Effector Repertoire of the Sweetpotato Black Rot Fungal Pathogen Ceratocystis fimbriata

In 2015, sweetpotato producers in the United States experienced one of the worst outbreaks of black rot recorded in history, with up to 60% losses reported in the field and packing houses and at shipping ports. Host resistance remains the ideal management tool to decrease crop losses. Lack of knowle...

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Main Authors: Camilo H. Parada-Rojas, Madison Stahr, Kevin L. Childs, Lina M. Quesada-Ocampo
Format: Article
Language:English
Published: The American Phytopathological Society 2024-03-01
Series:Molecular Plant-Microbe Interactions
Subjects:
Online Access:https://apsjournals.apsnet.org/doi/10.1094/MPMI-09-23-0146-FI
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author Camilo H. Parada-Rojas
Madison Stahr
Kevin L. Childs
Lina M. Quesada-Ocampo
author_facet Camilo H. Parada-Rojas
Madison Stahr
Kevin L. Childs
Lina M. Quesada-Ocampo
author_sort Camilo H. Parada-Rojas
collection DOAJ
description In 2015, sweetpotato producers in the United States experienced one of the worst outbreaks of black rot recorded in history, with up to 60% losses reported in the field and packing houses and at shipping ports. Host resistance remains the ideal management tool to decrease crop losses. Lack of knowledge of Ceratocystis fimbriata biology represents a critical barrier for the deployment of resistance to black rot in sweetpotato. In this study, we scanned the recent near chromosomal-level assembly for putative secreted effectors in the sweetpotato C. fimbriata isolate AS236 using a custom fungal effector annotation pipeline. We identified a set of 188 putative effectors on the basis of secretion signal and in silico prediction in EffectorP. We conducted a deep RNA time-course sequencing experiment to determine whether C. fimbriata modulates effectors in planta and to define a candidate list of effectors expressed during infection. We examined the expression profile of two C. fimbriata isolates, a pre-epidemic (1990s) isolate and a post-epidemic (2015) isolate. Our in planta expression profiling revealed clusters of co-expressed secreted effector candidates. Based on fold-change differences of putative effectors in both isolates and over the course of infection, we suggested prioritization of 31 effectors for functional characterization. Among this set, we identified several effectors that provide evidence for a marked biotrophic phase in C. fimbriata during infection of sweetpotato storage roots. Our study revealed a catalog of effector proteins that provide insight into C. fimbriata infection mechanisms and represent a core catalog to implement effector-assisted breeding in sweetpotato. [Graphic: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.
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spelling doaj.art-d53f9ed0d2b846329f5c4c699edd129d2024-04-04T17:01:39ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062024-03-0137331532610.1094/MPMI-09-23-0146-FIEffector Repertoire of the Sweetpotato Black Rot Fungal Pathogen Ceratocystis fimbriataCamilo H. Parada-Rojas0Madison Stahr1Kevin L. Childs2Lina M. Quesada-Ocampo3Department of Entomology and Plant Pathology and NC Plant Sciences Initiative, North Carolina State University, Raleigh, NC 27606, U.S.A.Department of Entomology and Plant Pathology and NC Plant Sciences Initiative, North Carolina State University, Raleigh, NC 27606, U.S.A.Department of Plant Biology, Michigan State University, East Lansing, MI 48824, U.S.A.Department of Entomology and Plant Pathology and NC Plant Sciences Initiative, North Carolina State University, Raleigh, NC 27606, U.S.A.In 2015, sweetpotato producers in the United States experienced one of the worst outbreaks of black rot recorded in history, with up to 60% losses reported in the field and packing houses and at shipping ports. Host resistance remains the ideal management tool to decrease crop losses. Lack of knowledge of Ceratocystis fimbriata biology represents a critical barrier for the deployment of resistance to black rot in sweetpotato. In this study, we scanned the recent near chromosomal-level assembly for putative secreted effectors in the sweetpotato C. fimbriata isolate AS236 using a custom fungal effector annotation pipeline. We identified a set of 188 putative effectors on the basis of secretion signal and in silico prediction in EffectorP. We conducted a deep RNA time-course sequencing experiment to determine whether C. fimbriata modulates effectors in planta and to define a candidate list of effectors expressed during infection. We examined the expression profile of two C. fimbriata isolates, a pre-epidemic (1990s) isolate and a post-epidemic (2015) isolate. Our in planta expression profiling revealed clusters of co-expressed secreted effector candidates. Based on fold-change differences of putative effectors in both isolates and over the course of infection, we suggested prioritization of 31 effectors for functional characterization. Among this set, we identified several effectors that provide evidence for a marked biotrophic phase in C. fimbriata during infection of sweetpotato storage roots. Our study revealed a catalog of effector proteins that provide insight into C. fimbriata infection mechanisms and represent a core catalog to implement effector-assisted breeding in sweetpotato. [Graphic: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.https://apsjournals.apsnet.org/doi/10.1094/MPMI-09-23-0146-FICeratocystis fimbriataeffectorsin plantaplant immunitysweetpotato
spellingShingle Camilo H. Parada-Rojas
Madison Stahr
Kevin L. Childs
Lina M. Quesada-Ocampo
Effector Repertoire of the Sweetpotato Black Rot Fungal Pathogen Ceratocystis fimbriata
Molecular Plant-Microbe Interactions
Ceratocystis fimbriata
effectors
in planta
plant immunity
sweetpotato
title Effector Repertoire of the Sweetpotato Black Rot Fungal Pathogen Ceratocystis fimbriata
title_full Effector Repertoire of the Sweetpotato Black Rot Fungal Pathogen Ceratocystis fimbriata
title_fullStr Effector Repertoire of the Sweetpotato Black Rot Fungal Pathogen Ceratocystis fimbriata
title_full_unstemmed Effector Repertoire of the Sweetpotato Black Rot Fungal Pathogen Ceratocystis fimbriata
title_short Effector Repertoire of the Sweetpotato Black Rot Fungal Pathogen Ceratocystis fimbriata
title_sort effector repertoire of the sweetpotato black rot fungal pathogen ceratocystis fimbriata
topic Ceratocystis fimbriata
effectors
in planta
plant immunity
sweetpotato
url https://apsjournals.apsnet.org/doi/10.1094/MPMI-09-23-0146-FI
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