Down-regulation of cladofulvin biosynthesis is required for biotrophic growth of Cladosporium fulvum on tomato

A secondary metabolite prevents fungal biotrophy

Scott Griffiths, Carl H. Mesarich, Elysa J.R. Overdijk, Benedetta Saccomanno, Pierre J.G.M. De Wit, Jérôme Collemare

Research output: Contribution to journalArticleAcademicpeer-review

6 Citations (Scopus)

Abstract

Fungal biotrophy is associated with a reduced capacity to produce potentially toxic secondary metabolites (SMs). Yet, the genome of the biotrophic plant pathogen Cladosporium fulvum contains many SM biosynthetic gene clusters, with several related to toxin production. These gene clusters are, however, poorly expressed during colonisation of tomato. The sole detectable SM produced by C. fulvum during in vitro growth is the anthraquinone cladofulvin. Although this pigment is not detected in infected leaves, cladofulvin biosynthetic genes are expressed throughout the pre-penetration phase and during conidiation at the end of the infection cycle, but they are repressed during the biotrophic phase of tomato colonization. It was suggested that tight regulation of SM gene clusters is required for C. fulvum to behave as a biotrophic pathogen, while retaining potential fitness determinants for growth and survival outside its host. To address this hypothesis, we analysed the disease symptoms caused by mutant C. fulvum strains that do not produce or over-produce cladofulvin during the biotrophic growth phase. Non-producers infected tomato similar to wild type, suggesting that cladofulvin is not a virulence factor. In contrast, the cladofulvin over-producers caused strong necrosis and desiccation of tomato leaves, which in turn, arrested conidiation. Consistent with the role of pigments in survival against abiotic stresses, cladofulvin protects conidia against UV light and low temperature stress. Overall this study demonstrates that repression of cladofulvin production is required for C. fulvum to sustain its biotrophic lifestyle in tomato, while its production is important for survival outside its host.
Original languageEnglish
Pages (from-to)369-380
JournalMolecular Plant Pathology
Volume19
Issue number2
Early online date20 Dec 2016
DOIs
Publication statusPublished - 25 Jan 2018

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Passalora fulva
Cladosporium
secondary metabolite
Lycopersicon esculentum
secondary metabolites
Down-Regulation
tomatoes
biosynthesis
Multigene Family
multigene family
gene
Growth
disease by symptom
pigment
colonization
pathogen
pigments
Plant Genome
virulence
Desiccation

Cite this

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title = "Down-regulation of cladofulvin biosynthesis is required for biotrophic growth of Cladosporium fulvum on tomato: A secondary metabolite prevents fungal biotrophy",
abstract = "Fungal biotrophy is associated with a reduced capacity to produce potentially toxic secondary metabolites (SMs). Yet, the genome of the biotrophic plant pathogen Cladosporium fulvum contains many SM biosynthetic gene clusters, with several related to toxin production. These gene clusters are, however, poorly expressed during colonisation of tomato. The sole detectable SM produced by C. fulvum during in vitro growth is the anthraquinone cladofulvin. Although this pigment is not detected in infected leaves, cladofulvin biosynthetic genes are expressed throughout the pre-penetration phase and during conidiation at the end of the infection cycle, but they are repressed during the biotrophic phase of tomato colonization. It was suggested that tight regulation of SM gene clusters is required for C. fulvum to behave as a biotrophic pathogen, while retaining potential fitness determinants for growth and survival outside its host. To address this hypothesis, we analysed the disease symptoms caused by mutant C. fulvum strains that do not produce or over-produce cladofulvin during the biotrophic growth phase. Non-producers infected tomato similar to wild type, suggesting that cladofulvin is not a virulence factor. In contrast, the cladofulvin over-producers caused strong necrosis and desiccation of tomato leaves, which in turn, arrested conidiation. Consistent with the role of pigments in survival against abiotic stresses, cladofulvin protects conidia against UV light and low temperature stress. Overall this study demonstrates that repression of cladofulvin production is required for C. fulvum to sustain its biotrophic lifestyle in tomato, while its production is important for survival outside its host.",
author = "Scott Griffiths and Mesarich, {Carl H.} and Overdijk, {Elysa J.R.} and Benedetta Saccomanno and {De Wit}, {Pierre J.G.M.} and J{\'e}r{\^o}me Collemare",
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Down-regulation of cladofulvin biosynthesis is required for biotrophic growth of Cladosporium fulvum on tomato : A secondary metabolite prevents fungal biotrophy. / Griffiths, Scott; Mesarich, Carl H.; Overdijk, Elysa J.R.; Saccomanno, Benedetta; De Wit, Pierre J.G.M.; Collemare, Jérôme.

