The Role of the Wheat Reduced height (Rht)-DELLA Mutants and Associated Hormones in Infection by Claviceps purpurea, the Causal Agent of Ergot.

Partial resistance to the biotrophic fungal pathogen Claviceps purpurea, causal agent of ergot, has been found that colocates with mutant alleles of the wheat Reduced height (Rht) loci on chromosomes 4B and 4D. These Rht loci represent the wheat orthologs of the Arabidopsis Della genes. To investigate the role of the Rht mutant DELLA proteins in ergot resistance, we assessed C. purpurea infection in wheat near-isogenic lines (NILs) carrying the gibberellic acid (GA)-insensitive semidwarf alleles Rht-B1b and Rht-D1b and the severe dwarf alleles Rht-B1c and Rht-D1c. NILs of the GA-sensitive alleles Rht8 (chromosome 2D) and Rht12 (chromosome 5A) were also included. A general trend toward increased resistance to C. purpurea, with smaller and lighter sclerotia, was observed on the NILs Rht-B1b, Rht-D1b, Rht-B1c, and Rht-D1c, and also on Rht8. Levels of the bioactive GA4 and the auxin indole-3-acetic acid increased after inoculation with C. purpurea, following similar patterns and implicating a potential auxin-mediated induction of GA biosynthesis. In contrast, jasmonic acid (JA) levels fell in the parental lines 'Mercia' and 'Maris Huntsman' after inoculation with C. purpurea, but increased in all the Rht-mutant NILs. Inoculation with C. purpurea did not show any informative changes in the levels of salicylic acid. Our results suggest that GA-mediated degradation of the DELLA proteins and down-regulation of JA-signaling pathways supports infection of wheat by C. purpurea. As these responses are generally associated with necrotrophic fungal pathogens, we propose that the biotroph C. purpurea may have a necrotrophic growth stage.

Reprogramming of the wheat transcriptome in response to infection with Claviceps purpurea, the causal agent of ergot.

BACKGROUND: Ergot, caused by the fungal pathogen Claviceps purpurea, infects the female flowers of a range of cereal crops, including wheat. To understand the interaction between C. purpurea and hexaploid wheat we undertook an extensive examination of the reprogramming of the wheat transcriptome in response to C. purpurea infection through floral tissues (i.e. the stigma, transmitting and base ovule tissues of the ovary) and over time. RESULTS: C. purpurea hyphae were observed to have grown into and down the stigma at 24 h (H) after inoculation. By 48H hyphae had grown through the transmitting tissue into the base, while by 72H hyphae had surrounded the ovule. By 5 days (D) the ovule had been replaced by fungal tissue. Differential gene expression was first observed at 1H in the stigma tissue. Many of the wheat genes differentially transcribed in response to C. purpurea infection were associated with plant hormones and included the ethylene (ET), auxin, cytokinin, gibberellic acid (GA), salicylic acid and jasmonic acid (JA) biosynthetic and signaling pathways. Hormone-associated genes were first detected in the stigma and base tissues at 24H, but not in the transmitting tissue. Genes associated with GA and JA pathways were seen in the stigma at 24H, while JA and ET-associated genes were identified in the base at 24H. In addition, several defence-related genes were differential expressed in response to C. purpurea infection, including antifungal proteins, endocytosis/exocytosis-related proteins, NBS-LRR class proteins, genes involved in programmed cell death, receptor protein kinases and transcription factors. Of particular interest was the identification of differential expression of wheat genes in the base tissue well before the appearance of fungal hyphae, suggesting that a mobile signal, either pathogen or plant-derived, is delivered to the base prior to colonisation. CONCLUSIONS: Multiple host hormone biosynthesis and signalling pathways were significantly perturbed from an early stage in the wheat - C. purpurea interaction. Differential gene expression at the base of the ovary, ahead of arrival of the pathogen, indicated the potential presence of a long-distance signal modifying host gene expression.