Combating a Global Threat to a Clonal Crop

Banana Black Sigatoka Pathogen Pseudocercospora fijiensis (Synonym Mycosphaerella fijiensis) Genomes Reveal Clues for Disease Control

Rafael E. Arango Isaza, Caucasella Diaz-Trujillo, Braham Dhillon, Andrea Aerts, Jean Carlier, Charles F. Crane, Tristan V. de Jong, Ineke de Vries, Robert Dietrich, Andrew D. Farmer, Claudia Fortes Fereira, Suzana Garcia, Mauricio Guzman, Richard C. Hamelin, Erika A. Lindquist, Rahim Mehrabi, Olman Quiros, Jeremy Schmutz, Harris Shapiro, Elizabeth Reynolds & 10 others Gabriel Scalliet, Manoel Souza, Ioannis Stergiopoulos, Theo A.J. van der Lee, Pierre J.G.M. de Wit, Marie Françoise Zapater, Lute Harm Zwiers, Igor V. Grigoriev, Stephen B. Goodwin*, Gert H.J. Kema

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

25 Citations (Scopus)

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. 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.

Original languageEnglish
Article numbere1005876
JournalPlos Genetics
Volume12
Issue number8
DOIs
Publication statusPublished - 2016

Fingerprint

black Sigatoka
Mycosphaerella fijiensis
Musa
disease control
bananas
fungicide
genome
pathogen
Genome
crop
pathogens
Dothideomycetes
crops
fungicides
plantation
Economics
resistance management
Population
Cladosporium
Karyotyping

Cite this

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. / Combating a Global Threat to a Clonal Crop : Banana Black Sigatoka Pathogen Pseudocercospora fijiensis (Synonym Mycosphaerella fijiensis) Genomes Reveal Clues for Disease Control. In: Plos Genetics. 2016 ; Vol. 12, No. 8.
@article{50b02f47924d4a41a6702b99818f9504,
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. 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.",
author = "{Arango Isaza}, {Rafael E.} and Caucasella Diaz-Trujillo and Braham Dhillon and Andrea Aerts and Jean Carlier and Crane, {Charles F.} and {V. de Jong}, Tristan and {de Vries}, Ineke and Robert Dietrich and Farmer, {Andrew D.} and {Fortes Fereira}, Claudia and Suzana Garcia and Mauricio Guzman and Hamelin, {Richard C.} and Lindquist, {Erika A.} and Rahim Mehrabi and Olman Quiros and Jeremy Schmutz and Harris Shapiro and Elizabeth Reynolds and Gabriel Scalliet and Manoel Souza and Ioannis Stergiopoulos and {van der Lee}, {Theo A.J.} and {de Wit}, {Pierre J.G.M.} and Zapater, {Marie Fran{\cc}oise} and Zwiers, {Lute Harm} and Grigoriev, {Igor V.} and Goodwin, {Stephen B.} and Kema, {Gert H.J.}",
year = "2016",
doi = "10.1371/journal.pgen.1005876",
language = "English",
volume = "12",
journal = "Plos Genetics",
issn = "1553-7404",
publisher = "Public Library of Science",
number = "8",

}

Arango Isaza, RE, Diaz-Trujillo, C, Dhillon, B, Aerts, A, Carlier, J, Crane, CF, V. de Jong, T, de Vries, I, Dietrich, R, Farmer, AD, Fortes Fereira, C, Garcia, S, Guzman, M, Hamelin, RC, Lindquist, EA, Mehrabi, R, Quiros, O, Schmutz, J, Shapiro, H, Reynolds, E, Scalliet, G, Souza, M, Stergiopoulos, I, van der Lee, TAJ, de Wit, PJGM, Zapater, MF, Zwiers, LH, Grigoriev, IV, Goodwin, SB & Kema, GHJ 2016, 'Combating a Global Threat to a Clonal Crop: Banana Black Sigatoka Pathogen Pseudocercospora fijiensis (Synonym Mycosphaerella fijiensis) Genomes Reveal Clues for Disease Control', Plos Genetics, vol. 12, no. 8, e1005876. https://doi.org/10.1371/journal.pgen.1005876

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

In: Plos Genetics, Vol. 12, No. 8, e1005876, 2016.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Combating a Global Threat to a Clonal Crop

T2 - Banana Black Sigatoka Pathogen Pseudocercospora fijiensis (Synonym Mycosphaerella fijiensis) Genomes Reveal Clues for Disease Control

AU - Arango Isaza, Rafael E.

AU - Diaz-Trujillo, Caucasella

AU - Dhillon, Braham

AU - Aerts, Andrea

AU - Carlier, Jean

AU - Crane, Charles F.

AU - V. de Jong, Tristan

AU - de Vries, Ineke

AU - Dietrich, Robert

AU - Farmer, Andrew D.

AU - Fortes Fereira, Claudia

AU - Garcia, Suzana

AU - Guzman, Mauricio

AU - Hamelin, Richard C.

AU - Lindquist, Erika A.

AU - Mehrabi, Rahim

AU - Quiros, Olman

AU - Schmutz, Jeremy

AU - Shapiro, Harris

AU - Reynolds, Elizabeth

AU - Scalliet, Gabriel

AU - Souza, Manoel

AU - Stergiopoulos, Ioannis

AU - van der Lee, Theo A.J.

AU - de Wit, Pierre J.G.M.

AU - Zapater, Marie Françoise

AU - Zwiers, Lute Harm

AU - Grigoriev, Igor V.

AU - Goodwin, Stephen B.

AU - Kema, Gert H.J.

PY - 2016

Y1 - 2016

N2 - 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.

AB - 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.

U2 - 10.1371/journal.pgen.1005876

DO - 10.1371/journal.pgen.1005876

M3 - Article

VL - 12

JO - Plos Genetics

JF - Plos Genetics

SN - 1553-7404

IS - 8

M1 - e1005876

ER -