The origin, versatility and distribution of azole fungicide resistance in the banana black Sigatoka pathogen Pseudocercospora fijiensis

Aguirre, Pablo Antonio Chong

doi:10.18174/387237

Cited by 3 publications

(7 citation statements)

References 111 publications

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“…These insertions comprise six copies of a repetitive element, whereas a single copy of this element is present in all sensitive isolates. Isolates with reduced sensitivity usually have two, three or more copies of this element (Chong‐Aguirre, ).…”

Section: Discussionmentioning

confidence: 99%

“…Finally, swapping the wt Pfcyp51 coding domain of a sensitive strain with this domain of an isolate with reduced sensitivity, thereby generating a strain with a wt coding domain, but multiple promoter inserts, which we have never encountered in nature, should result in increased sensitivity. However, the discovery of additional mechanisms for DMI sensitivity requires genetic studies, genome‐wide associations or mapping analyses (Chong‐Aguirre, ). We expect, however, that the combination of overexpression conferred by promoter insertions and Pfcyp51 target site mutations will explain most DMI sensitivity modulations.…”

Section: Discussionmentioning

confidence: 99%

“…As a result, reduced fungicide efficacy develops frequently and spreads rapidly (Arango Isaza et al ., ). This situation has contributed to a grave increase in the number of fungicide applications, which can reach over 50 applications per year (maximum of 10 applications with sterol 14α‐demethylation‐inhibitors, DMIs) in most banana export countries (Chong‐Aguirre, ; De Lapeyre De Bellaire et al ., ; FRAC, ; Martínez‐Bolaños et al ., ), thereby frequently comprising a 30% share of the production costs (Marín et al ., ). This practice poses a threat to the occupational health of plantation workers and the environment if guidelines are not followed.…”

Section: Introductionmentioning

confidence: 99%

“…Azole fungicide applications against black Sigatoka started in 1987 and have been widely used since 1991 when propiconazole, one of the major contemporary DMIs, was introduced to the market (Chong‐Aguirre, ; Romero and Sutton, ). Currently, several DMIs, such as difenoconazole, bitertanol and epoxiconazole, are used in disease management programmes, either alone or in mixtures with other fungicides with different modes of action.…”

Section: Introductionmentioning

confidence: 99%

“…However, reduced efficacy of single‐site fungicides surfaced rapidly in P. fijiensis after the introduction of quinone outside inhibitors (QoIs or strobilurins), methyl benzimidazole carbamates (MBCs) and DMIs for disease control in banana production (Amil et al ., ; Arango Isaza et al ., ; Cañas‐Gutiérrez et al ., ; Romero and Sutton, ). Previous studies on P. fijiensis have revealed the correlation between the reduced efficacy of propiconazole and point mutations in the coding domain of the Pfcyp51 gene, which cause non‐synonymous amino acid substitutions surrounding the substrate recognition sites (SRSs) at positions Y136, A313, Y461 and Y463 (Cañas‐Gutiérrez et al ., ; Chong‐Aguirre, ). Until now, this was the only explanatory mechanism for reduced sensitivity towards azoles in P. fijiensis .…”

Section: Introductionmentioning

confidence: 99%

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A new mechanism for reduced sensitivity to demethylation‐inhibitor fungicides in the fungal banana black Sigatoka pathogen Pseudocercospora fijiensis

Díaz-Trujillo

Chong

Stergiopoulos

et al. 2018

Molecular Plant Pathology

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The Dothideomycete Pseudocercospora fijiensis, previously Mycosphaerella fijiensis, is the causal agent of black Sigatoka, one of the most destructive diseases of bananas and plantains. Disease management depends on fungicide applications, with a major contribution from sterol demethylation-inhibitors (DMIs). The continued use of DMIs places considerable selection pressure on natural P. fijiensis populations, enabling the selection of novel genotypes with reduced sensitivity. The hitherto explanatory mechanism for this reduced sensitivity was the presence of non-synonymous point mutations in the target gene Pfcyp51, encoding the sterol 14α-demethylase enzyme. Here, we demonstrate a second mechanism involved in DMI sensitivity of P. fijiensis. We identified a 19-bp element in the wild-type (wt) Pfcyp51 promoter that concatenates in strains with reduced DMI sensitivity. A polymerase chain reaction (PCR) assay identified up to six Pfcyp51 promoter repeats in four field populations of P. fijiensis in Costa Rica. We used transformation experiments to swap the wt promoter of a sensitive field isolate with a promoter from a strain with reduced DMI sensitivity that comprised multiple insertions. Comparative in vivo phenotyping showed a functional and proportional up-regulation of Pfcyp51, which consequently decreased DMI sensitivity. Our data demonstrate that point mutations in the Pfcyp51 coding domain, as well as promoter inserts, contribute to the reduced DMI sensitivity of P. fijiensis. These results provide new insights into the importance of the appropriate use of DMIs and the need for the discovery of new molecules for black Sigatoka management.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A new mechanism for reduced sensitivity to demethylation‐inhibitor fungicides in the fungal banana black Sigatoka pathogen Pseudocercospora fijiensis

