Comparative genomics of geographically distant Fusarium fujikuroi isolates revealed two distinct pathotypes correlating with secondary metabolite profiles.

Eva-Maria Niehaus,Slavica Janevska,Ulrich Güldener,Svetlana A Kalinina,Martin Münsterkötter,Ilaria Alberti,Petra M Houterman,Da-Woon Kim,Birgit Arndt,Sung-Hwan Yun,Il-Pyung Ahn,Christian M K Sieber,Bettina Tudzynski,Hans-Ulrich Humpf,Stefano Tonti,Hee-Kyoung Kim,Bart Thomma

doi:10.1371/journal.ppat.1006670

Abstract

Fusarium fujikuroi causes bakanae (“foolish seedling”) disease of rice which is characterized by hyper-elongation of seedlings resulting from production of gibberellic acids (GAs) by the fungus. This plant pathogen is also known for production of harmful mycotoxins, such as fusarins, fusaric acid, apicidin F and beauvericin. Recently, we generated the first de novo genome sequence of F. fujikuroi strain IMI 58289 combined with extensive transcriptional, epigenetic, proteomic and chemical product analyses. GA production was shown to provide a selective advantage during infection of the preferred host plant rice. Here, we provide genome sequences of eight additional F. fujikuroi isolates from distant geographic regions. The isolates differ in the size of chromosomes, most likely due to variability of subtelomeric regions, the type of asexual spores (microconidia and/or macroconidia), and the number and expression of secondary metabolite gene clusters. Whilst most of the isolates caused the typical bakanae symptoms, one isolate, B14, caused stunting and early withering of infected seedlings. In contrast to the other isolates, B14 produced no GAs but high amounts of fumonisins during infection on rice. Furthermore, it differed from the other isolates by the presence of three additional polyketide synthase (PKS) genes (PKS40, PKS43, PKS51) and the absence of the F. fujikuroi-specific apicidin F (NRPS31) gene cluster. Analysis of additional field isolates confirmed the strong correlation between the pathotype (bakanae or stunting/withering), and the ability to produce either GAs or fumonisins. Deletion of the fumonisin and fusaric acid-specific PKS genes in B14 reduced the stunting/withering symptoms, whereas deletion of the PKS51 gene resulted in elevated symptom development. Phylogenetic analyses revealed two subclades of F. fujikuroi strains according to their pathotype and secondary metabolite profiles.

Highlights

The heterothallic ascomycete Fusarium fujikuroi Nirenberg is a member of the Fusarium fujikuroi species complex (FFC), a monophyletic lineage which includes at least eleven mating populations (MPs A-K) that are sexually infertile with one another, and numerous distinct anamorphic species [1].F. fujikuroi (MP-C) is the causal agent of the rice disease bakanae (“foolish seedlings”), one of the most notorious seed-borne diseases with increasing economic importance in the major rice-growing countries in the world, including all rice-growing Asian and African countries, California, and more recently, Italy [1,2,3]
Infected seedlings appear to be taller and more slender when compared to healthy seedlings due to its ability to produce gibberellic acids (GAs)
The disease is responsible for high yield losses, and its incidence varies with regions, rice cultivars grown and the aggressiveness of the fungal isolates

Summary

Introduction

The heterothallic ascomycete Fusarium fujikuroi Nirenberg is a member of the Fusarium fujikuroi species complex (FFC), a monophyletic lineage which includes at least eleven mating populations (MPs A-K) that are sexually infertile with one another, and numerous distinct anamorphic species [1].F. fujikuroi (MP-C) is the causal agent of the rice disease bakanae (“foolish seedlings”), one of the most notorious seed-borne diseases with increasing economic importance in the major rice-growing countries in the world, including all rice-growing Asian and African countries, California, and more recently, Italy [1,2,3]. The fungus was one of the first fungal pathogens to be described, and bakanae is one of the oldest known diseases of rice being reported more than 100 years ago by Japanese scientists [4,5]. The most prominent symptoms of the disease are chlorotic, elongated and thin seedlings that are often several inches taller than healthy plants, and empty panicles leading to yield losses ranging from ca. The incidence and severity of the bakanae or stunting disease symptoms varies with regions and isolate. The pathogen is dispersed predominantly with infected seeds, infected crop residues from the previous season in the soil, or by conidia on diseased stems which can be transmitted by rain and wind [6]. Disease control has become increasingly difficult due to rapidly developing fungicide resistance in the fungal population [4]

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Conclusion