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Title: Combating a Global Threat to a Clonal Crop: Banana Black Sigatoka Pathogen Pseudocercospora fijiensis (Synonym Mycosphaerella fijiensis) Genomes Reveal Clues for Disease Control

Abstract

Black Sigatoka or black leaf streak disease, caused by the Dothideomycete fungus Pseudocercospora fijiensis (previously: Mycosphaerella fijiensis), is the most significant foliar disease of banana worldwide. Due to the lack of effective host resistance, management of this disease requires frequent fungicide applications, which greatly increase the economic and environmental costs to produce banana. Weekly applications in most banana plantations lead to rapid evolution of fungicide-resistant strains within populations causing disease-control failures throughout the world. Given its extremely high economic importance, two strains of P. fijiensis were sequenced and assembled with the aid of a new genetic linkage map. The 74-Mb genome of P. fijiensis is massively expanded by LTR retrotransposons, making it the largest genome within the Dothideomycetes. Melting-curve assays suggest that the genomes of two closely related members of the Sigatoka disease complex, P. eumusae and P. musae, also are expanded. Electrophoretic karyotyping and analyses of molecular markers in P. fijiensis field populations showed chromosome-length polymorphisms and high genetic diversity. Genetic differentiation was also detected using neutral markers, suggesting strong selection with limited gene flow at the studied geographic scale. Frequencies of fungicide resistance in fungicide-treated plantations were much higher than those in untreated wild-type P. fijiensis populations. Amore » homologue of the Cladosporium fulvum Avr4 effector, PfAvr4, was identified in the P. fijiensis genome. Infiltration of the purified PfAVR4 protein into leaves of the resistant banana variety Calcutta 4 resulted in a hypersensitive-like response. This result suggests that Calcutta 4 could carry an unknown resistance gene recognizing PfAVR4. Besides adding to our understanding of the overall Dothideomycete genome structures, the P. fijiensis genome will aid in developing fungicide treatment schedules to combat this pathogen and in improving the efficiency of banana breeding programs.« less

Authors:
 [1]; ORCiD logo [2];  [3];  [4];  [5];  [6]; ORCiD logo [7];  [2];  [8];  [9];  [10];  [11];  [12];  [13];  [4];  [14];  [12];  [4]; ORCiD logo [4];  [15] more »;  [16];  [17];  [18];  [19];  [20];  [5];  [21];  [4];  [6];  [20];  [22] « less
  1. National Univ. of Columbia, Medellin (Columbia). School of Biosciences
  2. Wageningen Univ. (Netherlands). Plant Research International
  3. Purdue Univ., West Lafayette, IN (United States). Dept. of Botany and Plant Pathology
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. Joint Research Unit, Montpellier (France). Biology and Genetics of Plant-Pathogen Interactions (UMR-BGPI)
  6. US Dept. of Agriculture (USDA)., West Lafayette, IN (United States)
  7. Univ. Medical Center Groningen (Netherlands)
  8. Syngenta Biotechnology Inc., Research Triangle Park, NC (United States)
  9. National Center for Genome Resources, Santa Fe, NM (United States)
  10. Brazilian Agricultural Research Corporation, Cruz das Almas (Brazil)
  11. Univ. of Lavras (Brazil)
  12. National Banana Corporation of Costa Rica (CORBANA), Limon (Costa Rica)
  13. Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Forest and Conservation Sciences; Laurentian Forestry Centre, Quebec, QC (Canada)
  14. Seed and Plant Improvement Inst., Karaj (Iran). Dept. of Genetics
  15. Jeallots HIll International Research Centre, Berkshire (United Kingdom)
  16. Syngenta Crop Protection, Stein (Switzerland)
  17. Embrapa-LABEX Europ, Wageningen (Netherlands)
  18. Univ. of California, Davis, CA (United States)
  19. Wageningen Univ., (Netherlands). Plant Research International
  20. Wageningen Univ. (Netherlands)
  21. Fungal Diversity Center, Utrecht (Netherlands)
  22. Virginia Polytechnic Inst. and State Univ. (Virginia Tech), Blacksburg, VA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1338423
Alternate Identifier(s):
OSTI ID: 1379542
Grant/Contract Number:
AC02-05CH11231; 3602-22000-015-00D
Resource Type:
Journal Article: Published Article
Journal Name:
PLoS Genetics
Additional Journal Information:
Journal Volume: 12; Journal Issue: 8; Journal ID: ISSN 1553-7404
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Arango Isaza, Rafael E., Diaz-Trujillo, Caucasella, Dhillon, Braham, Aerts, Andrea, Carlier, Jean, Crane, Charles F., V. de Jong, Tristan, de Vries, Ineke, Dietrich, Robert, Farmer, Andrew D., Fortes Fereira, Claudia, Garcia, Suzana, Guzman, Mauricio, Hamelin, Richard C., Lindquist, Erika A., Mehrabi, Rahim, Quiros, Olman, Schmutz, Jeremy, Shapiro, Harris, Reynolds, Elizabeth, Scalliet, Gabriel, Souza, Manoel, Stergiopoulos, Ioannis, Van der Lee, Theo A. J., De Wit, Pierre J. G. M., Zapater, Marie-Françoise, Zwiers, Lute-Harm, Grigoriev, Igor V., Goodwin, Stephen B., Kema, Gert H. J., and McDowell, John M. Combating a Global Threat to a Clonal Crop: Banana Black Sigatoka Pathogen Pseudocercospora fijiensis (Synonym Mycosphaerella fijiensis) Genomes Reveal Clues for Disease Control. United States: N. p., 2016. Web. doi:10.1371/journal.pgen.1005876.
