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

PLoS Genet. 2016 Aug 11;12(8):e1005876. doi: 10.1371/journal.pgen.1005876. eCollection 2016 Aug.

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.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Ascomycota / genetics*
  • Ascomycota / pathogenicity
  • Breeding
  • Chromosomes, Fungal / genetics
  • Disease Resistance / genetics*
  • Genetic Variation
  • Genome, Fungal
  • Genotype
  • Musa / genetics*
  • Musa / growth & development
  • Musa / microbiology
  • Plant Diseases / genetics*
  • Plant Diseases / microbiology
  • Plant Leaves / genetics*
  • Plant Leaves / microbiology
  • Retroelements / genetics

Substances

  • Retroelements

Grant support

The work conducted by the U.S. Department of Energy Joint Genome Institute is supported by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231.This work was supported in part by USDA CRIS projects 3602-22000-015-00D and 3602-22000-017-00D. Work at Plant Research International was partly funded by The Dutch Dioraphte VSM grant 14.03.01.00. UNALMED and CIB work was supported by the Colombian Administrative department of Science, Technology and Innovation – Colciencias contracts no 0031–2013 and No 018-2015, and by the National University of Colombia at Medellín. CDT's research work was supported by scholarship 187781 from the National Council of Science and Technology (CONACyT) from Mexico. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.