Effectors with Different Gears: Divergence of <i>Ustilago maydis</i> Effector Genes Is Associated with Their Temporal Expression Pattern during Plant Infection

Plant pathogens secrete a variety of effector proteins that enable host colonization but are also typical pathogen detection targets for the host immune system. Consequently, effector genes encounter high selection pressures, which typically makes them fast evolving. The corn smut pathogen <i>...

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Main Authors: Jasper R. L. Depotter, Weiliang Zuo, Maike Hansen, Boqi Zhang, Mingliang Xu, Gunther Doehlemann
Format: Article
Language:English
Published: MDPI AG 2020-12-01
Series:Journal of Fungi
Subjects:
Online Access:https://www.mdpi.com/2309-608X/7/1/16
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author Jasper R. L. Depotter
Weiliang Zuo
Maike Hansen
Boqi Zhang
Mingliang Xu
Gunther Doehlemann
author_facet Jasper R. L. Depotter
Weiliang Zuo
Maike Hansen
Boqi Zhang
Mingliang Xu
Gunther Doehlemann
author_sort Jasper R. L. Depotter
collection DOAJ
description Plant pathogens secrete a variety of effector proteins that enable host colonization but are also typical pathogen detection targets for the host immune system. Consequently, effector genes encounter high selection pressures, which typically makes them fast evolving. The corn smut pathogen <i>Ustilago maydis</i> has an effector gene repertoire with a dynamic expression across the different disease stages. We determined the amino acid divergence of <i>U. maydis</i> effector candidates with <i>Sporisorium reilianum</i> orthologs, a close relative of <i>U. maydis</i>. Intriguingly, there are two distinct groups of effector candidates, ones with a respective conserved and diverged protein evolution. Conservatively evolving effector genes especially have their peak expression during the (pre-)penetration stages of the disease cycle. In contrast, expression of divergently evolving effector genes generally peaks during fungal proliferation within the host. To test if this interspecific effector diversity corresponds to intraspecific diversity, we sampled and sequenced a diverse collection of <i>U. maydis</i> strains from the most important maize breeding and production regions in China. Effector candidates with a diverged interspecific evolution had more intraspecific amino acid variation than candidates with a conserved evolution. In conclusion, we highlight diversity in evolution within the <i>U. maydis</i> effector repertoire with dynamically and conservatively evolving members.
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spelling doaj.art-5275fe7762d9403c8101855c2a0c6a322023-11-21T03:01:51ZengMDPI AGJournal of Fungi2309-608X2020-12-01711610.3390/jof7010016Effectors with Different Gears: Divergence of <i>Ustilago maydis</i> Effector Genes Is Associated with Their Temporal Expression Pattern during Plant InfectionJasper R. L. Depotter0Weiliang Zuo1Maike Hansen2Boqi Zhang3Mingliang Xu4Gunther Doehlemann5Institute for Plant Sciences, University of Cologne, CEPLAS, D-50674 Cologne, GermanyInstitute for Plant Sciences, University of Cologne, CEPLAS, D-50674 Cologne, GermanyInstitute for Plant Sciences, University of Cologne, CEPLAS, D-50674 Cologne, GermanyNational Maize Improvement Centre of China, China Agricultural University, Beijing 100193, ChinaNational Maize Improvement Centre of China, China Agricultural University, Beijing 100193, ChinaInstitute for Plant Sciences, University of Cologne, CEPLAS, D-50674 Cologne, GermanyPlant pathogens secrete a variety of effector proteins that enable host colonization but are also typical pathogen detection targets for the host immune system. Consequently, effector genes encounter high selection pressures, which typically makes them fast evolving. The corn smut pathogen <i>Ustilago maydis</i> has an effector gene repertoire with a dynamic expression across the different disease stages. We determined the amino acid divergence of <i>U. maydis</i> effector candidates with <i>Sporisorium reilianum</i> orthologs, a close relative of <i>U. maydis</i>. Intriguingly, there are two distinct groups of effector candidates, ones with a respective conserved and diverged protein evolution. Conservatively evolving effector genes especially have their peak expression during the (pre-)penetration stages of the disease cycle. In contrast, expression of divergently evolving effector genes generally peaks during fungal proliferation within the host. To test if this interspecific effector diversity corresponds to intraspecific diversity, we sampled and sequenced a diverse collection of <i>U. maydis</i> strains from the most important maize breeding and production regions in China. Effector candidates with a diverged interspecific evolution had more intraspecific amino acid variation than candidates with a conserved evolution. In conclusion, we highlight diversity in evolution within the <i>U. maydis</i> effector repertoire with dynamically and conservatively evolving members.https://www.mdpi.com/2309-608X/7/1/16effector repertoire<i>Sporisorium</i>evolutionary arms racesmut pathogen<i>Ustilago</i>
spellingShingle Jasper R. L. Depotter
Weiliang Zuo
Maike Hansen
Boqi Zhang
Mingliang Xu
Gunther Doehlemann
Effectors with Different Gears: Divergence of <i>Ustilago maydis</i> Effector Genes Is Associated with Their Temporal Expression Pattern during Plant Infection
Journal of Fungi
effector repertoire
<i>Sporisorium</i>
evolutionary arms race
smut pathogen
<i>Ustilago</i>
title Effectors with Different Gears: Divergence of <i>Ustilago maydis</i> Effector Genes Is Associated with Their Temporal Expression Pattern during Plant Infection
title_full Effectors with Different Gears: Divergence of <i>Ustilago maydis</i> Effector Genes Is Associated with Their Temporal Expression Pattern during Plant Infection
title_fullStr Effectors with Different Gears: Divergence of <i>Ustilago maydis</i> Effector Genes Is Associated with Their Temporal Expression Pattern during Plant Infection
title_full_unstemmed Effectors with Different Gears: Divergence of <i>Ustilago maydis</i> Effector Genes Is Associated with Their Temporal Expression Pattern during Plant Infection
title_short Effectors with Different Gears: Divergence of <i>Ustilago maydis</i> Effector Genes Is Associated with Their Temporal Expression Pattern during Plant Infection
title_sort effectors with different gears divergence of i ustilago maydis i effector genes is associated with their temporal expression pattern during plant infection
topic effector repertoire
<i>Sporisorium</i>
evolutionary arms race
smut pathogen
<i>Ustilago</i>
url https://www.mdpi.com/2309-608X/7/1/16
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