secci?n de estad?stica del Departamento de Agricultura, Ganader?a y Medio Ambiente del Gobierno de Arag?n (Silvia Qu?lez-Domingo). The support of Daniel G?mez and Alberto Pastoriza (Herbarium curators in the Pyrenean Institute of Ecology, IPE-CSIC, Jaca) is thankfully acknowledged. Technical assistance of Melissa Carter, Jerry Johnson and Kim-Phuong Nguyen from USDA-ARS is acknowledged. Dr Villegas acknowledges the contribution of the CERCA program (Generalitat de Catalunya, Spain).

Publisher Copyright:
© 2022 The Authors. Plant Pathology published by John Wiley & Sons Ltd on behalf of British Society for Plant Pathology. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA

Keywords

Berberis garciae
Berberis hispanica
aecial host
sexual cycle
stem rust

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10.1111/ppa.13540

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title = "Barberry plays an active role as an alternate host of Puccinia graminis in Spain",

abstract = "Stem rust, caused by Puccinia graminis, is a destructive group of diseases. The pathogen uses Berberis species as alternate hosts to complete its life cycle. B. vulgaris and the endemic species B. hispanica and B. garciae are present in Spain. The objective of this study was to investigate the functionality of the indigenous barberry as alternate hosts. Field surveys were conducted in 2018 and 2019 in Huesca, Teruel and Albacete provinces of Spain. Aecial samples on barberry were analysed via infection assays and DNA analysis. B. garciae was predominant in Huesca and Teruel provinces, often found in the field margins of cereal crops. Aecial infections on B. garciae were observed in May and uredinial infections on cereal crops in June. Scattered B. hispanica bushes were occasionally found near cereal crops in Albacete, where aecial infections on B. hispanica were observed in June when most cereal crops were mature. Infection assays using aeciospores resulted in stem rust infections on susceptible genotypes of wheat, barley, rye and oat, indicating the presence of the sexual cycle for P. graminis f. sp. tritici, f. sp. secalis and f. sp. avenae. Sequence analyses from aecial samples supported this finding as well as the presence of Puccinia brachypodii. This study provides the first evidence that indigenous Berberis species play an active role in the sexual cycle of P. graminis under natural conditions in Spain.",

keywords = "Berberis garciae, Berberis hispanica, aecial host, sexual cycle, stem rust",

author = "Dolors Villegas and Radhika Bartaula and Carlos Cantero-Mart{\'i}nez and Douglas Luster and Szabo, {Les J} and Pablo Olivera and Anna Berlin and Julian Rodriguez-Algaba and Hovm{\o}ller, {Mogens S.} and Robert McIntosh and Yue Jin",

note = "Funding Information: The research was supported by the United States Department of Agriculture‐Agricultural Research Service, the Bill and Melinda Gates Foundation and the United Kingdom Department for International Development managed by Cornell University, USA, grant number: DGGW‐OPP1133199, and the State Research Agency (AEI), Spain, project PID2020‐118650RR‐C31. Thanks to Dr Fanny {\'A}lvaro for the initial observation and sampling of aecial infection on barberry. The assistance of Dr Joan Pedrol and Dr Rosario Fanlo (University of Lleida, Spain) in grass species identification is gratefully acknowledged. We thank the assistance of Amparo L{\'o}pez Olmeda (Teruel Plant Health Service), Gloria Herrero S{\'a}nchez (Cereales Teruel Sociedad Cooperativa) and Vicente Lozano Herrera (farmer cereal producer). Meteorological data from the El Ballestero site (Albacete province) were kindly provided by Manuel Fern{\'a}ndez. Data from surface cropping area of Arag{\'o}n have been provided by Secci{\'o}n de estad{\'i}stica del Departamento de Agricultura, Ganader{\'i}a y Medio Ambiente del Gobierno de Arag{\'o}n (Silvia Qu{\'i}lez‐Domingo). The support of Daniel G{\'o}mez and Alberto Pastoriza (Herbarium curators in the Pyrenean Institute of Ecology, IPE‐CSIC, Jaca) is thankfully acknowledged. Technical assistance of Melissa Carter, Jerry Johnson and Kim‐Phuong Nguyen from USDA‐ARS is acknowledged. Dr Villegas acknowledges the contribution of the CERCA program (Generalitat de Catalunya, Spain). Funding Information: The research was supported by the United States Department of Agriculture-Agricultural Research Service, the Bill and Melinda Gates Foundation and the United Kingdom Department for International Development managed by Cornell University, USA, grant number: DGGW-OPP1133199, and the State Research Agency (AEI), Spain, project PID2020-118650RR-C31. Thanks to Dr Fanny ?lvaro for the initial observation and sampling of aecial infection on barberry. The assistance of Dr Joan Pedrol and Dr Rosario Fanlo (University of Lleida, Spain) in grass species identification is gratefully acknowledged. We thank the assistance of Amparo L?pez Olmeda (Teruel Plant Health Service), Gloria Herrero S?nchez (Cereales Teruel Sociedad Cooperativa) and Vicente Lozano Herrera (farmer cereal producer). Meteorological data from the El Ballestero site (Albacete province) were kindly provided by Manuel Fern?ndez. Data from surface cropping area of Arag?n have been provided by Secci?n de estad?stica del Departamento de Agricultura, Ganader?a y Medio Ambiente del Gobierno de Arag?n (Silvia Qu?lez-Domingo). The support of Daniel G?mez and Alberto Pastoriza (Herbarium curators in the Pyrenean Institute of Ecology, IPE-CSIC, Jaca) is thankfully acknowledged. Technical assistance of Melissa Carter, Jerry Johnson and Kim-Phuong Nguyen from USDA-ARS is acknowledged. Dr Villegas acknowledges the contribution of the CERCA program (Generalitat de Catalunya, Spain). Publisher Copyright: {\textcopyright} 2022 The Authors. Plant Pathology published by John Wiley & Sons Ltd on behalf of British Society for Plant Pathology. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA",

