Ceratocystis cacaofunesta genome analysis reveals a large expansion of extracellular phosphatidylinositol-specific phospholipase-C genes (PI-PLC)

Abstract Background The Ceratocystis genus harbors a large number of phytopathogenic fungi that cause xylem parenchyma degradation and vascular destruction on a broad range of economically important plants. Ceratocystis cacaofunesta is a necrotrophic fungus responsible for lethal wilt disease in cac...

Full description

Bibliographic Details
Main Authors: Eddy Patricia Lopez Molano, Odalys García Cabrera, Juliana Jose, Leandro Costa do Nascimento, Marcelo Falsarella Carazzolle, Paulo José Pereira Lima Teixeira, Javier Correa Alvarez, Ricardo Augusto Tiburcio, Paulo Massanari Tokimatu Filho, Gustavo Machado Alvares de Lima, Rafael Victório Carvalho Guido, Thamy Lívia Ribeiro Corrêa, Adriana Franco Paes Leme, Piotr Mieczkowski, Gonçalo Amarante Guimarães Pereira
Format: Article
Language:English
Published: BMC 2018-01-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-018-4440-4
id doaj-03dfa04d911c450abbace3387d1930f3
record_format Article
collection DOAJ
language English
format Article
sources DOAJ
author Eddy Patricia Lopez Molano
Odalys García Cabrera
Juliana Jose
Leandro Costa do Nascimento
Marcelo Falsarella Carazzolle
Paulo José Pereira Lima Teixeira
Javier Correa Alvarez
Ricardo Augusto Tiburcio
Paulo Massanari Tokimatu Filho
Gustavo Machado Alvares de Lima
Rafael Victório Carvalho Guido
Thamy Lívia Ribeiro Corrêa
Adriana Franco Paes Leme
Piotr Mieczkowski
Gonçalo Amarante Guimarães Pereira
spellingShingle Eddy Patricia Lopez Molano
Odalys García Cabrera
Juliana Jose
Leandro Costa do Nascimento
Marcelo Falsarella Carazzolle
Paulo José Pereira Lima Teixeira
Javier Correa Alvarez
Ricardo Augusto Tiburcio
Paulo Massanari Tokimatu Filho
Gustavo Machado Alvares de Lima
Rafael Victório Carvalho Guido
Thamy Lívia Ribeiro Corrêa
Adriana Franco Paes Leme
Piotr Mieczkowski
Gonçalo Amarante Guimarães Pereira
Ceratocystis cacaofunesta genome analysis reveals a large expansion of extracellular phosphatidylinositol-specific phospholipase-C genes (PI-PLC)
BMC Genomics
Phosphoinositide-specific phospholipases C (PI PLC)
Ceratocystis wilt of cacao
Plant pathogen
author_facet Eddy Patricia Lopez Molano
Odalys García Cabrera
Juliana Jose
Leandro Costa do Nascimento
Marcelo Falsarella Carazzolle
Paulo José Pereira Lima Teixeira
Javier Correa Alvarez
Ricardo Augusto Tiburcio
Paulo Massanari Tokimatu Filho
Gustavo Machado Alvares de Lima
Rafael Victório Carvalho Guido
Thamy Lívia Ribeiro Corrêa
Adriana Franco Paes Leme
Piotr Mieczkowski
Gonçalo Amarante Guimarães Pereira
author_sort Eddy Patricia Lopez Molano
title Ceratocystis cacaofunesta genome analysis reveals a large expansion of extracellular phosphatidylinositol-specific phospholipase-C genes (PI-PLC)
title_short Ceratocystis cacaofunesta genome analysis reveals a large expansion of extracellular phosphatidylinositol-specific phospholipase-C genes (PI-PLC)
title_full Ceratocystis cacaofunesta genome analysis reveals a large expansion of extracellular phosphatidylinositol-specific phospholipase-C genes (PI-PLC)
title_fullStr Ceratocystis cacaofunesta genome analysis reveals a large expansion of extracellular phosphatidylinositol-specific phospholipase-C genes (PI-PLC)
title_full_unstemmed Ceratocystis cacaofunesta genome analysis reveals a large expansion of extracellular phosphatidylinositol-specific phospholipase-C genes (PI-PLC)
title_sort ceratocystis cacaofunesta genome analysis reveals a large expansion of extracellular phosphatidylinositol-specific phospholipase-c genes (pi-plc)
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2018-01-01
