Wheat Encodes Small, Secreted Proteins That Contribute to Resistance to Septoria Tritici Blotch

During plant–pathogen interactions, pathogens secrete many rapidly evolving, small secreted proteins (SSPs) that can modify plant defense and permit pathogens to colonize plant tissue. The fungal pathogen Zymoseptoria tritici is the causal agent of Septoria tritici blotch (STB), one of the most impo...

Full description

Bibliographic Details
Main Authors: Binbin Zhou, Harriet R. Benbow, Ciarán J. Brennan, Chanemougasoundharam Arunachalam, Sujit J. Karki, Ewen Mullins, Angela Feechan, James I. Burke, Fiona M. Doohan
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-05-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fgene.2020.00469/full
id doaj-32bf41884cb343ada4dde97abd947f9c
record_format Article
spelling doaj-32bf41884cb343ada4dde97abd947f9c2020-11-25T03:02:48ZengFrontiers Media S.A.Frontiers in Genetics1664-80212020-05-011110.3389/fgene.2020.00469537573Wheat Encodes Small, Secreted Proteins That Contribute to Resistance to Septoria Tritici BlotchBinbin Zhou0Harriet R. Benbow1Ciarán J. Brennan2Chanemougasoundharam Arunachalam3Sujit J. Karki4Ewen Mullins5Angela Feechan6James I. Burke7Fiona M. Doohan8UCD School of Biology and Environmental Science, UCD Earth Institute, UCD O’Brien Centre for Science (East), University College Dublin, Dublin, IrelandUCD School of Biology and Environmental Science, UCD Earth Institute, UCD O’Brien Centre for Science (East), University College Dublin, Dublin, IrelandUCD School of Biology and Environmental Science, UCD Earth Institute, UCD O’Brien Centre for Science (East), University College Dublin, Dublin, IrelandUCD School of Biology and Environmental Science, UCD Earth Institute, UCD O’Brien Centre for Science (East), University College Dublin, Dublin, IrelandUCD School of Agriculture and Food Science, University College Dublin, Dublin, IrelandDepartment of Crop Science, Teagasc, Carlow, IrelandUCD School of Agriculture and Food Science, University College Dublin, Dublin, IrelandUCD School of Agriculture and Food Science, University College Dublin, Dublin, IrelandUCD School of Biology and Environmental Science, UCD Earth Institute, UCD O’Brien Centre for Science (East), University College Dublin, Dublin, IrelandDuring plant–pathogen interactions, pathogens secrete many rapidly evolving, small secreted proteins (SSPs) that can modify plant defense and permit pathogens to colonize plant tissue. The fungal pathogen Zymoseptoria tritici is the causal agent of Septoria tritici blotch (STB), one of the most important foliar diseases of wheat, globally. Z. tritici is a strictly apoplastic pathogen that can secrete numerous proteins into the apoplast of wheat leaves to promote infection. We sought to determine if, during STB infection, wheat also secretes small proteins into the apoplast to mediate the recognition of pathogen proteins and/or induce defense responses. To explore this, we developed an SSP-discovery pipeline to identify small, secreted proteins from wheat genomic data. Using this pipeline, we identified 6,998 SSPs, representing 2.3% of all proteins encoded by the wheat genome. We then mined a microarray dataset, detailing a resistant and susceptible host response to STB, and identified 141 Z. tritici- responsive SSPs, representing 4.7% of all proteins encoded by Z. tritici – responsive genes. We demonstrate that a subset of these SSPs have a functional signal peptide and can interact with Z. tritici SSPs. Transiently silencing two of these wheat SSPs using virus-induced gene silencing (VIGS) shows an increase in susceptibility to STB, confirming their role in defense against Z. tritici.https://www.frontiersin.org/article/10.3389/fgene.2020.00469/fullSeptoria tritici blotch (STB)Zymoseptoria triticismall secreted proteins (SSPs)wheat disease resistanceapoplastic proteinsprotein secretion
collection DOAJ
language English
format Article
sources DOAJ
author Binbin Zhou
Harriet R. Benbow
Ciarán J. Brennan
Chanemougasoundharam Arunachalam
