Reprogramming of the Wheat Transcriptome in Response to Infection with Claviceps Purpurea, the Causal Agent of Ergot

Abstract

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 hours (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 By 5 days (D) the ovule had been replaced by fungal tissue. Significant 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-associated 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 significant 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 hormonal biosynthesis and signalling pathways were significantly perturbed from an early stage in the wheat – C. purpurea interaction. Significant 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.

Maternal differences for the reaction to ergot in unfertilized hybrid rye (Secale cereale)

“…Thus, it is indicated that a maternal mechanism based on a resistance response of the ovary is existing because in our study the three other factors for the ergot reaction (1) influence of pollen, (2) ease of restoration of the female, and (3) morphological and/or escape mechanisms were excluded. This is supported by the fact that a significant differential gene expression at the base of the ovary was detected that included the activation of defense-related genes ahead of the arrival of the pathogen in the wheat-Claviceps interaction (Boyd et al, 2020).…”

“…Besides pollen-fertility restoration, ergot infection in rye is affected by (1) morphological measures leading to a disease escape like closed flowering, small aperture angle of the glumes or a short glume opening period, (2) the ease of restoration by the female and (3) a resistance mechanism in the ovaries that has, however, not been fully proven, yet (Menzies & Turkington, 2015;Miedaner & Geiger, 2015). Recently, transcriptomic analyses in wheat showed that shortly after the conidia have reached the pistil, plant resistance is already activated (Boyd et al, 2020). Small, but significant differences of ergot severity were already shown for fully male-sterile entries under pollen isolation in rye (Miedaner et al, 2010b) and pearl millet (Willingale et al, 1986).…”