Two novel Venturia inaequalis genes induced upon morphogenetic differentiation during infection and in vitro growth on cellophane

Venturia inaequalis is a hemibiotrophic ascomycete that causes apple scab. Germ tubes, from conidia or ascospores, penetrate the leaf or fruit surface directly via appressoria-like swellings; subsequently the hyphae divide laterally to form a stroma between the cuticle and the outer wall of the epid...

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Published in:Fungal genetics and biology Vol. 45; no. 10; pp. 1329 - 1339
Main Authors: Kucheryava, Nataliya, Bowen, Joanna K., Sutherland, Paul W., Conolly, Joshua J., Mesarich, Carl H., Rikkerink, Erik H.A., Kemen, Eric, Plummer, Kim M., Hahn, Matthias, Templeton, Matthew D.
Format: Journal Article
Language:English
Published: United States Elsevier Inc 01-10-2008
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Abstract Venturia inaequalis is a hemibiotrophic ascomycete that causes apple scab. Germ tubes, from conidia or ascospores, penetrate the leaf or fruit surface directly via appressoria-like swellings; subsequently the hyphae divide laterally to form a stroma between the cuticle and the outer wall of the epidermal cells. This morphological switch can be mimicked by growing the fungus in vitro on cellophane discs. The aim of this work was to identify genes upregulated in planta using growth on cellophane as a model. Four cDNA clones were found to be induced by growth on cellophane, and qRT-PCR showed two of these genes were up-regulated over a thousand fold in infected apple leaves compared to liquid culture. The predicted proteins for both genes possess putative signal peptides for secretion but have no similarity to sequences in publicly available databases. Both genes encode proteins with novel, imperfect repeat domain structures, the number of which vary in an isolate-specific fashion. Cin1 has seven or eight repeats of about 60 amino acids with four conserved cysteine residues per repeat, while Cin3 has four or five repeats of 32 amino acids with no cysteines. Both proteins appear to have evolved through internal duplication. Cin3, in particular, shows considerable between-strain variation in domain structure, indicating a high degree of recombination at this locus and revealing that the repeat structure has most likely arisen by unequal crossing-over. Results of this study support the hypothesis that cellophane-grown V. inaequalis mimics aspects of biotrophic infection and provide the first insights into novel fungal genes expressed during apple scab infection and their mechanisms of evolution.
AbstractList Venturia inaequalis is a hemibiotrophic ascomycete that causes apple scab. Germ tubes, from conidia or ascospores, penetrate the leaf or fruit surface directly via appressoria-like swellings; subsequently the hyphae divide laterally to form a stroma between the cuticle and the outer wall of the epidermal cells. This morphological switch can be mimicked by growing the fungus in vitro on cellophane discs. The aim of this work was to identify genes upregulated in planta using growth on cellophane as a model. Four cDNA clones were found to be induced by growth on cellophane, and qRT-PCR showed two of these genes were up-regulated over a thousand fold in infected apple leaves compared to liquid culture. The predicted proteins for both genes possess putative signal peptides for secretion but have no similarity to sequences in publicly available databases. Both genes encode proteins with novel, imperfect repeat domain structures, the number of which vary in an isolate-specific fashion. Cin1 has seven or eight repeats of about 60 amino acids with four conserved cysteine residues per repeat, while Cin3 has four or five repeats of 32 amino acids with no cysteines. Both proteins appear to have evolved through internal duplication. Cin3, in particular, shows considerable between-strain variation in domain structure, indicating a high degree of recombination at this locus and revealing that the repeat structure has most likely arisen by unequal crossing-over. Results of this study support the hypothesis that cellophane-grown V. inaequalis mimics aspects of biotrophic infection and provide the first insights into novel fungal genes expressed during apple scab infection and their mechanisms of evolution.
Author Conolly, Joshua J.
Templeton, Matthew D.
Kucheryava, Nataliya
Sutherland, Paul W.
Bowen, Joanna K.
Plummer, Kim M.
Rikkerink, Erik H.A.
Hahn, Matthias
Mesarich, Carl H.
Kemen, Eric
Author_xml – sequence: 1
  givenname: Nataliya
  surname: Kucheryava
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  organization: University of Kaiserslautern, Department of Biology, Phytopathology, Postbox 3049, 67653 Kaiserslautern, Germany
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  givenname: Joanna K.
  surname: Bowen
  fullname: Bowen, Joanna K.
  organization: Horticulture and Food Research Institute of New Zealand, Mt Albert Research Centre, PB 92-169, Auckland 1142, New Zealand
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  givenname: Paul W.
  surname: Sutherland
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  givenname: Joshua J.
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  organization: Horticulture and Food Research Institute of New Zealand, Mt Albert Research Centre, PB 92-169, Auckland 1142, New Zealand
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  givenname: Carl H.
  surname: Mesarich
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  fullname: Kemen, Eric
  organization: University of Konstanz, Department of Biology, Universitätstr. 10, Konstanz, 78457, Germany
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  givenname: Kim M.
  surname: Plummer
  fullname: Plummer, Kim M.
  organization: La Trobe University, Department of Botany, Bundoora, Vic. 3086, Australia
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  givenname: Matthias
  surname: Hahn
  fullname: Hahn, Matthias
  organization: University of Kaiserslautern, Department of Biology, Phytopathology, Postbox 3049, 67653 Kaiserslautern, Germany
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  givenname: Matthew D.
  surname: Templeton
  fullname: Templeton, Matthew D.
  email: MTempleton@hortresearch.co.nz
  organization: Horticulture and Food Research Institute of New Zealand, Mt Albert Research Centre, PB 92-169, Auckland 1142, New Zealand
BackLink https://www.ncbi.nlm.nih.gov/pubmed/18692586$$D View this record in MEDLINE/PubMed
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Issue 10
Keywords Apple black spot
Malus X domestica
Unequal crossing-over
Stroma
Apple scab
Malus pumila
Repeat-domain proteins
Haplotype
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Snippet Venturia inaequalis is a hemibiotrophic ascomycete that causes apple scab. Germ tubes, from conidia or ascospores, penetrate the leaf or fruit surface directly...
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SubjectTerms Amino Acid Sequence
Apple black spot
Apple scab
Ascomycetes
Ascomycota - chemistry
Ascomycota - genetics
Ascomycota - growth & development
Ascomycota - metabolism
Cellophane
Fungal Proteins - chemistry
Fungal Proteins - genetics
Fungal Proteins - metabolism
Gene Expression Regulation, Fungal
Haplotype
Malus
Malus - microbiology
Malus pumila
Malus X domestica
Models, Biological
Molecular Sequence Data
Morphogenesis
Plant Diseases - microbiology
Plant Leaves - chemistry
Plant Leaves - genetics
Plant Leaves - growth & development
Plant Leaves - metabolism
Protein Sorting Signals
Protein Structure, Tertiary
Repeat-domain proteins
Sequence Alignment
Stroma
Unequal crossing-over
Up-Regulation
Venturia inaequalis
Title Two novel Venturia inaequalis genes induced upon morphogenetic differentiation during infection and in vitro growth on cellophane
URI https://dx.doi.org/10.1016/j.fgb.2008.07.010
https://www.ncbi.nlm.nih.gov/pubmed/18692586
https://search.proquest.com/docview/19680106
https://search.proquest.com/docview/69677527
Volume 45
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