Arango Isaza, Rafael E., Diaz-Trujillo, Caucasella, Dhillon, Braham, Aerts, Andrea, Carlier, Jean, Crane, Charles F., V. de Jong, Tristan, de Vries, Ineke, Dietrich, Robert, Farmer, Andrew D., Fortes Fereira, Claudia, Garcia, Suzana, Guzman, Mauricio, Hamelin, Richard C., Lindquist, Erika A., Mehrabi, Rahim, Quiros, Olman, Schmutz, Jeremy, Shapiro, Harris, Reynolds, Elizabeth, Scalliet, Gabriel, Souza, Manoel, Stergiopoulos, Ioannis, Van der Lee, Theo A. J., De Wit, Pierre J. G. M., Zapater, Marie-Françoise, Zwiers, Lute-Harm, Grigoriev, Igor V., Goodwin, Stephen B., Kema, Gert H. J., & McDowell, John M. Combating a Global Threat to a Clonal Crop: Banana Black Sigatoka Pathogen Pseudocercospora fijiensis (Synonym Mycosphaerella fijiensis) Genomes Reveal Clues for Disease Control. United States. doi:10.1371/journal.pgen.1005876.
Arango Isaza, Rafael E., Diaz-Trujillo, Caucasella, Dhillon, Braham, Aerts, Andrea, Carlier, Jean, Crane, Charles F., V. de Jong, Tristan, de Vries, Ineke, Dietrich, Robert, Farmer, Andrew D., Fortes Fereira, Claudia, Garcia, Suzana, Guzman, Mauricio, Hamelin, Richard C., Lindquist, Erika A., Mehrabi, Rahim, Quiros, Olman, Schmutz, Jeremy, Shapiro, Harris, Reynolds, Elizabeth, Scalliet, Gabriel, Souza, Manoel, Stergiopoulos, Ioannis, Van der Lee, Theo A. J., De Wit, Pierre J. G. M., Zapater, Marie-Françoise, Zwiers, Lute-Harm, Grigoriev, Igor V., Goodwin, Stephen B., Kema, Gert H. J., and McDowell, John M. Thu . "Combating a Global Threat to a Clonal Crop: Banana Black Sigatoka Pathogen Pseudocercospora fijiensis (Synonym Mycosphaerella fijiensis) Genomes Reveal Clues for Disease Control". United States. doi:10.1371/journal.pgen.1005876.
