Intracellular Siderophores Are Essential for Ascomycete Sexual Development in Heterothallic Cochliobolus heterostrophus and Homothallic Gibberella zeae

• Published in: Eukaryotic Cell Vol. 6; no. 8; pp. 1339 - 1353
• Main Authors: Oide, S, Krasnoff, S.B, Gibson, D.M, Turgeon, B.G
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 01-08-2007
• Subjects: Ascomycota - genetics; Ascomycota - growth & development; ascospores; Cochliobolus heterostrophus; enzymes; ferricrocin; Gene Deletion; Gibberella - genetics; Gibberella - growth & development; Gibberella zeae; heterothallism; homothallism; Intracellular Fluid - metabolism; iron; mutants; nonribosomal peptide synthetase; plant fertility; plant reproduction; Reproduction; selfing; sexual development; sexual systems; siderophores; Siderophores - physiology
• ISSN: 1535-9786; 1535-9778; 1535-9786
• DOI: 10.1128/EC.00111-07

Connections between fungal development and secondary metabolism have been reported previously, but as yet, no comprehensive analysis of a family of secondary metabolites and their possible role in fungal development has been reported. In the present study, mutant strains of the heterothallic ascomycete Cochliobolus heterostrophus, each lacking one of 12 genes (NPS1 to NPS12) encoding a nonribosomal peptide synthetase (NRPS), were examined for a role in sexual development. One type of strain (deltanps2) was defective in ascus/ascospore development in homozygous deltanps2 crosses. Homozygous crosses of the remaining 11 deltanps strains showed wild-type (WT) fertility. Phylogenetic, expression, and biochemical analyses demonstrated that the NRPS encoded by NPS2 is responsible for the biosynthesis of ferricrocin, the intracellular siderophore of C. heterostrophus. Functional conservation of NPS2 in both heterothallic C. heterostrophus and the unrelated homothallic ascomycete Gibberella zeae was demonstrated. G. zeae deltanps2 strains are concomitantly defective in intracellular siderophore (ferricrocin) biosynthesis and sexual development. Exogenous application of iron partially restored fertility to C. heterostrophus and G. zeae deltanps2 strains, demonstrating that abnormal sexual development of deltanps2 strains is at least partly due to their iron deficiency. Exogenous application of the natural siderophore ferricrocin to C. heterostrophus and G. zeae deltanps2 strains restored WT fertility. NPS1, a G. zeae NPS gene that groups phylogenetically with NPS2, does not play a role in sexual development. Overall, these data demonstrate that iron and intracellular siderophores are essential for successful sexual development of the heterothallic ascomycete C. heterostrophus and the homothallic ascomycete G. zeae.