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

Eleni Tente,Nelzo Ereful,Donal M. O’Sullivan,Anyela Camargo Rodriguez,Anna Gordon,Lesley A. Boyd,Paul Grant

doi:10.1186/s12870-021-03086-3

Abstract

BackgroundErgot, 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.ResultsC. 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 By 5 days (D) the ovule had been replaced by fungal tissue.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.ConclusionsMultiple 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.

Highlights

Ergot, caused by the fungal pathogen Claviceps purpurea, infects the female flowers of a range of cereal crops, including wheat
Microscopic examination of Claviceps purpurea infection of wheat The percentage of ovaries with C. purpurea hyphae in stigma, transmitting and base tissues were scored across time points (Table 1)
While sclerotia can be removed from contaminated grain loads by physical cleaning methods: colour sorting and gravity tables [4,5,6], we know very little about the interactions that occur between wheat and C. purpurea at a cellular and molecular genetic level

Summary

Introduction

Ergot, caused by the fungal pathogen Claviceps purpurea, infects the female flowers of a range of cereal crops, including wheat. Ergot, caused by the fungal pathogen Claviceps purpurea, is an ear disease of grasses and cereal, and infects a number of economically important cereal crops, including wheat, barley and rye [1, 2]. Sclerotia contain a range of ergot alkaloids that are highly toxic to humans and animals [4, 7]. These alkaloids are responsible for the condition ergotism, which during the Middle Ages was known as St Anthony’s Fire. Recent findings suggest that ergot alkaloids, produced by the fungus and found at high concentrations in sclerotia, can find their way onto otherwise “healthy” grain [9]

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