Polyketide synthases of  Diaporthe helianthi  and involvement of  DhPKS1  in virulence on sunflower

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Abstract

Background

The early phases of Diaporthe helianthi pathogenesis on sunflower are characterized by the production of phytotoxins that may play a role in host colonisation. In previous studies, phytotoxins of a polyketidic nature were isolated and purified from culture filtrates of virulent strains of D. helianthi isolated from sunflower. A highly aggressive isolate (7/96) from France contained a gene fragment of a putative nonaketide synthase ( lovB) which was conserved in a virulent D. helianthi population.

Results

In order to investigate the role of polyketide synthases in D. helianthi 7/96, a draft genome of this isolate was examined. We were able to find and phylogenetically analyse 40 genes putatively coding for polyketide synthases (PKSs). Analysis of their domains revealed that most PKS genes of D. helianthi are reducing PKSs, whereas only eight lacked reducing domains. Most of the identified PKSs have orthologs shown to be virulence factors or genetic determinants for toxin production in other pathogenic fungi. One of the genes ( DhPKS1) corresponded to the previously cloned D. helianthi lovB gene fragment and clustered with a nonribosomal peptide synthetase (NRPS) -PKS hybrid/lovastatin nonaketide like A. nidulans LovB. We used DhPKS1 as a case study and carried out its disruption through Agrobacterium-mediated transformation in the isolate 7/96. D. helianthi DhPKS1 deleted mutants were less virulent to sunflower compared to the wild type, indicating a role for this gene in the pathogenesis of the fungus.

Conclusion

The PKS sequences analysed and reported here constitute a new genomic resource that will be useful for further research on the biology, ecology and evolution of D. helianthi and generally of fungal plant pathogens.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-017-4405-z) contains supplementary material, which is available to authorized users.

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Most cited references 60

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Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans.

Volker Schroeckh, Kirstin Scherlach, Hans-Wilhelm Nützmann … (2009)

Fungi produce numerous low molecular weight molecules endowed with a multitude of biological activities. However, mining the full-genome sequences of fungi indicates that their potential to produce secondary metabolites is greatly underestimated. Because most of the biosynthesis gene clusters are silent under laboratory conditions, one of the major challenges is to understand the physiological conditions under which these genes are activated. Thus, we cocultivated the important model fungus Aspergillus nidulans with a collection of 58 soil-dwelling actinomycetes. By microarray analyses of both Aspergillus secondary metabolism and full-genome arrays and Northern blot and quantitative RT-PCR analyses, we demonstrate at the molecular level that a distinct fungal-bacterial interaction leads to the specific activation of fungal secondary metabolism genes. Most surprisingly, dialysis experiments and electron microscopy indicated that an intimate physical interaction of the bacterial and fungal mycelia is required to elicit the specific response. Gene knockout experiments provided evidence that one induced gene cluster codes for the long-sought after polyketide synthase (PKS) required for the biosynthesis of the archetypal polyketide orsellinic acid, the typical lichen metabolite lecanoric acid, and the cathepsin K inhibitors F-9775A and F-9775B. A phylogenetic analysis demonstrates that orthologs of this PKS are widespread in nature in all major fungal groups, including mycobionts of lichens. These results provide evidence of specific interaction among microorganisms belonging to different domains and support the hypothesis that not only diffusible signals but intimate physical interactions contribute to the communication among microorganisms and induction of otherwise silent biosynthesis genes.

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Agrobacterium tumefaciens-mediated transformation of filamentous fungi.

M. J. De Groot, P Bundock, P J Hooykaas … (1998)

Agrobacterium tumefaciens transfers part of its Ti plasmid, the T-DNA, to plant cells during tumorigenesis. It is routinely used for the genetic modification of a wide range of plant species. We report that A. tumefaciens can also transfer its T-DNA efficiently to the filamentous fungus Aspergillus awamori, demonstrating DNA transfer between a prokaryote and a filamentous fungus. We transformed both protoplasts and conidia with frequencies that were improved up to 600-fold as compared with conventional techniques for transformation of A. awamori protoplasts. The majority of the A. awamori transformants contained a single T-DNA copy randomly integrated at a chromosomal locus. The T-DNA integrated into the A. awamori genome in a manner similar to that described for plants. We also transformed a variety of other filamentous fungi, including Aspergillus niger, Fusarium venenatum, Trichoderma reesei, Colletotrichum gloeosporioides, Neurospora crassa, and the mushroom Agaricus bisporus, demonstrating that transformation using A. tumefaciens is generally applicable to filamentous fungi.

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Modulation of polyketide synthase activity by accessory proteins during lovastatin biosynthesis.

