Mitochondrial Carnitine-Dependent Acetyl Coenzyme A Transport Is Required for Normal Sexual and Asexual Development of the Ascomycete Gibberella zeae

Abstract

<jats:title>ABSTRACT</jats:title><jats:p>Fungi have evolved efficient metabolic mechanisms for the exact temporal (developmental stages) and spatial (organelles) production of acetyl coenzyme A (acetyl-CoA). We previously demonstrated mechanistic roles of several acetyl-CoA synthetic enzymes, namely, ATP citrate lyase and acetyl-CoA synthetases (ACSs), in the plant-pathogenic fungus<jats:named-content content-type="genus-species">Gibberella zeae</jats:named-content>. In this study, we characterized two carnitine acetyltransferases (CATs; CAT1 and CAT2) to obtain a better understanding of the metabolic processes occurring in<jats:named-content content-type="genus-species">G. zeae</jats:named-content>. We found that CAT1 functioned as an alternative source of acetyl-CoA required for lipid accumulation in an<jats:italic>ACS1</jats:italic>deletion mutant. Moreover, deletion of<jats:italic>CAT1</jats:italic>and/or<jats:italic>CAT2</jats:italic>resulted in various defects, including changes to vegetative growth, asexual/sexual development, trichothecene production, and virulence. Although CAT1 is associated primarily with peroxisomal CAT function, mislocalization experiments showed that the role of CAT1 in acetyl-CoA transport between the mitochondria and cytosol is important for sexual and asexual development in<jats:named-content content-type="genus-species">G. zeae</jats:named-content>. Taking these data together, we concluded that<jats:named-content content-type="genus-species">G. zeae</jats:named-content>CATs are responsible for facilitating the exchange of acetyl-CoA across intracellular membranes, particularly between the mitochondria and the cytosol, during various developmental stages.</jats:p>

Comparative transcriptome analysis between an evolved abscisic acid-overproducing mutant Botrytis cinerea TBC-A and its ancestral strain Botrytis cinerea TBC-6

“…In fungi, the carnitine/acetyl-carnitine shuttle is essential for the intracellular transport of acetyl-CoA among the mitochondria, peroxisomes and the cytosol46474849. In the present study, the transcription levels of Bc1G_14516 and Bc1G_14666, which encode the B. cinerea ortholog of the mitochondrial/peroxisomal carnitine acetyltransferase Cat2 and the mitochondrial carnitine carrier50515253, respectively, were upregulated in TBC-A compared to TBC-6 (p value < 0.05).…”

Peroxisomes and sexual development in fungi

“…This transport depends on the carnitine acetyltransferase-mediated acetyl-carnitine shuttle (Figure 2) (Strijbis and Distel, 2010). G. zeae mutants defective for a peroxisomal/mitochondrial carnitine acetyltransferase (CAT) produce fewer perithecia than a wild-type strain (Son et al, 2012). This finding is consistent with a role for the fatty acid β-oxidation pathway in sustaining fruiting-body formation.…”

“…However, elimination of CATs has an ambiguous impact on ascospore germination in different fungi. While ascospore germination is slightly reduced in S. sclerotiorum pth2 null strains (Liberti et al, 2013), deletion of its ortholog exerts no developmental defect in A. nidulans (Hynes et al, 2011), and results in precocious germination in G. zeae (Son et al, 2012). Furthermore, defective glyoxylate cycle or peroxisome assembly does not affect sexual or asexual spore viability in A. nidulans (Armitt et al, 1976; Gainey et al, 1992; Hynes et al, 2008).…”

WetA Is Required for Conidiogenesis and Conidium Maturation in the Ascomycete Fungus Fusarium graminearum

“…We have used the A. nidulans model as a basis for characterizing F. graminearum orthologs of genes involved in acetyl coenzyme A synthesis (39,43), the velvet complex (27), the G protein complex (44), and G protein signaling (45). These orthologs play species-specific roles in various aspects of development and virulence.…”

“…Most of these genes encode transcription factors (TFs) and kinases (34)(35)(36)(37)(38)(39)(40), and many play pivotal roles in major cellular processes. Knockout mutants of these genes were found to be pleiotropic and defective in sexual reproduction, vegetative growth, virulence, and conidiation.…”