Transposable elements in phytopathogenic Verticillium spp.

insights into genome evolution and inter- and intra-specific diversification

Stefan G. Amyotte, Xiaoping Tan, Kayla Pennerman, Maria Del Mar Jimenez Gasco, Steven J. Klosterman, Li Jun Ma, Katherine F. Dobinson, Paola Veronese

Research output: Contribution to journalArticle

37 Citations (Scopus)

Abstract

Background: Verticillium dahliae (Vd) and Verticillium albo-atrum (Va) are cosmopolitan soil fungi causing very disruptive vascular diseases on a wide range of crop plants. To date, no sexual stage has been identified in either microorganism suggesting that somatic mutation is a major force in generating genetic diversity. Whole genome comparative analysis of the recently sequenced strains VdLs.17 and VaMs.102 revealed that non-random insertions of transposable elements (TEs) have contributed to the generation of four lineage-specific (LS) regions in VdLs.17.Results: We present here a detailed analysis of Class I retrotransposons and Class II " cut-and-paste" DNA elements detected in the sequenced Verticillium genomes. We report also of their distribution in other Vd and Va isolates from various geographic origins. In VdLs.17, we identified and characterized 56 complete retrotransposons of the Gypsy-, Copia- and LINE-like types, as well as 34 full-length elements of the " cut-and-paste" superfamilies Tc1/mariner, Activator and Mutator. While Copia and Tc1/mariner were present in multiple identical copies, Activator and Mutator sequences were highly divergent. Most elements comprised complete ORFs, had matching ESTs and showed active transcription in response to stress treatment. Noticeably, we found evidences of repeat-induced point mutation (RIP) only in some of the Gypsy retroelements. While Copia-, Gypsy- and Tc1/mariner-like transposons were prominent, a large variation in presence of the other types of mobile elements was detected in the other Verticillium spp. strains surveyed. In particular, neither complete nor defective " cut-and-paste" TEs were found in VaMs.102.Conclusions: Copia-, Gypsy- and Tc1/mariner-like transposons are the most wide-spread TEs in the phytopathogens V. dahliae and V. albo-atrum. In VdLs.17, we identified several retroelements and " cut-and-paste" transposons still potentially active. Some of these elements have undergone diversification and subsequent selective amplification after introgression into the fungal genome. Others, such as the ripped Copias, have been potentially acquired by horizontal transfer. The observed biased TE insertion in gene-rich regions within an individual genome (VdLs.17) and the " patchy" distribution among different strains point to the mobile elements as major generators of Verticillium intra- and inter-specific genomic variation.

Original languageEnglish (US)
Article number314
JournalBMC genomics
Volume13
Issue number1
DOIs
StatePublished - Jul 16 2012

Fingerprint

Verticillium
DNA Transposable Elements
Genome
Retroelements
Ointments
Fungal Genome
Insertional Mutagenesis
Expressed Sequence Tags
Vascular Diseases
Point Mutation
Open Reading Frames
Fungi
Soil
Mutation
DNA

All Science Journal Classification (ASJC) codes

  • Biotechnology
  • Genetics

Cite this

Amyotte, Stefan G. ; Tan, Xiaoping ; Pennerman, Kayla ; Jimenez Gasco, Maria Del Mar ; Klosterman, Steven J. ; Ma, Li Jun ; Dobinson, Katherine F. ; Veronese, Paola. / Transposable elements in phytopathogenic Verticillium spp. insights into genome evolution and inter- and intra-specific diversification. In: BMC genomics. 2012 ; Vol. 13, No. 1.
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abstract = "Background: Verticillium dahliae (Vd) and Verticillium albo-atrum (Va) are cosmopolitan soil fungi causing very disruptive vascular diseases on a wide range of crop plants. To date, no sexual stage has been identified in either microorganism suggesting that somatic mutation is a major force in generating genetic diversity. Whole genome comparative analysis of the recently sequenced strains VdLs.17 and VaMs.102 revealed that non-random insertions of transposable elements (TEs) have contributed to the generation of four lineage-specific (LS) regions in VdLs.17.Results: We present here a detailed analysis of Class I retrotransposons and Class II {"} cut-and-paste{"} DNA elements detected in the sequenced Verticillium genomes. We report also of their distribution in other Vd and Va isolates from various geographic origins. In VdLs.17, we identified and characterized 56 complete retrotransposons of the Gypsy-, Copia- and LINE-like types, as well as 34 full-length elements of the {"} cut-and-paste{"} superfamilies Tc1/mariner, Activator and Mutator. While Copia and Tc1/mariner were present in multiple identical copies, Activator and Mutator sequences were highly divergent. Most elements comprised complete ORFs, had matching ESTs and showed active transcription in response to stress treatment. Noticeably, we found evidences of repeat-induced point mutation (RIP) only in some of the Gypsy retroelements. While Copia-, Gypsy- and Tc1/mariner-like transposons were prominent, a large variation in presence of the other types of mobile elements was detected in the other Verticillium spp. strains surveyed. In particular, neither complete nor defective {"} cut-and-paste{"} TEs were found in VaMs.102.Conclusions: Copia-, Gypsy- and Tc1/mariner-like transposons are the most wide-spread TEs in the phytopathogens V. dahliae and V. albo-atrum. In VdLs.17, we identified several retroelements and {"} cut-and-paste{"} transposons still potentially active. Some of these elements have undergone diversification and subsequent selective amplification after introgression into the fungal genome. Others, such as the ripped Copias, have been potentially acquired by horizontal transfer. The observed biased TE insertion in gene-rich regions within an individual genome (VdLs.17) and the {"} patchy{"} distribution among different strains point to the mobile elements as major generators of Verticillium intra- and inter-specific genomic variation.",
author = "Amyotte, {Stefan G.} and Xiaoping Tan and Kayla Pennerman and {Jimenez Gasco}, {Maria Del Mar} and Klosterman, {Steven J.} and Ma, {Li Jun} and Dobinson, {Katherine F.} and Paola Veronese",
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Transposable elements in phytopathogenic Verticillium spp. insights into genome evolution and inter- and intra-specific diversification. / Amyotte, Stefan G.; Tan, Xiaoping; Pennerman, Kayla; Jimenez Gasco, Maria Del Mar; Klosterman, Steven J.; Ma, Li Jun; Dobinson, Katherine F.; Veronese, Paola.

