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Title: Genetic and Genomic Dissection of the Cochliobolus heterostrophus Tox1 Locus Controlling Biosynthesis of the Polyketide Virulence Factor T-toxin

Abstract

Fungal pathogenesis to plants is an intricate developmental process requiring biological components found in most fungi, as well as factors that are unique to fungal taxa that participate in particular fungus–plant interactions. The host-selective polyketide toxin known as T-toxin produced by Cochliobolus heterostrophus race T, a highly virulent pathogen of maize, is an intriguing example of the latter type of virulence determinant. The Tox1 locus, which controls biosynthesis of T-toxin, originally defined as a single genetic locus, it is, in fact, two exceedingly complex loci on two chromosomes that are reciprocally translocated with respect to their counterparts in weakly pathogenic race O. Race O lacks the Tox1 locus and does not produce T-toxin. Highly virulent race T was first recognized when it caused an epidemic of Southern Corn Leaf Blight, which devastated the US corn crop in 1970. The evolutionary origin of the Tox1 locus remains unknown.

Authors:
;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1006334
Report Number(s):
PNNL-SA-55067
BM0102070; TRN: US201105%%997
DOE Contract Number:
AC05-76RL01830
Resource Type:
Book
Resource Relation:
Related Information: Fungal Genomics, Advances in Genetics, 57:219-261
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 99 GENERAL AND MISCELLANEOUS//MATHEMATICS, COMPUTING, AND INFORMATION SCIENCE; BIOSYNTHESIS; CHROMOSOMES; CROPS; FUNGI; GENETICS; MAIZE; ORIGIN; PATHOGENESIS; PATHOGENS; TOXINS; VIRULENCE; fungi; genomics; genetics; plant pathogen; secondary metabolism

Citation Formats

Turgeon, Barbara G., and Baker, Scott E.. Genetic and Genomic Dissection of the Cochliobolus heterostrophus Tox1 Locus Controlling Biosynthesis of the Polyketide Virulence Factor T-toxin. United States: N. p., 2007. Web.
Turgeon, Barbara G., & Baker, Scott E.. Genetic and Genomic Dissection of the Cochliobolus heterostrophus Tox1 Locus Controlling Biosynthesis of the Polyketide Virulence Factor T-toxin. United States.
Turgeon, Barbara G., and Baker, Scott E.. Fri . "Genetic and Genomic Dissection of the Cochliobolus heterostrophus Tox1 Locus Controlling Biosynthesis of the Polyketide Virulence Factor T-toxin". United States. doi:.
@article{osti_1006334,
title = {Genetic and Genomic Dissection of the Cochliobolus heterostrophus Tox1 Locus Controlling Biosynthesis of the Polyketide Virulence Factor T-toxin},
author = {Turgeon, Barbara G. and Baker, Scott E.},
abstractNote = {Fungal pathogenesis to plants is an intricate developmental process requiring biological components found in most fungi, as well as factors that are unique to fungal taxa that participate in particular fungus–plant interactions. The host-selective polyketide toxin known as T-toxin produced by Cochliobolus heterostrophus race T, a highly virulent pathogen of maize, is an intriguing example of the latter type of virulence determinant. The Tox1 locus, which controls biosynthesis of T-toxin, originally defined as a single genetic locus, it is, in fact, two exceedingly complex loci on two chromosomes that are reciprocally translocated with respect to their counterparts in weakly pathogenic race O. Race O lacks the Tox1 locus and does not produce T-toxin. Highly virulent race T was first recognized when it caused an epidemic of Southern Corn Leaf Blight, which devastated the US corn crop in 1970. The evolutionary origin of the Tox1 locus remains unknown.},
doi = {},
journal = {},
number = ,
volume = ,
place = {United States},
year = {Fri Apr 27 00:00:00 EDT 2007},
month = {Fri Apr 27 00:00:00 EDT 2007}
}

