LDS1-produced oxylipins are negative regulators of growth, conidiation and fumonisin synthesis in the fungal maize pathogen Fusarium verticillioides

Valeria Scala,Corrado Fanelli,Gianni Galaverna,Francesca Cardinale,Anna A Fabbri,Martina Cirlini,Paola Battilani,Matteo Ludovici,Massimo Reverberi,Chiara Dall'Asta,Ivan Visentin,Paola Giorni

doi:10.3389/fmicb.2014.00669

Abstract

Oxylipins are fatty acid-derived signaling compounds produced by all eukaryotes so far investigated; in mycotoxigenic fungi, they modulate toxin production and interactions with the host plants. Among the many enzymes responsible for oxylipin generation, Linoleate Diol Synthase 1 (LDS1) produces mainly 8-hydroperoxyoctadecenoic acid and subsequently different di-hydroxyoctadecenoic acids. In this study, we inactivated a copy of the putative LDS1 ortholog (acc. N. FVEG_09294.3) of Fusarium verticillioides, with the aim to investigate its influence on the oxylipin profile of the fungus, on its development, secondary metabolism and virulence. LC-MS/MS oxylipin profiling carried out on the selected mutant strain revealed significant quali-quantitative differences for several oxylipins when compared to the WT strain. The Fvlds1-deleted mutant grew better, produced more conidia, synthesized more fumonisins and infected maize cobs faster than the WT strain. We hypothesize that oxylipins may act as regulators of gene expression in the toxigenic plant pathogen F. verticillioides, in turn causing notable changes in its phenotype. These changes could relate to the ability of oxylipins to re-shape the transcriptional profile of F. verticillioides by inducing chromatin modifications and exerting a direct control on the transcription of secondary metabolism in fungi.

Highlights

Fusarium verticillioides causes the ear and stalk rot of maize (Zea mays) by entering through roots, stalks and ears at different growth stages
VERTICILLIOIDES Our previous study (Scala et al, 2013) identified the bona fide Linoleate Diol Synthase 1 (LDS1) gene homolog as one of the putative oxylipin-forming genes most highly expressed during the saprophytic growth of WT F. verticillioides (ITEM 10027) on a FB-inducing medium containing cracked maize
The results indicated the presence of two hybridization signals with the LDS1 probe whilst at least one putative mutant presented a recognizable deletion pattern (Supplementary Image 1)

Summary

Introduction

Fusarium verticillioides causes the ear and stalk rot of maize (Zea mays) by entering through roots, stalks and ears at different growth stages. Tissue invasion is often asymptomatic even in the presence of massive growth inside the kernels (Estrada et al, 2012), where F. verticillioides produces fumonisins. This is a family of mycotoxins that, especially in their B series (FB), are hazardous for human and animal health, while apparently not directly related to fungal virulence and aggressiveness. The non-enzymatic pathway of oxylipin synthesis derives from spontaneous formation of reactive oxygen species (ROS) such as hydroxyl radical, which may initiate lipid peroxidation (Brodhun and Feussner, 2011). Oxylipins possess pivotal functions as signal molecules (Christensen and Kolomiets, 2011)

Methods

Results

Conclusion