Díaz-Trujillo

Chong

Stergiopoulos

et al. 2018

Molecular Plant Pathology

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Genetic Diversity and Azole Fungicide Sensitivity in Pseudocercospora musae Field Populations in Brazil

et al. 2020

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Pseudocercospora musae, causal agent of Sigatoka leaf spot, or yellow Sigatoka disease, is considered a major pathogen of banana (Musa spp.). Widely disseminated in Brazil, this study explored the genetic diversity in field populations of the pathogen from production areas in the Distrito Federal and the States of Bahia, Minas Gerais, and Rio Grande do Norte. Resistance to demethylation inhibitor (DMI) fungicides was also examined. For 162 isolates from 10 banana growing regions, analysis of mating type idiomorph frequency was conducted, together with estimation of genetic diversity at 15 microsatellite loci. A total of 149 haplotypes were identified across the examined populations, with an average genetic diversity of 4.06. In general, populations displayed 1:1 proportions of idiomorphs MAT1-1 and MAT1-2, providing evidence for sexual recombination. Multilocus linkage disequilibrium also indicated asexual reproduction contributing to the genetic structure of certain populations. AMOVA revealed that 86.3% of the genetic differentiation of the pathogen occurred among isolates within populations. Discriminant Analysis of Principal Components (DAPC) identified six most probable genetic groups, with no population structure associated with geographic origin or collection site. Although genetic similarity was observed among certain populations from different states, data revealed increasing genetic differentiation with increasing geographic distance, as validated by Mantel's test (r = 0.19, P < 0.001). On the basis of DMI fungicide sensitivity testing and CYP51 gene sequence polymorphism, isolates from the Distrito Federal separated into two main groups, one with generally higher EC 50 values against eight DMI fungicides. A clear phenotype-to-genotype relationship was observed for isolates carrying the CYP51 alteration Y461N. Conventionally adopted fungicides for control of Sigatoka leaf spot are likely to be overcome by combined sexual and asexual reproduction mechanisms in P. musae driving genetic variability. Continued analysis of pathogen genetic diversity and monitoring of DMI sensitivity profiles of Brazilian field populations is essential for the development of integrated control strategies based on host resistance breeding and rational design of fungicide regimes.

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Genetic Improvement for Resistance to Black Sigatoka in Bananas: A Systematic Review

et al. 2021

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Bananas are an important staple food crop in tropical and subtropical regions in Asia, sub-Saharan Africa, and Central and South America. The plant is affected by numerous diseases, with the fungal leaf disease black Sigatoka, caused by Mycosphaerella fijiensis Morelet [anamorph: Pseudocercospora fijiensis (Morelet) Deighton], considered one of the most economically important phytosanitary problem. Although the development of resistant cultivars is recognized as most effective method for long term control of the disease, the majority of today's cultivars are susceptible. In order to gain insights into this pathosystem, this first systematic literature review on the topic is presented. Utilizing six databases (PubMed Central, Web of Science, Google Academic, Springer, CAPES and Scopus Journals) searches were performed using pre-established inclusion and exclusion criteria. From a total of 3,070 published studies examined, 24 were relevant with regard to the Musa-P. fijiensis pathosystem. Relevant papers highlighted that resistant and susceptible cultivars clearly respond differently to infection by this pathogen. M. acuminata wild diploids such as Calcutta 4 and other diploid cultivars can harbor sources of resistance genes, serving as parentals for the generation of improved diploids and subsequent gene introgression in new cultivars. From the sequenced reference genome of Musa acuminata, although the function of many genes in the genome still require validation, on the basis of transcriptome, proteome and biochemical data, numerous candidate genes and molecules have been identified for further evaluation through genetic transformation and gene editing approaches. Genes identified in the resistance response have included those associated with jasmonic acid and ethylene signaling, transcription factors, phenylpropanoid pathways, antioxidants and pathogenesis-related proteins. Papers in this study also revealed gene-derived markers in Musa applicable for downstream application in marker assisted selection. The information gathered in this review furthers understanding of the immune response in Musa to the pathogen P. fijiensis and is relevant for genetic improvement programs for bananas and plantains for control of black Sigatoka.

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The origin, versatility and distribution of azole fungicide resistance in the banana black Sigatoka pathogen Pseudocercospora fijiensis

Cited by 3 publications

References 111 publications

A new mechanism for reduced sensitivity to demethylation‐inhibitor fungicides in the fungal banana black Sigatoka pathogen Pseudocercospora fijiensis

A new mechanism for reduced sensitivity to demethylation‐inhibitor fungicides in the fungal banana black Sigatoka pathogen Pseudocercospora fijiensis

Genetic Diversity and Azole Fungicide Sensitivity in Pseudocercospora musae Field Populations in Brazil

Genetic Improvement for Resistance to Black Sigatoka in Bananas: A Systematic Review

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