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Eukaryotic Cell, August 2007, p. 1339-1353, Vol. 6, No. 8
1535-9778/07/$08.00+0     doi:10.1128/EC.00111-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

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

Shinichi Oide,^1, Stuart B. Krasnoff,² Donna M. Gibson,² and B. Gillian Turgeon^1*

Department of Plant Pathology and Plant-Microbe Biology, 334 Plant Science Building, Cornell University, Ithaca, New York 14853,¹ Plant Protection Research Unit USDA-ARS, Tower Road, Ithaca, New York 14853²

Received 8 April 2007/ Accepted 18 June 2007

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 (nps2) was defective in ascus/ascospore development in homozygous nps2 crosses. Homozygous crosses of the remaining 11 nps 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 nps2 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 nps2 strains, demonstrating that abnormal sexual development of nps2 strains is at least partly due to their iron deficiency. Exogenous application of the natural siderophore ferricrocin to C. heterostrophus and G. zeae nps2 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.

Published ahead of print on 29 June 2007.

Supplemental material for this article may be found at http://ec.asm.org/.

Present address: Uppsala Genetics Centre, Department of Plant Biology and Forest Genetics, University of Agricultural Sciences, 750 07 Uppsala, Sweden.