An expanded subfamily of G-protein-coupled receptor genes in Fusarium graminearum required for wheat infection

Abstract

The cAMP–PKA and MAP kinase pathways are essential for plant infection in the wheat head blight fungus Fusarium graminearum. To identify upstream receptors of these well-conserved signalling pathways, we systematically characterized the 105 G-protein-coupled receptor (GPCR) genes. Although none were required for vegetative growth, five GPCR genes (GIV1GIV5) significantly upregulated during plant infection were important for virulence. The giv1 mutant was defective in the formation of specialized infection structures known as infection cushions, which was suppressed by application of exogenous cAMP and dominant active FST7 MEK kinase. GIV1 was important for the stimulation of PKA and Gpmk1 MAP kinase by compounds in wheat spikelets. GIV2 and GIV3 were important for infectious growth after penetration. Invasive hyphae of the giv2 mutant were defective in cell-to-cell spreading and mainly grew intercellularly in rachis tissues. Interestingly, the GIV2–GIV5 genes form a phylogenetic cluster with GIV6, which had overlapping functions with GIV5 during pathogenesis. Furthermore, the GIV2–GIV6 cluster is part of a 22-member subfamily of GPCRs, with many of them having in planta-specific upregulation and a common promoter element; however, only three subfamily members are conserved in other fungi. Taken together, F. graminearum has an expanded subfamily of infection-related GPCRs for regulating various infection processes.

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Fig. 1: Expression profiles of the 105 GPCR genes and mutants with defects in plant infection.
Fig. 2: Defects of the giv1, giv2 and giv3 mutant in infection-related morphogenesis and infectious growth.
Fig. 3: Assays for the effects of wheat spikelets on PKA activities and activation of MAPKs.
Fig. 4: Assays for the effects of dominant active FST7 and nuclear localization of Gpmk1–GFP.
Fig. 5: GPCR genes of the EIG subfamily.

Data availability

The data that support the findings of this study are available from the corresponding author and C. J. (cjiang@nwafu.edu.cn) upon request. RNA-seq data generated in this study are accessible under the accession numbers SRR8568982SRR8568984 and SRR8569386SRR8569394.

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Acknowledgements

We thank W. Wang, R. Hei, H. Jiang, J. Ren, P. Huang, C. Wu and C. Wang for assistance with generating GPCR gene deletion mutants. We also thank L. Dunkle and P. Goldsbrough at Purdue University for critical reading of this manuscript. This work was supported by grants from the National Natural Science Foundation of China (no. 31772114), NSWBSI, USDA NIFA (Award no. 2013-68004-20378), Tang Scholar and the Natural Science Basic Research Plan in Shaanxi Province of China (no. 2017JM3001).

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J.-R.X. and C.J. designed the research and wrote the paper. C.J., S.C., Z.W., H.X., J.L., G.W., M.D., C.G., C.F. and C.H. performed the experiments. C.J., H.L. and Q.W. analysed the data.

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Correspondence to Jin-Rong Xu.

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Jiang, C., Cao, S., Wang, Z. et al. An expanded subfamily of G-protein-coupled receptor genes in Fusarium graminearum required for wheat infection. Nat Microbiol 4, 1582–1591 (2019). https://doi.org/10.1038/s41564-019-0468-8

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