The Mitochondrial Genome of a Plant Fungal Pathogen Pseudocercospora fijiensis (Mycosphaerellaceae), Comparative Analysis and Diversification Times of the Sigatoka Disease Complex Using Fossil Calibrated Phylogenies.

Juliana E Arcila-Galvis,Tatiana Arias,Javier M Torres-Bonilla,Rafael E Arango

doi:10.3390/life11030215

Abstract

Mycosphaerellaceae is a highly diverse fungal family containing a variety of pathogens affecting many economically important crops. Mitochondria play a crucial role in fungal metabolism and in the study of fungal evolution. This study aims to: (i) describe the mitochondrial genome of Pseudocercospora fijiensis, and (ii) compare it with closely related species (Sphaerulina musiva, S. populicola, P. musae and P. eumusae) available online, paying particular attention to the Sigatoka disease’s complex causal agents. The mitochondrial genome of P. fijiensis is a circular molecule of 74,089 bp containing typical genes coding for the 14 proteins related to oxidative phosphorylation, 2 rRNA genes and a set of 38 tRNAs. P. fijiensis mitogenome has two truncated cox1 copies, and bicistronic transcription of nad2-nad3 and atp6-atp8 confirmed experimentally. Comparative analysis revealed high variability in size and gene order among selected Mycosphaerellaceae mitogenomes likely to be due to rearrangements caused by mobile intron invasion. Using fossil calibrated Bayesian phylogenies, we found later diversification times for Mycosphaerellaceae (66.6 MYA) and the Sigatoka disease complex causal agents, compared to previous strict molecular clock studies. An early divergent Pseudocercospora fijiensis split from the sister species P. musae + P. eumusae 13.31 MYA while their sister group, the sister species P. eumusae and P. musae, split from their shared common ancestor in the late Miocene 8.22 MYA. This newly dated phylogeny suggests that species belonging to the Sigatoka disease complex originated after wild relatives of domesticated bananas (section Eumusae; 27.9 MYA). During this time frame, mitochondrial genomes expanded significantly, possibly due to invasions of introns into different electron transport chain genes.

Highlights

Mycosphaerellaceae is a highly diverse fungal family containing endophytes, saprobes, epiphytes, fungicolous and phytopathogenic species in more than 56 genera [1,2]
We found that in mitogenomes analyzed there were differences in content of freestanding and intronic Homing Endonuclease Genes (HEGs), genes coding for hypothetical proteins, and accessory genes such as DNA/RNA polymerases, reverse transcriptases and transposases
Fossil calibrated phylogenies are reported for the first time here for fungal plant pathogens that had later diversification times for the origin of all the species involved, compared to previous studies

Summary

Introduction

Mycosphaerellaceae is a highly diverse fungal family containing endophytes, saprobes, epiphytes, fungicolous and phytopathogenic species in more than 56 genera [1,2]. Three Mycosphaerellaceae members, Pseudocercospora eumusae, P. fijiensis, and P. musae, [1] are major pathogens of bananas and plantains. They comprise the so-called Sigatoka disease complex which is responsible for one of the most economically destructive diseases for banana growers [9,10]. Diseases caused by these three pathogens induce plant physiological alterations including a reduction in photosynthetic capacity, crop yield, and fruit quality [9]. Pseudocercospora fijiensis (teleomorph Mycosphaerella fijiensis) is the causal agent of black leaf streak disease (BLSD; aka Black Leaf Spot Disease), one the most damaging and costly diseases for banana and plantain worldwide [13]

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