@article{osti_1338423,
title = {Combating a Global Threat to a Clonal Crop: Banana Black Sigatoka Pathogen Pseudocercospora fijiensis (Synonym Mycosphaerella fijiensis) Genomes Reveal Clues for Disease Control},
author = {Arango Isaza, Rafael E. and Diaz-Trujillo, Caucasella and Dhillon, Braham and Aerts, Andrea and Carlier, Jean and Crane, Charles F. and V. de Jong, Tristan and de Vries, Ineke and Dietrich, Robert and Farmer, Andrew D. and Fortes Fereira, Claudia and Garcia, Suzana and Guzman, Mauricio and Hamelin, Richard C. and Lindquist, Erika A. and Mehrabi, Rahim and Quiros, Olman and Schmutz, Jeremy and Shapiro, Harris and Reynolds, Elizabeth and Scalliet, Gabriel and Souza, Manoel and Stergiopoulos, Ioannis and Van der Lee, Theo A. J. and De Wit, Pierre J. G. M. and Zapater, Marie-Françoise and Zwiers, Lute-Harm and Grigoriev, Igor V. and Goodwin, Stephen B. and Kema, Gert H. J. and McDowell, John M.},
abstractNote = {Black Sigatoka or black leaf streak disease, caused by the Dothideomycete fungus Pseudocercospora fijiensis (previously: Mycosphaerella fijiensis), is the most significant foliar disease of banana worldwide. Due to the lack of effective host resistance, management of this disease requires frequent fungicide applications, which greatly increase the economic and environmental costs to produce banana. Weekly applications in most banana plantations lead to rapid evolution of fungicide-resistant strains within populations causing disease-control failures throughout the world. Given its extremely high economic importance, two strains of P. fijiensis were sequenced and assembled with the aid of a new genetic linkage map. The 74-Mb genome of P. fijiensis is massively expanded by LTR retrotransposons, making it the largest genome within the Dothideomycetes. Melting-curve assays suggest that the genomes of two closely related members of the Sigatoka disease complex, P. eumusae and P. musae, also are expanded. Electrophoretic karyotyping and analyses of molecular markers in P. fijiensis field populations showed chromosome-length polymorphisms and high genetic diversity. Genetic differentiation was also detected using neutral markers, suggesting strong selection with limited gene flow at the studied geographic scale. Frequencies of fungicide resistance in fungicide-treated plantations were much higher than those in untreated wild-type P. fijiensis populations. A homologue of the Cladosporium fulvum Avr4 effector, PfAvr4, was identified in the P. fijiensis genome. Infiltration of the purified PfAVR4 protein into leaves of the resistant banana variety Calcutta 4 resulted in a hypersensitive-like response. This result suggests that Calcutta 4 could carry an unknown resistance gene recognizing PfAVR4. Besides adding to our understanding of the overall Dothideomycete genome structures, the P. fijiensis genome will aid in developing fungicide treatment schedules to combat this pathogen and in improving the efficiency of banana breeding programs.},
doi = {10.1371/journal.pgen.1005876},
journal = {PLoS Genetics},
number = 8,
volume = 12,
place = {United States},
year = {Thu Aug 11 00:00:00 EDT 2016},
month = {Thu Aug 11 00:00:00 EDT 2016}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1371/journal.pgen.1005876

Citation Metrics:
Cited by: 4works
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  • Black Sigatoka or black leaf streak disease, caused by the Dothideomycete fungus Pseudocercospora fijiensis (previously: Mycosphaerella fijiensis), is the most significant foliar disease of banana worldwide. Due to the lack of effective host resistance, management of this disease requires frequent fungicide applications, which greatly increase the economic and environmental costs to produce banana. Weekly applications in most banana plantations lead to rapid evolution of fungicide-resistant strains within populations causing disease-control failures throughout the world. Given its extremely high economic importance, two strains of P. fijiensis were sequenced and assembled with the aid of a new genetic linkage map. The 74-Mbmore » genome of P. fijiensis is massively expanded by LTR retrotransposons, making it the largest genome within the Dothideomycetes. Melting-curve assays suggest that the genomes of two closely related members of the Sigatoka disease complex, P. eumusae and P. musae, also are expanded. Electrophoretic karyotyping and analyses of molecular markers in P. fijiensis field populations showed chromosome-length polymorphisms and high genetic diversity. Genetic differentiation was also detected using neutral markers, suggesting strong selection with limited gene flow at the studied geographic scale. Frequencies of fungicide resistance in fungicide-treated plantations were much higher than those in untreated wild-type P. fijiensis populations. A homologue of the Cladosporium fulvum Avr4 effector, PfAvr4, was identified in the P. fijiensis genome. Infiltration of the purified PfAVR4 protein into leaves of the resistant banana variety Calcutta 4 resulted in a hypersensitive-like response. This result suggests that Calcutta 4 could carry an unknown resistance gene recognizing PfAVR4. Besides adding to our understanding of the overall Dothideomycete genome structures, the P. fijiensis genome will aid in developing fungicide treatment schedules to combat this pathogen and in improving the efficiency of banana breeding programs.« less
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