Gapless genome assembly of Colletotrichum higginsianum reveals chromosome structure and association of transposable elements with secondary metabolite gene clusters

Dallery, Jean‐Félix; Lapalu, Nicolas; Zampounis, Antonios; Pigné, Sandrine; Luyten, Isabelle; Amselem, Joëlle; Wittenberg, Alexander H. J.; Zhou, Shiguo; Queiroz, Marisa Vieira de; Robin, Guillaume P.; Auger, Annie; Hainaut, Matthieu; Henrissat, Bernard; Kim, Ki-Tae; Lee, Yong-Hwan; Lespinet, Olivier; Schwartz, David C.; Thon, Michael R.; O’Connell, Richard J.

doi:10.1186/s12864-017-4083-x

Cited by 96 publications

(130 citation statements)

References 124 publications

(142 reference statements)

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“…The number of PKSs, NRPSs and hybrid PKS/NRPSs found in this study is in line with those found in other plant pathogenic fungi (25, compared with 31 in B. cinerea and 11 to 59 in eight other plant pathogens [36][37][38][39]…”

Section: Discussionsupporting

confidence: 89%

A detailed in silico analysis of secondary metabolite biosynthesis clusters in the genome of the broad host range plant pathogenic fungus Sclerotinia sclerotiorum

Graham-Taylor

Kamphuis

Derbyshire

2019

Preprint

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Sclerotiniaceae) is a broad host range pathogen that infects over 400 plant species and causes substantial yield losses in crops worldwide. Crops affected are mainly dicotyledonous plants including oilseed rape and other brassicas, sunflower, chickpea, soybean, peanut and lentils, as well as some monocotyledonous plants such as onion and tulip [1]. Like other members of the Sclerotiniaceae, S.sclerotiorum spends approximately 90% of its life cycle as sclerotia: melanised hyphal aggregates that can remain viable for up to eight years in the soil and that play a major role in the disease cycle [2,3]. Infection proceeds when sclerotia germinate either myceliogenically to directly infect a plant, or carpogenically to form an apothecium and disseminate ascospores [2]. After penetrating the plant cuticle S. sclerotiorum proliferates inside the host in a brief biotrophic phase (approximately 24 hours in Brassica napus (oilseed rape)) before commencing a necrotrophic phase in which it kills plant cells, then feeds off the dead tissue [4].The large host range of S. sclerotiorum, its ability to spread via wind dispersal and its persistence in the soil make this fungus a difficult pathogen to control. As a result, there is a need to better understand the molecular basis of S. sclerotiorum disease. One aspect of infection that has been little investigated in S. sclerotiorum is production of secondary metabolites: small, structurally diverse organic molecules that contribute to fungal growth and survival in diverse environments [5]. Secondary metabolites are synthesised by pathogenic fungi for defence, signalling, nutrient uptake and interfering with host cell structure and function [6]. Secondary metabolites that have been shown to contribute to the virulence of plant pathogenic fungi include siderophores, pigments and phytotoxins [7,8]. Although it may be argued that some pigments and siderophores are primary metabolites as they are essential for survival, we refer to them as secondary metabolites in this study as a disambiguation as they are produced by genes in families frequently involved in production of secondary metabolites sensu stricto.Siderophores are small, iron-chelating compounds used by fungi both to scavenge iron from the environment and to bind intracellular iron. Fungi require iron for many essential biochemical processes including respiration, the tricarboxylic acid cycle and the synthesis of deoxyribonucleotides,

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Section: Discussionsupporting

confidence: 89%

A detailed in silico analysis of secondary metabolite biosynthesis clusters in the genome of the broad host range plant pathogenic fungus Sclerotinia sclerotiorum

Graham-Taylor

Kamphuis

Derbyshire

2019

Preprint

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“…In contrast, broad host‐range necrotrophic fungal pathogens such as S. sclerotiorum and B. cinerea exhibit relatively repeat‐poor genomes (Derbyshire et al , ; Van Kan et al , ). Nevertheless, effector genes may also be associated with repeat sequences in necrotrophic fungi and fungi with a broad host range (Dallery et al , ; Laurent et al , ; Syme et al , ; Wang et al , ). Secretome analyses highlighted a number of candidate effector‐like proteins in the genome of S. sclerotiorum (Badet et al , ; Derbyshire et al , ; Guyon et al , ; Heard et al , ).…”