Sujit J. Karki
Ewen Mullins
Angela Feechan
James I. Burke
Fiona M. Doohan
spellingShingle Binbin Zhou
Harriet R. Benbow
Ciarán J. Brennan
Chanemougasoundharam Arunachalam
Sujit J. Karki
Ewen Mullins
Angela Feechan
James I. Burke
Fiona M. Doohan
Wheat Encodes Small, Secreted Proteins That Contribute to Resistance to Septoria Tritici Blotch
Frontiers in Genetics
Septoria tritici blotch (STB)
Zymoseptoria tritici
small secreted proteins (SSPs)
wheat disease resistance
apoplastic proteins
protein secretion
author_facet Binbin Zhou
Harriet R. Benbow
Ciarán J. Brennan
Chanemougasoundharam Arunachalam
Sujit J. Karki
Ewen Mullins
Angela Feechan
James I. Burke
Fiona M. Doohan
author_sort Binbin Zhou
title Wheat Encodes Small, Secreted Proteins That Contribute to Resistance to Septoria Tritici Blotch
title_short Wheat Encodes Small, Secreted Proteins That Contribute to Resistance to Septoria Tritici Blotch
title_full Wheat Encodes Small, Secreted Proteins That Contribute to Resistance to Septoria Tritici Blotch
title_fullStr Wheat Encodes Small, Secreted Proteins That Contribute to Resistance to Septoria Tritici Blotch
title_full_unstemmed Wheat Encodes Small, Secreted Proteins That Contribute to Resistance to Septoria Tritici Blotch
title_sort wheat encodes small, secreted proteins that contribute to resistance to septoria tritici blotch
publisher Frontiers Media S.A.
series Frontiers in Genetics
issn 1664-8021
publishDate 2020-05-01
description During plant–pathogen interactions, pathogens secrete many rapidly evolving, small secreted proteins (SSPs) that can modify plant defense and permit pathogens to colonize plant tissue. The fungal pathogen Zymoseptoria tritici is the causal agent of Septoria tritici blotch (STB), one of the most important foliar diseases of wheat, globally. Z. tritici is a strictly apoplastic pathogen that can secrete numerous proteins into the apoplast of wheat leaves to promote infection. We sought to determine if, during STB infection, wheat also secretes small proteins into the apoplast to mediate the recognition of pathogen proteins and/or induce defense responses. To explore this, we developed an SSP-discovery pipeline to identify small, secreted proteins from wheat genomic data. Using this pipeline, we identified 6,998 SSPs, representing 2.3% of all proteins encoded by the wheat genome. We then mined a microarray dataset, detailing a resistant and susceptible host response to STB, and identified 141 Z. tritici- responsive SSPs, representing 4.7% of all proteins encoded by Z. tritici – responsive genes. We demonstrate that a subset of these SSPs have a functional signal peptide and can interact with Z. tritici SSPs. Transiently silencing two of these wheat SSPs using virus-induced gene silencing (VIGS) shows an increase in susceptibility to STB, confirming their role in defense against Z. tritici.
topic Septoria tritici blotch (STB)
Zymoseptoria tritici
small secreted proteins (SSPs)
wheat disease resistance
apoplastic proteins
protein secretion
url https://www.frontiersin.org/article/10.3389/fgene.2020.00469/full
work_keys_str_mv AT binbinzhou wheatencodessmallsecretedproteinsthatcontributetoresistancetoseptoriatriticiblotch
AT harrietrbenbow wheatencodessmallsecretedproteinsthatcontributetoresistancetoseptoriatriticiblotch
AT ciaranjbrennan wheatencodessmallsecretedproteinsthatcontributetoresistancetoseptoriatriticiblotch
AT chanemougasoundharamarunachalam wheatencodessmallsecretedproteinsthatcontributetoresistancetoseptoriatriticiblotch
AT sujitjkarki wheatencodessmallsecretedproteinsthatcontributetoresistancetoseptoriatriticiblotch
AT ewenmullins wheatencodessmallsecretedproteinsthatcontributetoresistancetoseptoriatriticiblotch
AT angelafeechan wheatencodessmallsecretedproteinsthatcontributetoresistancetoseptoriatriticiblotch
AT jamesiburke wheatencodessmallsecretedproteinsthatcontributetoresistancetoseptoriatriticiblotch
AT fionamdoohan wheatencodessmallsecretedproteinsthatcontributetoresistancetoseptoriatriticiblotch
_version_ 1724688289525399552