year = "2022",

month = jun,

doi = "10.1111/ppa.13540",

language = "English (US)",

volume = "71",

pages = "1174--1184",

journal = "Plant Pathology",

issn = "0032-0862",

publisher = "Wiley-Blackwell Publishing Ltd",

number = "5",

}

TY - JOUR

T1 - Barberry plays an active role as an alternate host of Puccinia graminis in Spain

AU - Villegas, Dolors

AU - Bartaula, Radhika

AU - Cantero-Martínez, Carlos

AU - Luster, Douglas

AU - Szabo, Les J

AU - Olivera, Pablo

AU - Berlin, Anna

AU - Rodriguez-Algaba, Julian

AU - Hovmøller, Mogens S.

AU - McIntosh, Robert

AU - Jin, Yue

N1 - Funding Information: The research was supported by the United States Department of Agriculture‐Agricultural Research Service, the Bill and Melinda Gates Foundation and the United Kingdom Department for International Development managed by Cornell University, USA, grant number: DGGW‐OPP1133199, and the State Research Agency (AEI), Spain, project PID2020‐118650RR‐C31. Thanks to Dr Fanny Álvaro for the initial observation and sampling of aecial infection on barberry. The assistance of Dr Joan Pedrol and Dr Rosario Fanlo (University of Lleida, Spain) in grass species identification is gratefully acknowledged. We thank the assistance of Amparo López Olmeda (Teruel Plant Health Service), Gloria Herrero Sánchez (Cereales Teruel Sociedad Cooperativa) and Vicente Lozano Herrera (farmer cereal producer). Meteorological data from the El Ballestero site (Albacete province) were kindly provided by Manuel Fernández. Data from surface cropping area of Aragón have been provided by Sección de estadística del Departamento de Agricultura, Ganadería y Medio Ambiente del Gobierno de Aragón (Silvia Quílez‐Domingo). The support of Daniel Gómez and Alberto Pastoriza (Herbarium curators in the Pyrenean Institute of Ecology, IPE‐CSIC, Jaca) is thankfully acknowledged. Technical assistance of Melissa Carter, Jerry Johnson and Kim‐Phuong Nguyen from USDA‐ARS is acknowledged. Dr Villegas acknowledges the contribution of the CERCA program (Generalitat de Catalunya, Spain). Funding Information: The research was supported by the United States Department of Agriculture-Agricultural Research Service, the Bill and Melinda Gates Foundation and the United Kingdom Department for International Development managed by Cornell University, USA, grant number: DGGW-OPP1133199, and the State Research Agency (AEI), Spain, project PID2020-118650RR-C31. Thanks to Dr Fanny ?lvaro for the initial observation and sampling of aecial infection on barberry. The assistance of Dr Joan Pedrol and Dr Rosario Fanlo (University of Lleida, Spain) in grass species identification is gratefully acknowledged. We thank the assistance of Amparo L?pez Olmeda (Teruel Plant Health Service), Gloria Herrero S?nchez (Cereales Teruel Sociedad Cooperativa) and Vicente Lozano Herrera (farmer cereal producer). Meteorological data from the El Ballestero site (Albacete province) were kindly provided by Manuel Fern?ndez. Data from surface cropping area of Arag?n have been provided by Secci?n de estad?stica del Departamento de Agricultura, Ganader?a y Medio Ambiente del Gobierno de Arag?n (Silvia Qu?lez-Domingo). The support of Daniel G?mez and Alberto Pastoriza (Herbarium curators in the Pyrenean Institute of Ecology, IPE-CSIC, Jaca) is thankfully acknowledged. Technical assistance of Melissa Carter, Jerry Johnson and Kim-Phuong Nguyen from USDA-ARS is acknowledged. Dr Villegas acknowledges the contribution of the CERCA program (Generalitat de Catalunya, Spain). Publisher Copyright: © 2022 The Authors. Plant Pathology published by John Wiley & Sons Ltd on behalf of British Society for Plant Pathology. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA

