Unrelated Fungal Rust Candidate Effectors Act on Overlapping Plant Functions

Rust fungi cause epidemics that threaten the production of important plant species, such as wheat and soy. <i>Melampsora larici-populina</i> (<i>Mlp</i>) causes the poplar rust and encodes at least 1184 candidate effectors (CEs) whose functions are poorly known. In this study...

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Main Authors: Karen Cristine Goncalves dos Santos, Gervais Pelletier, Armand Séguin, François Guillemette, Jeffrey Hawkes, Isabel Desgagné-Penix, Hugo Germain
Format: Article
Language:English
Published: MDPI AG 2021-05-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/9/5/996
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spelling doaj-7c023d8e310344188b9ed489c0aac4312021-05-31T23:14:19ZengMDPI AGMicroorganisms2076-26072021-05-01999699610.3390/microorganisms9050996Unrelated Fungal Rust Candidate Effectors Act on Overlapping Plant FunctionsKaren Cristine Goncalves dos Santos0Gervais Pelletier1Armand Séguin2François Guillemette3Jeffrey Hawkes4Isabel Desgagné-Penix5Hugo Germain6Department of Chemistry, Biochemistry and Physics, Université du Québec à Trois-Rivières, Trois-Rivières, QC G9A 5H9, CanadaNatural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Quebec City, QC G1V 4C7, CanadaNatural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Quebec City, QC G1V 4C7, CanadaCentre for Research on Aquatic Ecosystem Interactions (RIVE), Université du Québec à Trois-Rivières, Trois-Rivières, QC G8Z 1V3, CanadaDepartment of Chemistry—BMC, Analytical Chemistry, Uppsala University, VJ2J+92 Uppsala, SwedenDepartment of Chemistry, Biochemistry and Physics, Université du Québec à Trois-Rivières, Trois-Rivières, QC G9A 5H9, CanadaDepartment of Chemistry, Biochemistry and Physics, Université du Québec à Trois-Rivières, Trois-Rivières, QC G9A 5H9, CanadaRust fungi cause epidemics that threaten the production of important plant species, such as wheat and soy. <i>Melampsora larici-populina</i> (<i>Mlp</i>) causes the poplar rust and encodes at least 1184 candidate effectors (CEs) whose functions are poorly known. In this study, we sequenced the transcriptome and used mass spectrometry to analyze the metabolome of <i>Arabidopsis</i> plants constitutively expressing 14 <i>Mlp</i> CEs and of a control line to discover alterations leading to plant susceptibility. We found 2299 deregulated genes across the experiment. Genes involved in pattern-triggered immunity, such as FRK1, PR1, RBOHD, and WRKY33, as well as AUX/IAA genes were down-regulated. We further observed that 680 metabolites were deregulated in at least one CE-expressing transgenic line, with “highly unsaturated and phenolic compounds” and “peptides” enriched among down- and up-regulated metabolites. Interestingly, transgenic lines expressing unrelated CEs had correlated patterns of gene and metabolite deregulation, while expression of CEs belonging to the same family deregulated different genes and metabolites. Thus, our results uncouple effector sequence similarity and function. This supports that effector functional investigation in the context of their virulence activity and effect on plant susceptibility requires the investigation of the individual effector and precludes generalization based on sequence similarity.https://www.mdpi.com/2076-2607/9/5/996transcriptomemetabolomeplant-microbe interactionsrust fungieffector biology<i>Melampsora larici-populina</i>
collection DOAJ
language English
format Article
sources DOAJ
author Karen Cristine Goncalves dos Santos
Gervais Pelletier
Armand Séguin
François Guillemette
Jeffrey Hawkes
Isabel Desgagné-Penix
Hugo Germain
spellingShingle Karen Cristine Goncalves dos Santos
Gervais Pelletier
Armand Séguin
François Guillemette
Jeffrey Hawkes
Isabel Desgagné-Penix
Hugo Germain
Unrelated Fungal Rust Candidate Effectors Act on Overlapping Plant Functions
Microorganisms
transcriptome
metabolome
plant-microbe interactions
rust fungi
effector biology
<i>Melampsora larici-populina</i>
author_facet Karen Cristine Goncalves dos Santos
Gervais Pelletier
Armand Séguin
François Guillemette
Jeffrey Hawkes
Isabel Desgagné-Penix
Hugo Germain
author_sort Karen Cristine Goncalves dos Santos
title Unrelated Fungal Rust Candidate Effectors Act on Overlapping Plant Functions
title_short Unrelated Fungal Rust Candidate Effectors Act on Overlapping Plant Functions
title_full Unrelated Fungal Rust Candidate Effectors Act on Overlapping Plant Functions
title_fullStr Unrelated Fungal Rust Candidate Effectors Act on Overlapping Plant Functions
title_full_unstemmed Unrelated Fungal Rust Candidate Effectors Act on Overlapping Plant Functions
title_sort unrelated fungal rust candidate effectors act on overlapping plant functions
publisher MDPI AG
series Microorganisms
issn 2076-2607
publishDate 2021-05-01
description Rust fungi cause epidemics that threaten the production of important plant species, such as wheat and soy. <i>Melampsora larici-populina</i> (<i>Mlp</i>) causes the poplar rust and encodes at least 1184 candidate effectors (CEs) whose functions are poorly known. In this study, we sequenced the transcriptome and used mass spectrometry to analyze the metabolome of <i>Arabidopsis</i> plants constitutively expressing 14 <i>Mlp</i> CEs and of a control line to discover alterations leading to plant susceptibility. We found 2299 deregulated genes across the experiment. Genes involved in pattern-triggered immunity, such as FRK1, PR1, RBOHD, and WRKY33, as well as AUX/IAA genes were down-regulated. We further observed that 680 metabolites were deregulated in at least one CE-expressing transgenic line, with “highly unsaturated and phenolic compounds” and “peptides” enriched among down- and up-regulated metabolites. Interestingly, transgenic lines expressing unrelated CEs had correlated patterns of gene and metabolite deregulation, while expression of CEs belonging to the same family deregulated different genes and metabolites. Thus, our results uncouple effector sequence similarity and function. This supports that effector functional investigation in the context of their virulence activity and effect on plant susceptibility requires the investigation of the individual effector and precludes generalization based on sequence similarity.
topic transcriptome
metabolome
plant-microbe interactions
rust fungi
effector biology
<i>Melampsora larici-populina</i>
url https://www.mdpi.com/2076-2607/9/5/996
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