A multi-omics analysis of the grapevine pathogen Lasiodiplodia theobromae reveals that temperature affects the expression of virulence- and pathogenicity-related genes

Abstract

Lasiodiplodia theobromae (Botryosphaeriaceae, Ascomycota) is a plant pathogen and human opportunist whose pathogenicity is modulated by temperature. The molecular effects of temperature on L. theobromae are mostly unknown, so we used a multi-omics approach to understand how temperature affects the molecular mechanisms of pathogenicity. The genome of L. theobromae LA-SOL3 was sequenced (Illumina MiSeq) and annotated. Furthermore, the transcriptome (Illumina TruSeq) and proteome (Orbitrap LC-MS/MS) of LA-SOL3 grown at 25 °C and 37 °C were analysed. Proteins related to pathogenicity (plant cell wall degradation, toxin synthesis, mitogen-activated kinases pathway and proteins involved in the velvet complex) were more abundant when the fungus grew at 25 °C. At 37 °C, proteins related to pathogenicity were less abundant than at 25 °C, while proteins related to cell wall organisation were more abundant. On the other hand, virulence factors involved in human pathogenesis, such as the SSD1 virulence protein, were expressed only at 37 °C. Taken together, our results showed that this species presents a typical phytopathogenic molecular profile that is compatible with a hemibiotrophic lifestyle. We showed that L. theobromae is equipped with the pathogenesis toolbox that enables it to infect not only plants but also animals.

A LysM Domain-Containing Protein LtLysM1 Is Important for Vegetative Growth and Pathogenesis in Woody Plant Pathogen Lasiodiplodia theobromae

“…Lasiodiplodia theobromae , a woody plant pathogen belonging to Botryosphaeriaceae family, has received much attention recently for the considerable damage caused by this fungus in fruiter’s industry. Research on this fungus have made great progress during the past two decades including strain isolation, diseases symptoms characterization, enzymatic activity analyses, and genome and transcription analyses ( Cao et al, 2020 ; Félix et al, 2019 ; Gonçalves et al, 2019 ; Paolinelli-Alfonso et al, 2016 ; Úrbez-Torres et al, 2008 ; Yan et al, 2018 ). However, investigation on the pathogenic mechanism are still at a preliminary stage and remain stagnant because of the multinuclear cell structure of this fungus, which seriously constrains the genetic manipulations in molecular studies.…”

“…Lasiodiplodia theobromae is emerging as one of the most aggressive pathogens that causes severe grapevine canker disease in vineyards, resulting in considerable yield losses to global grape industry ( Rodríguez-Gálvez et al 2015 ; Úrbez-Torres, 2011 ; Yan et al, 2013 ). So far, numerous pathogenicity-related genes have been identified in L. theobromae based on genome sequencing and bioinformatic analyses ( Félix et al, 2019 ; Yan et al, 2018 ), functional mechanisms of these genes, however, is barely documented.…”

Fun(gi)omics: Advanced and Diverse Technologies to Explore Emerging Fungal Pathogens and Define Mechanisms of Antifungal Resistance

“…The aggressive and emergent grapevine pathogen Lasiodiplodia theobromae , which is associated with >500 plant species and a multitude of diseases, also has a history of rare human infections, such as keratitis ( 115 , 116 ). The sensitivity of this fungal agent to elevated temperatures provokes its pathogenicity; therefore, a combination of L. theobromae genome, transcriptome, and proteome analyses was recently performed for ambient and mammalian host temperatures ( 117 ). At 25°C, there was a substantial increase in extracellular proteins involved in plant cell wall degradation and pathogenesis, whereas a temperature increase shifted the protein and transcript profiles toward survival responses, including for the maintenance of cell wall integrity.…”

Effect of γ-Aminobutyric Acid (GABA) on the Metabolome of Two Strains of Lasiodiplodia theobromae Isolated from Grapevine

“…It is also known that the expression of some fungal genes, including genes required for virulence, is influenced by temperature and nutritional state [ 4 , 5 ]. More recently, new evidences have emerged from studies on the effect of abiotic factors on the metabolome of fungi isolated from several hosts [ 6 ].…”