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Abstract
The Sigatoka disease complex, caused by the closely-related Dothideomycete fungi Pseudocercospora musae (yellow sigatoka), Pseudocercospora eumusae (eumusae leaf spot), and Pseudocercospora fijiensis (black sigatoka), is currently the most devastating disease on banana worldwide. The three species emerged on bananas from a recent common ancestor and show clear differences in virulence, with P. eumusae and P. fijiensis considered the most aggressive. In order to understand the genomic modifications associated with shifts in the species virulence spectra after speciation, and to identify their pathogenic core that can be exploited in disease management programs, we have sequenced and analyzed the genomes of P. eumusae and P. musae and compared them with the available genome sequence of P. fijiensis. Comparative analysis of genome architectures revealed significant differences in genome size, mainly due to different rates of LTR retrotransposon proliferation. Still, gene counts remained relatively equal and in the range of other Dothideomycetes. Phylogenetic reconstruction based on a set of 46 conserved single-copy genes strongly supported an earlier evolutionary radiation of P. fijiensis from P. musae and P. eumusae. However, pairwise analyses of gene content indicated that the more virulent P. eumusae and P. fijiensis share complementary patterns of expansions and contractions in core gene families related to metabolism and enzymatic degradation of plant cell walls, suggesting that the evolution of virulence in these two pathogens has, to some extent, been facilitated by convergent changes in metabolic pathways associated with nutrient acquisition and assimilation. In spite of their common ancestry and shared host-specificity, the three species retain fairly dissimilar repertoires of effector proteins, suggesting that they likely evolved different strategies for manipulating the host immune system. Finally, 234 gene families, including seven putative effectors, were exclusively present in the three Sigatoka species, and could thus be related to adaptation to the banana host.
Highlights
Bananas and plantains (Musa spp.) are amongst the world's top five staple food crops, as approximately 100 million tons of bananas are produced annually in nearly 120 countries in tropical and subtropical regions [1]
Given the high sequencing depth of 100-150x that is considered sufficient to cover the breadth of protein-coding exons, the apparent discrepancy between the final assembly sizes and the genome sizes estimated by the k-mer distribution analysis, can be attributed to the high repeat content, which prevented the complete assembly of the repeat-rich regions and led to highly fragmented genome assemblies
The three species have surfaced as destructive pathogens on bananas during the last century and they have evolved from a recent common ancestor, clear differences in virulence exist amongst them that correlate with the time of their appearance [5,6,7]
Summary
Bananas and plantains (Musa spp.) are amongst the world's top five staple food crops, as approximately 100 million tons of bananas are produced annually in nearly 120 countries in tropical and subtropical regions [1]. The problem is intensified by the very narrow genetic basis of currently cultivated banana varieties, as most are sterile triploid hybrids (AAA, AAB, ABB) between the wild species Musa acuminata (A genome) and Musa balbisiana (B genome) This includes desert bananas (AAA) of the Cavendish-subgroup, cooking bananas (AAA or ABB), and most plantain landraces (AAB) [2]. The socio-economic impact of the disease is much higher in small farming communities in sub-Saharan Africa, Southeast Asia, and Latin America that depend almost exclusively on the banana crop for their survival. Managing this disease is of urgent importance and is currently under critical public review for humanitarian, biosafety, and environmental reasons [1, 4]
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