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ARS Home » Pacific West Area » Pullman, Washington » Grain Legume Genetics Physiology Research » Research » Publications at this Location » Publication #317416
Title: Genomic analysis of Ascochyta rabiei identifies dynamic genome environments of solanapyrone biosynthesis gene cluster and a novel type of pathway-specific regulator

Author
item KIM, WONYONG - Washington State University
item PARK, JEONG-JIN - Washington State University
item GANG, DAVID - Washington State University
item PEEVER, TOBOIN - Washington State University
item Chen, Weidong

Submitted to: Eukaryotic Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/4/2015
Publication Date: 11/5/2015
Citation: Kim, W., Park, J., Gang, D.R., Peever, T., Chen, W. 2015. Genomic analysis of Ascochyta rabiei identifies dynamic genome environments of solanapyrone biosynthesis gene cluster and a novel type of pathway-specific regulator. Eukaryotic Cell. 14: 1102-1113.

Interpretive Summary: Fungi produce diverse secondary metabolites that play important roles in fungal biology such as host and niche specialization, serving as virulence factors, antibiotics and metal ion-chelating agents. The chickpea pathogen Ascochyta rabiei and the potato pathogen Alternaria solani produce secondary metabolites known as solanapyrones. Solanapyrone genes (Sol1 through Sol6) are clustered together in both Ascochyta rabiei and Alternaria solani. Among the six solanapyrone cluster genes, sol4 encodes a unique gene that initiates action of other genes. Deletion of sol4 created mutants that totally lost the ability to produce solanapyrone, but showed normal growth and development. Deletion of Sol 4 affected genes of the cluster, but not the genes outside the gene cluster, suggesting that sol4 is a specific regulator for solanapyrone biosynthesis and is necessary and sufficient for induction of the solanapyrone cluster genes. Despite the dynamic surrounding genomic regions, the solanapyrone cluster appears to have maintained its integrity, suggesting important roles of solanapyrones for fungal biology.

Technical Abstract: Secondary metabolite genes are often clustered together and situated in particular genomic regions such as the subtelomere, which can facilitate niche adaptation in fungi. Solanapyrones are toxic secondary metabolites produced by fungi occupying different ecological niches. Full genome sequencing of the ascomycete Ascochyta rabiei revealed a solanapyrone biosynthesis gene cluster embedded in an AT-rich isochore-like region proximal to a telomere end and surrounded by Tc1/Mariner-type transposable elements. The highly AT-rich environment of the solanapyrone cluster is likely the product of repeat-induced point mutations. Several secondary metabolism-related genes are found in the flanking regions of the solanapyrone cluster. Although the solanapyrone cluster appears to be resistant to repeat-induced point mutations, a P450 monooxygenase gene adjacent to the cluster has been degraded by such mutations. Among the solanapyrone cluster genes, sol4 encodes a novel type of Zn(II)2Cys6 zinc cluster transcription factor. Deletion of sol4 caused a total loss of solanapyrone production, but did not compromise growth and development. Gene expression studies with the sol4-deletion mutant delimited the boundaries of the solanapyrone cluster and revealed that sol4 is a specific regulator for solanapyrone biosynthesis and is necessary and sufficient for induction of the solanapyrone cluster genes. Despite the dynamic surrounding genomic regions, the solanapyrone cluster appears to have maintained its integrity, suggesting important roles of solanapyrones in fungal biology.