In: Molecular Plant Pathology, Vol. 19, No. 2, 25.01.2018, p. 369-380.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Down-regulation of cladofulvin biosynthesis is required for biotrophic growth of Cladosporium fulvum on tomato

T2 - A secondary metabolite prevents fungal biotrophy

AU - Griffiths, Scott

AU - Mesarich, Carl H.

AU - Overdijk, Elysa J.R.

AU - Saccomanno, Benedetta

AU - De Wit, Pierre J.G.M.

AU - Collemare, Jérôme

PY - 2018/1/25

Y1 - 2018/1/25

N2 - Fungal biotrophy is associated with a reduced capacity to produce potentially toxic secondary metabolites (SMs). Yet, the genome of the biotrophic plant pathogen Cladosporium fulvum contains many SM biosynthetic gene clusters, with several related to toxin production. These gene clusters are, however, poorly expressed during colonisation of tomato. The sole detectable SM produced by C. fulvum during in vitro growth is the anthraquinone cladofulvin. Although this pigment is not detected in infected leaves, cladofulvin biosynthetic genes are expressed throughout the pre-penetration phase and during conidiation at the end of the infection cycle, but they are repressed during the biotrophic phase of tomato colonization. It was suggested that tight regulation of SM gene clusters is required for C. fulvum to behave as a biotrophic pathogen, while retaining potential fitness determinants for growth and survival outside its host. To address this hypothesis, we analysed the disease symptoms caused by mutant C. fulvum strains that do not produce or over-produce cladofulvin during the biotrophic growth phase. Non-producers infected tomato similar to wild type, suggesting that cladofulvin is not a virulence factor. In contrast, the cladofulvin over-producers caused strong necrosis and desiccation of tomato leaves, which in turn, arrested conidiation. Consistent with the role of pigments in survival against abiotic stresses, cladofulvin protects conidia against UV light and low temperature stress. Overall this study demonstrates that repression of cladofulvin production is required for C. fulvum to sustain its biotrophic lifestyle in tomato, while its production is important for survival outside its host.

AB - Fungal biotrophy is associated with a reduced capacity to produce potentially toxic secondary metabolites (SMs). Yet, the genome of the biotrophic plant pathogen Cladosporium fulvum contains many SM biosynthetic gene clusters, with several related to toxin production. These gene clusters are, however, poorly expressed during colonisation of tomato. The sole detectable SM produced by C. fulvum during in vitro growth is the anthraquinone cladofulvin. Although this pigment is not detected in infected leaves, cladofulvin biosynthetic genes are expressed throughout the pre-penetration phase and during conidiation at the end of the infection cycle, but they are repressed during the biotrophic phase of tomato colonization. It was suggested that tight regulation of SM gene clusters is required for C. fulvum to behave as a biotrophic pathogen, while retaining potential fitness determinants for growth and survival outside its host. To address this hypothesis, we analysed the disease symptoms caused by mutant C. fulvum strains that do not produce or over-produce cladofulvin during the biotrophic growth phase. Non-producers infected tomato similar to wild type, suggesting that cladofulvin is not a virulence factor. In contrast, the cladofulvin over-producers caused strong necrosis and desiccation of tomato leaves, which in turn, arrested conidiation. Consistent with the role of pigments in survival against abiotic stresses, cladofulvin protects conidia against UV light and low temperature stress. Overall this study demonstrates that repression of cladofulvin production is required for C. fulvum to sustain its biotrophic lifestyle in tomato, while its production is important for survival outside its host.

U2 - 10.1111/mpp.12527

DO - 10.1111/mpp.12527

M3 - Article

VL - 19

SP - 369

EP - 380

JO - Molecular Plant Pathology

JF - Molecular Plant Pathology

SN - 1464-6722

IS - 2

ER -