Section: Discussionmentioning

confidence: 99%

Small RNAs from the plant pathogenic fungus Sclerotinia sclerotiorum highlight host candidate genes associated with quantitative disease resistance

Derbyshire

Mbengue

Barascud

et al. 2019

Molecular Plant Pathology

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Summary Fungal plant pathogens secrete effector proteins and metabolites to cause disease. Additionally, some species transfer small RNAs (sRNAs) into plant cells to silence host mRNAs through complementary base pairing and suppress plant immunity. The fungus Sclerotinia sclerotiorum infects over 600 plant species, but little is known about the molecular processes that govern interactions with its many hosts. In particular, evidence for the production of sRNAs by S. sclerotiorum during infection is lacking. We sequenced sRNAs produced by S. sclerotiorum in vitro and during infection of two host species, Arabidopsis thaliana and Phaseolus vulgaris . We found that S. sclerotiorum produces at least 374 distinct highly abundant sRNAs during infection, mostly originating from repeat‐rich plastic genomic regions. We predicted the targets of these sRNAs in A. thaliana and found that these genes were significantly more down‐regulated during infection than the rest of the genome. Predicted targets of S. sclerotiorum sRNAs in A. thaliana were enriched for functional domains associated with plant immunity and were more strongly associated with quantitative disease resistance in a genome‐wide association study (GWAS) than the rest of the genome. Mutants in A. thaliana predicted sRNA target genes SERK2 and SNAK2 were more susceptible to S. sclerotiorum than wild‐type, suggesting that S. sclerotiorum sRNAs may contribute to the silencing of immune components in plants. The prediction of fungal sRNA targets in plant genomes can be combined with other global approaches, such as GWAS, to assist in the identification of plant genes involved in quantitative disease resistance.

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“…In Colletotrichum , transcriptome analysis revealed that the expression of several SM synthesis‐related genes is strongly induced during infection, especially at the biotrophic phase, in addition to effector proteins (Dallery et al. , ; Gan et al. , ).…”

Section: Discussionmentioning

confidence: 99%

Establishment of a selection marker recycling system for sequential transformation of the plant‐pathogenic fungus Colletotrichum orbiculare

Kumakura

Ueno

Shirasu

2018

Molecular Plant Pathology

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Summary Genome sequencing of pathogenic fungi has revealed the presence of various effectors that aid pathogen invasion by the manipulation of plant immunity. Effectors are often individually dispensable because of duplication and functional redundancy as a result of the arms race between host plants and pathogens. To study effectors that have functional redundancy, multiple gene disruption is often required. However, the number of selection markers that can be used for gene targeting is limited. Here, we established a marker recycling system that allows the use of the same selection marker in successive transformations in the model fungal pathogen Colletotrichum orbiculare , a causal agent of anthracnose disease in plants belonging to the Cucurbitaceae. We identified two C. orbiculare homologues of yeast URA3/pyrG , designated as URA3A and URA3B , which can be used as selection markers on medium with no uridine. The gene can then be removed from the genome via homologous recombination when the fungus is grown in the presence of 5‐fluoroorotic acid (5‐FOA), a chemical that is converted into a toxin by URA3 activity. The ura3a/b double mutants showed auxotrophy for uridine and insensitivity to 5‐FOA. Using the ura3a/b mutants, transformation with the URA3B marker and its removal were successfully applied to disrupt the virulence‐related gene, PKS1 . The pks1 mutants showed a reduction in virulence, demonstrating that the method can be used to study virulence‐related genes in C. orbiculare . The establishment of a URA3 ‐based marker recycling system in plant‐pathogenic fungi enables the genetic analysis of multiple genes that have redundant functions, including effector genes.

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Gapless genome assembly of Colletotrichum higginsianum reveals chromosome structure and association of transposable elements with secondary metabolite gene clusters

Cited by 96 publications

References 124 publications

A detailed in silico analysis of secondary metabolite biosynthesis clusters in the genome of the broad host range plant pathogenic fungus Sclerotinia sclerotiorum

A detailed in silico analysis of secondary metabolite biosynthesis clusters in the genome of the broad host range plant pathogenic fungus Sclerotinia sclerotiorum

Small RNAs from the plant pathogenic fungus Sclerotinia sclerotiorum highlight host candidate genes associated with quantitative disease resistance

Establishment of a selection marker recycling system for sequential transformation of the plant‐pathogenic fungus Colletotrichum orbiculare

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