description Abstract Background The Ceratocystis genus harbors a large number of phytopathogenic fungi that cause xylem parenchyma degradation and vascular destruction on a broad range of economically important plants. Ceratocystis cacaofunesta is a necrotrophic fungus responsible for lethal wilt disease in cacao. The aim of this work is to analyze the genome of C. cacaofunesta through a comparative approach with genomes of other Sordariomycetes in order to better understand the molecular basis of pathogenicity in the Ceratocystis genus. Results We present an analysis of the C. cacaofunesta genome focusing on secreted proteins that might constitute pathogenicity factors. Comparative genome analyses among five Ceratocystidaceae species and 23 other Sordariomycetes fungi showed a strong reduction in gene content of the Ceratocystis genus. However, some gene families displayed a remarkable expansion, in particular, the Phosphatidylinositol specific phospholipases-C (PI-PLC) family. Also, evolutionary rate calculations suggest that the evolution process of this family was guided by positive selection. Interestingly, among the 82 PI-PLCs genes identified in the C. cacaofunesta genome, 70 genes encoding extracellular PI-PLCs are grouped in eight small scaffolds surrounded by transposon fragments and scars that could be involved in the rapid evolution of the PI-PLC family. Experimental secretome using LC–MS/MS validated 24% (86 proteins) of the total predicted secretome (342 proteins), including four PI-PLCs and other important pathogenicity factors. Conclusion Analysis of the Ceratocystis cacaofunesta genome provides evidence that PI-PLCs may play a role in pathogenicity. Subsequent functional studies will be aimed at evaluating this hypothesis. The observed genetic arsenals, together with the analysis of the PI-PLC family shown in this work, reveal significant differences in the Ceratocystis genome compared to the classical vascular fungi, Verticillium and Fusarium. Altogether, our analyses provide new insights into the evolution and the molecular basis of plant pathogenicity.
topic Phosphoinositide-specific phospholipases C (PI PLC)
Ceratocystis wilt of cacao
Plant pathogen
url http://link.springer.com/article/10.1186/s12864-018-4440-4
work_keys_str_mv AT eddypatricialopezmolano ceratocystiscacaofunestagenomeanalysisrevealsalargeexpansionofextracellularphosphatidylinositolspecificphospholipasecgenespiplc
AT odalysgarciacabrera ceratocystiscacaofunestagenomeanalysisrevealsalargeexpansionofextracellularphosphatidylinositolspecificphospholipasecgenespiplc
AT julianajose ceratocystiscacaofunestagenomeanalysisrevealsalargeexpansionofextracellularphosphatidylinositolspecificphospholipasecgenespiplc
AT leandrocostadonascimento ceratocystiscacaofunestagenomeanalysisrevealsalargeexpansionofextracellularphosphatidylinositolspecificphospholipasecgenespiplc
AT marcelofalsarellacarazzolle ceratocystiscacaofunestagenomeanalysisrevealsalargeexpansionofextracellularphosphatidylinositolspecificphospholipasecgenespiplc
AT paulojosepereiralimateixeira ceratocystiscacaofunestagenomeanalysisrevealsalargeexpansionofextracellularphosphatidylinositolspecificphospholipasecgenespiplc
AT javiercorreaalvarez ceratocystiscacaofunestagenomeanalysisrevealsalargeexpansionofextracellularphosphatidylinositolspecificphospholipasecgenespiplc
AT ricardoaugustotiburcio ceratocystiscacaofunestagenomeanalysisrevealsalargeexpansionofextracellularphosphatidylinositolspecificphospholipasecgenespiplc
AT paulomassanaritokimatufilho ceratocystiscacaofunestagenomeanalysisrevealsalargeexpansionofextracellularphosphatidylinositolspecificphospholipasecgenespiplc
AT gustavomachadoalvaresdelima ceratocystiscacaofunestagenomeanalysisrevealsalargeexpansionofextracellularphosphatidylinositolspecificphospholipasecgenespiplc
AT rafaelvictoriocarvalhoguido ceratocystiscacaofunestagenomeanalysisrevealsalargeexpansionofextracellularphosphatidylinositolspecificphospholipasecgenespiplc
AT thamyliviaribeirocorrea ceratocystiscacaofunestagenomeanalysisrevealsalargeexpansionofextracellularphosphatidylinositolspecificphospholipasecgenespiplc
AT adrianafrancopaesleme ceratocystiscacaofunestagenomeanalysisrevealsalargeexpansionofextracellularphosphatidylinositolspecificphospholipasecgenespiplc
AT piotrmieczkowski ceratocystiscacaofunestagenomeanalysisrevealsalargeexpansionofextracellularphosphatidylinositolspecificphospholipasecgenespiplc
AT goncaloamaranteguimaraespereira ceratocystiscacaofunestagenomeanalysisrevealsalargeexpansionofextracellularphosphatidylinositolspecificphospholipasecgenespiplc
_version_ 1725412509506076672