In: BMC genomics, Vol. 13, No. 1, 314, 16.07.2012.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Transposable elements in phytopathogenic Verticillium spp.

T2 - insights into genome evolution and inter- and intra-specific diversification

AU - Amyotte, Stefan G.

AU - Tan, Xiaoping

AU - Pennerman, Kayla

AU - Jimenez Gasco, Maria Del Mar

AU - Klosterman, Steven J.

AU - Ma, Li Jun

AU - Dobinson, Katherine F.

AU - Veronese, Paola

PY - 2012/7/16

Y1 - 2012/7/16

N2 - Background: Verticillium dahliae (Vd) and Verticillium albo-atrum (Va) are cosmopolitan soil fungi causing very disruptive vascular diseases on a wide range of crop plants. To date, no sexual stage has been identified in either microorganism suggesting that somatic mutation is a major force in generating genetic diversity. Whole genome comparative analysis of the recently sequenced strains VdLs.17 and VaMs.102 revealed that non-random insertions of transposable elements (TEs) have contributed to the generation of four lineage-specific (LS) regions in VdLs.17.Results: We present here a detailed analysis of Class I retrotransposons and Class II " cut-and-paste" DNA elements detected in the sequenced Verticillium genomes. We report also of their distribution in other Vd and Va isolates from various geographic origins. In VdLs.17, we identified and characterized 56 complete retrotransposons of the Gypsy-, Copia- and LINE-like types, as well as 34 full-length elements of the " cut-and-paste" superfamilies Tc1/mariner, Activator and Mutator. While Copia and Tc1/mariner were present in multiple identical copies, Activator and Mutator sequences were highly divergent. Most elements comprised complete ORFs, had matching ESTs and showed active transcription in response to stress treatment. Noticeably, we found evidences of repeat-induced point mutation (RIP) only in some of the Gypsy retroelements. While Copia-, Gypsy- and Tc1/mariner-like transposons were prominent, a large variation in presence of the other types of mobile elements was detected in the other Verticillium spp. strains surveyed. In particular, neither complete nor defective " cut-and-paste" TEs were found in VaMs.102.Conclusions: Copia-, Gypsy- and Tc1/mariner-like transposons are the most wide-spread TEs in the phytopathogens V. dahliae and V. albo-atrum. In VdLs.17, we identified several retroelements and " cut-and-paste" transposons still potentially active. Some of these elements have undergone diversification and subsequent selective amplification after introgression into the fungal genome. Others, such as the ripped Copias, have been potentially acquired by horizontal transfer. The observed biased TE insertion in gene-rich regions within an individual genome (VdLs.17) and the " patchy" distribution among different strains point to the mobile elements as major generators of Verticillium intra- and inter-specific genomic variation.

AB - Background: Verticillium dahliae (Vd) and Verticillium albo-atrum (Va) are cosmopolitan soil fungi causing very disruptive vascular diseases on a wide range of crop plants. To date, no sexual stage has been identified in either microorganism suggesting that somatic mutation is a major force in generating genetic diversity. Whole genome comparative analysis of the recently sequenced strains VdLs.17 and VaMs.102 revealed that non-random insertions of transposable elements (TEs) have contributed to the generation of four lineage-specific (LS) regions in VdLs.17.Results: We present here a detailed analysis of Class I retrotransposons and Class II " cut-and-paste" DNA elements detected in the sequenced Verticillium genomes. We report also of their distribution in other Vd and Va isolates from various geographic origins. In VdLs.17, we identified and characterized 56 complete retrotransposons of the Gypsy-, Copia- and LINE-like types, as well as 34 full-length elements of the " cut-and-paste" superfamilies Tc1/mariner, Activator and Mutator. While Copia and Tc1/mariner were present in multiple identical copies, Activator and Mutator sequences were highly divergent. Most elements comprised complete ORFs, had matching ESTs and showed active transcription in response to stress treatment. Noticeably, we found evidences of repeat-induced point mutation (RIP) only in some of the Gypsy retroelements. While Copia-, Gypsy- and Tc1/mariner-like transposons were prominent, a large variation in presence of the other types of mobile elements was detected in the other Verticillium spp. strains surveyed. In particular, neither complete nor defective " cut-and-paste" TEs were found in VaMs.102.Conclusions: Copia-, Gypsy- and Tc1/mariner-like transposons are the most wide-spread TEs in the phytopathogens V. dahliae and V. albo-atrum. In VdLs.17, we identified several retroelements and " cut-and-paste" transposons still potentially active. Some of these elements have undergone diversification and subsequent selective amplification after introgression into the fungal genome. Others, such as the ripped Copias, have been potentially acquired by horizontal transfer. The observed biased TE insertion in gene-rich regions within an individual genome (VdLs.17) and the " patchy" distribution among different strains point to the mobile elements as major generators of Verticillium intra- and inter-specific genomic variation.

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