J. Kennedy, K Auclair, S Kendrew … (1999)

Polyketides, the ubiquitous products of secondary metabolism in microorganisms, are made by a process resembling fatty acid biosynthesis that allows the suppression of reduction or dehydration reactions at specific biosynthetic steps, giving rise to a wide range of often medically useful products. The lovastatin biosynthesis cluster contains two type I polyketide synthase genes. Synthesis of the main nonaketide-derived skeleton was found to require the previously known iterative lovastatin nonaketide synthase (LNKS), plus at least one additional protein (LovC) that interacts with LNKS and is necessary for the correct processing of the growing polyketide chain and production of dihydromonacolin L. The noniterative lovastatin diketide synthase (LDKS) enzyme specifies formation of 2-methylbutyrate and interacts closely with an additional transesterase (LovD) responsible for assembling lovastatin from this polyketide and monacolin J.

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Author and article information

Contributors

Michelina Ruocco:

ORCID: http://orcid.org/0000-0002-8322-3503

+39 0817753625 , michelina.ruocco@ipsp.cnr.it

Riccardo Baroncelli: riccardobaroncelli@gmail.com

Santa Olga Cacciola: olgacacciola@unict.it

Catello Pane: catello.pane@crea.gov.it

Maurilia Maria Monti: maurilia.monti@ipsp.cnr.it

Giuseppe Firrao: giuseppe.firrao@uniud.it

Mariarosaria Vergara: mariarosaria.vergara@sns.it

Gaetano Magnano di San Lio: gmagnano@unirc.it

Giovanni Vannacci: giovanni.vannacci@unipi.it

Felice Scala: scala@unina.it

Journal

Journal ID (nlm-ta): BMC Genomics

Journal ID (iso-abbrev): BMC Genomics

Title: BMC Genomics

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2164

Publication date (Electronic): 6 January 2018

Publication date PMC-release: 6 January 2018

Publication date Collection: 2018

Volume: 19

Electronic Location Identifier: 27

Affiliations

[1 ]Istituto per la Protezione Sostenibile delle Piante, CNR-IPSP, Via Università 133, 80055 Portici (Naples), Italy

[2 ]ISNI 0000 0001 2188 0893, GRID grid.6289.5, Université de Brest, EA 3882, Laboratoire Universitaire de Biodiversité et Ecologie Microbienne, IBSAM, ESIAB, Technopôle Brest-Iroise, ; 29280 Plouzané, France

[3 ]ISNI 0000 0004 1757 1969, GRID grid.8158.4, Dipartimento di Agricoltura, Alimentazione e Ambiente, , Università di Catania, ; 95123 Catania, Italy

[4 ]ISNI 0000 0001 2293 6756, GRID grid.423616.4, Consiglio per la ricerca in agricoltura e l’analisi dell’economia agraria, Centro di ricerca Orticoltura e Florovivaismo, sede di Pontecagnano, ; via Cavalleggeri 25, 84098 Pontecagnano (Salerno), Italy

[5 ]ISNI 0000 0001 2113 062X, GRID grid.5390.f, Dipartimento di Scienze AgroAlimentari, Ambientali e Animali, , Università di Udine, ; via Scienze, Udine, Italy

[6 ]GRID grid.6093.c, Scuola Normale Superiore di Pisa, ; 56126 Pisa, Italy

[7 ]ISNI 0000 0004 1757 3729, GRID grid.5395.a, Dipartimento di Scienze Agrarie, Alimentari e Agro-Ambientali, , Università di Pisa, ; 56124 Pisa, Italy

[8 ]ISNI 0000000122070761, GRID grid.11567.34, Dipartimento di Gestione dei Sistemi Agrari e Forestali, , Università Mediterranea di Reggio Calabria, ; 89061 Reggio Calabria, Italy

[9 ]ISNI 0000 0001 0790 385X, GRID grid.4691.a, Dipartimento di Agraria, , Università di Napoli Federico II, ; 80055 Portici (Naples), Italy

Author information

Michelina Ruocco http://orcid.org/0000-0002-8322-3503

Article

Publisher ID: 4405

DOI: 10.1186/s12864-017-4405-z

PMC ID: 5756342

PubMed ID: 29306326

SO-VID: 8b19dd11-f167-4ea2-a8ba-1d1c067aed5d

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 7 June 2017

Date accepted : 20 December 2017

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100003852, Regione Campania;

Award ID: B25C13000290007

Award ID: B25B09000080007

Award Recipient : Michelina Ruocco

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: polyketide synthases,diaporthe helianthi,plant pathogen,pathogen virulence, toxins

Data availability:

ScienceOpen disciplines: Genetics

Keywords: polyketide synthases, diaporthe helianthi, plant pathogen, pathogen virulence, toxins

Polyketide synthases of Diaporthe helianthi and involvement of DhPKS1 in virulence on sunflower

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Abstract

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Electronic supplementary material

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G3: Genes|Genomes|Genetics

Most cited references 60

Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans.

Agrobacterium tumefaciens-mediated transformation of filamentous fungi.

Modulation of polyketide synthase activity by accessory proteins during lovastatin biosynthesis.

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