spelling doaj-03dfa04d911c450abbace3387d1930f32020-11-25T00:09:20ZengBMCBMC Genomics1471-21642018-01-0119112410.1186/s12864-018-4440-4Ceratocystis cacaofunesta genome analysis reveals a large expansion of extracellular phosphatidylinositol-specific phospholipase-C genes (PI-PLC)Eddy Patricia Lopez Molano0Odalys García Cabrera1Juliana Jose2Leandro Costa do Nascimento3Marcelo Falsarella Carazzolle4Paulo José Pereira Lima Teixeira5Javier Correa Alvarez6Ricardo Augusto Tiburcio7Paulo Massanari Tokimatu Filho8Gustavo Machado Alvares de Lima9Rafael Victório Carvalho Guido10Thamy Lívia Ribeiro Corrêa11Adriana Franco Paes Leme12Piotr Mieczkowski13Gonçalo Amarante Guimarães Pereira14Genomic and Expression Laboratory, Department of Genetics, Evolution and Bioagents, Institute of Biology, University of CampinasGenomic and Expression Laboratory, Department of Genetics, Evolution and Bioagents, Institute of Biology, University of CampinasGenomic and Expression Laboratory, Department of Genetics, Evolution and Bioagents, Institute of Biology, University of CampinasCentro Nacional de Processamento de Alto Desempenho, Universidade Estadual de CampinasGenomic and Expression Laboratory, Department of Genetics, Evolution and Bioagents, Institute of Biology, University of CampinasGenomic and Expression Laboratory, Department of Genetics, Evolution and Bioagents, Institute of Biology, University of CampinasDepartamento de Ciencias Biológicas, Escuela de Ciencias, Universidad EAFITGenomic and Expression Laboratory, Department of Genetics, Evolution and Bioagents, Institute of Biology, University of CampinasGenomic and Expression Laboratory, Department of Genetics, Evolution and Bioagents, Institute of Biology, University of CampinasCentro de Biotecnologia Molecular Estrutural, Instituto de Física de São Carlos, Universidade de São PauloCentro de Biotecnologia Molecular Estrutural, Instituto de Física de São Carlos, Universidade de São PauloGenomic and Expression Laboratory, Department of Genetics, Evolution and Bioagents, Institute of Biology, University of CampinasBrazilian Biosciences National Laboratory (LNBio) CNPEMHigh-Throughput Sequencing Facility, University of North CarolinaGenomic and Expression Laboratory, Department of Genetics, Evolution and Bioagents, Institute of Biology, University of CampinasAbstract Background The Ceratocystis genus harbors a large number of phytopathogenic fungi that cause xylem parenchyma degradation and vascular destruction on a broad range of economically important plants. Ceratocystis cacaofunesta is a necrotrophic fungus responsible for lethal wilt disease in cacao. The aim of this work is to analyze the genome of C. cacaofunesta through a comparative approach with genomes of other Sordariomycetes in order to better understand the molecular basis of pathogenicity in the Ceratocystis genus. Results We present an analysis of the C. cacaofunesta genome focusing on secreted proteins that might constitute pathogenicity factors. Comparative genome analyses among five Ceratocystidaceae species and 23 other Sordariomycetes fungi showed a strong reduction in gene content of the Ceratocystis genus. However, some gene families displayed a remarkable expansion, in particular, the Phosphatidylinositol specific phospholipases-C (PI-PLC) family. Also, evolutionary rate calculations suggest that the evolution process of this family was guided by positive selection. Interestingly, among the 82 PI-PLCs genes identified in the C. cacaofunesta genome, 70 genes encoding extracellular PI-PLCs are grouped in eight small scaffolds surrounded by transposon fragments and scars that could be involved in the rapid evolution of the PI-PLC family. Experimental secretome using LC–MS/MS validated 24% (86 proteins) of the total predicted secretome (342 proteins), including four PI-PLCs and other important pathogenicity factors. Conclusion Analysis of the Ceratocystis cacaofunesta genome provides evidence that PI-PLCs may play a role in pathogenicity. Subsequent functional studies will be aimed at evaluating this hypothesis. The observed genetic arsenals, together with the analysis of the PI-PLC family shown in this work, reveal significant differences in the Ceratocystis genome compared to the classical vascular fungi, Verticillium and Fusarium. Altogether, our analyses provide new insights into the evolution and the molecular basis of plant pathogenicity.http://link.springer.com/article/10.1186/s12864-018-4440-4Phosphoinositide-specific phospholipases C (PI PLC)Ceratocystis wilt of cacaoPlant pathogen