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  • Cochliobolus heterostrophus race T, causal agent of Southern Corn Leaf Blight, requires T-toxin (a family of C35 – C49 polyketides) for high virulence on T-cytoplasm maize. Production of T-toxin is controlled by two unlinked loci, Tox1A and Tox1B, carried on 1.2 Mb of DNA not found in race O, a mildly virulent form of the fungus that does not produce T-toxin, or in any other Cochliobolus spp. or closely related fungus. PKS1, a polyketide synthase (PKS)-encoding gene at Tox1A and DEC1, a decarboxylase-encoding gene at Tox1B, are necessary for T-toxin production. Although there is evidence that additional genes are requiredmore » for T-toxin production, efforts to clone them have been frustrated because the genes are located in highly repeated, A+T-rich DNA. To overcome this difficulty, Ligation specificity-based Expression Analysis Display (LEAD), a comparative AFLP/gel fractionation/capillary sequencing procedure was applied to cDNAs from a near isogenic pair of race T (Tox1+) and race O (Tox1-) strains. This led to discovery of PKS2, a second PKS-encoding gene that maps at Tox1A and is required for both T-toxin biosynthesis and high virulence to maize. Thus, the carbon chain of each T-toxin family member is likely assembled by action of two PKSs, which produce two polyketides, one of which may act as the starter unit for biosynthesis of the mature T-toxin molecule.« less
  • Suppressor T cell factor(s) (TsF/sub 1/) inhibit the in vivo priming of azobenzenearsonate-specific cytotoxic T-cell responses. The activity of TsF/sub 1/ is restricted by genes linked to Igh-1 allotypic markers. TsF/sub 1/ obtained from B6.Igh-1/sup n/ mice was unable to suppress the immune response in B6.Igh-1/sup b/ mice and vice versa. However, TsF/sub 1/ prepared from B6.Igh-1/sup n/ T cells parked in an Igh-congeneic B6.Igh-1/sup b/ environment displays an additional restriction specificity of the host. Thus, TsF/sub 1/ prepared from these Igh-chimeric mice suppressed immune responses in both B6.Igh-1/sup n/ (donor) and B6.Igh-1/sup b/ (recipient) mice but not in micemore » of the unrelated strain BALB/c.Igh-1/sup a/. The results indicate that the establishment of the suppressor T-cell repertoire is dependent not only upon the genetic background of the individual T cell but also upon the influence of Igh-linked determinants present when T-cell clones are selected during the response.« less
  • Modular collaboration between iterative fungal polyketide synthases (IPKSs) is an important mechanism for generating structural diversity of polyketide natural products. Inter-PKS communication and substrate channeling are controlled in large by the starter unit acyl carrier protein transacylase (SAT) domain found in the accepting IPKS module. Here in this study, we reconstituted the modular biosynthesis of the benzaldehyde core of the chaetoviridin and chaetomugilin azaphilone natural products using the IPKSs CazF and CazM. Our studies revealed a critical role of CazM’s SAT domain in selectively transferring a highly reduced triketide product from CazF. In contrast, a more oxidized triketide that ismore » also produced by CazF and required in later stages of biosynthesis of the final product is not recognized by the SAT domain. The structural basis for the acyl unit selectivity was uncovered by the first X-ray structure of a fungal SAT domain, highlighted by a covalent hexanoyl thioester intermediate in the SAT active site. Finally, the crystal structure of SAT domain will enable protein engineering efforts aimed at mixing and matching different IPKS modules for the biosynthesis of new compounds.« less
  • Differentiation-inducing factors (DIFs) are well known to modulate formation of distinct communal cell types from identical Dictyostelium discoideum amoebas, but DIF biosynthesis remains obscure. We report complimentary in vivo and in vitro experiments identifying one of two {approx}3,000-residue D. discoideum proteins, termed 'steely', as responsible for biosynthesis of the DIF acylphloroglucinol scaffold. Steely proteins possess six catalytic domains homologous to metazoan type I fatty acid synthases (FASs) but feature an iterative type III polyketide synthase (PKS) in place of the expected FAS C-terminal thioesterase used to off load fatty acid products. This new domain arrangement likely facilitates covalent transfer ofmore » steely N-terminal acyl products directly to the C-terminal type III PKS active sites, which catalyze both iterative polyketide extension and cyclization. The crystal structure of a steely C-terminal domain confirms conservation of the homodimeric type III PKS fold. These findings suggest new bioengineering strategies for expanding the scope of fatty acid and polyketide biosynthesis.« less