PY - 2022/6

Y1 - 2022/6

N2 - Stem rust, caused by Puccinia graminis, is a destructive group of diseases. The pathogen uses Berberis species as alternate hosts to complete its life cycle. B. vulgaris and the endemic species B. hispanica and B. garciae are present in Spain. The objective of this study was to investigate the functionality of the indigenous barberry as alternate hosts. Field surveys were conducted in 2018 and 2019 in Huesca, Teruel and Albacete provinces of Spain. Aecial samples on barberry were analysed via infection assays and DNA analysis. B. garciae was predominant in Huesca and Teruel provinces, often found in the field margins of cereal crops. Aecial infections on B. garciae were observed in May and uredinial infections on cereal crops in June. Scattered B. hispanica bushes were occasionally found near cereal crops in Albacete, where aecial infections on B. hispanica were observed in June when most cereal crops were mature. Infection assays using aeciospores resulted in stem rust infections on susceptible genotypes of wheat, barley, rye and oat, indicating the presence of the sexual cycle for P. graminis f. sp. tritici, f. sp. secalis and f. sp. avenae. Sequence analyses from aecial samples supported this finding as well as the presence of Puccinia brachypodii. This study provides the first evidence that indigenous Berberis species play an active role in the sexual cycle of P. graminis under natural conditions in Spain.

AB - Stem rust, caused by Puccinia graminis, is a destructive group of diseases. The pathogen uses Berberis species as alternate hosts to complete its life cycle. B. vulgaris and the endemic species B. hispanica and B. garciae are present in Spain. The objective of this study was to investigate the functionality of the indigenous barberry as alternate hosts. Field surveys were conducted in 2018 and 2019 in Huesca, Teruel and Albacete provinces of Spain. Aecial samples on barberry were analysed via infection assays and DNA analysis. B. garciae was predominant in Huesca and Teruel provinces, often found in the field margins of cereal crops. Aecial infections on B. garciae were observed in May and uredinial infections on cereal crops in June. Scattered B. hispanica bushes were occasionally found near cereal crops in Albacete, where aecial infections on B. hispanica were observed in June when most cereal crops were mature. Infection assays using aeciospores resulted in stem rust infections on susceptible genotypes of wheat, barley, rye and oat, indicating the presence of the sexual cycle for P. graminis f. sp. tritici, f. sp. secalis and f. sp. avenae. Sequence analyses from aecial samples supported this finding as well as the presence of Puccinia brachypodii. This study provides the first evidence that indigenous Berberis species play an active role in the sexual cycle of P. graminis under natural conditions in Spain.

KW - Berberis garciae

KW - Berberis hispanica

KW - aecial host

KW - sexual cycle

KW - stem rust

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UR - http://www.scopus.com/inward/citedby.url?scp=85126061163&partnerID=8YFLogxK

U2 - 10.1111/ppa.13540

DO - 10.1111/ppa.13540

M3 - Article

C2 - 35915821

AN - SCOPUS:85126061163

SN - 0032-0862

VL - 71

SP - 1174

EP - 1184

JO - Plant Pathology

JF - Plant Pathology

IS - 5

ER -

Barberry plays an active role as an alternate host of Puccinia graminis in Spain

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Bibliographical note

Keywords

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