The transcriptional landscape of plant infection by the rice blast fungus Magnaporthe oryzae reveals distinct families of temporally co-regulated and structurally conserved effectors.

The rice blast fungus Magnaporthe oryzae causes a devastating disease that threatens global rice (Oryza sativa) production. Despite intense study, the biology of plant tissue invasion during blast disease remains poorly understood. Here we report a high-resolution transcriptional profiling study of the entire plant-associated development of the blast fungus. Our analysis revealed major temporal changes in fungal gene expression during plant infection. Pathogen gene expression could be classified into 10 modules of temporally co-expressed genes, providing evidence for the induction of pronounced shifts in primary and secondary metabolism, cell signaling, and transcriptional regulation. A set of 863 genes encoding secreted proteins are differentially expressed at specific stages of infection, and 546 genes named MEP (Magnaportheeffector protein) genes were predicted to encode effectors. Computational prediction of structurally related MEPs, including the MAX effector family, revealed their temporal co-regulation in the same co-expression modules. We characterized 32 MEP genes and demonstrate that Mep effectors are predominantly targeted to the cytoplasm of rice cells via the biotrophic interfacial complex and use a common unconventional secretory pathway. Taken together, our study reveals major changes in gene expression associated with blast disease and identifies a diverse repertoire of effectors critical for successful infection.

Genomic surveillance uncovers a pandemic clonal lineage of the wheat blast fungus.

Wheat, one of the most important food crops, is threatened by a blast disease pandemic. Here, we show that a clonal lineage of the wheat blast fungus recently spread to Asia and Africa following two independent introductions from South America. Through a combination of genome analyses and laboratory experiments, we show that the decade-old blast pandemic lineage can be controlled by the Rmg8 disease resistance gene and is sensitive to strobilurin fungicides. However, we also highlight the potential of the pandemic clone to evolve fungicide-insensitive variants and sexually recombine with African lineages. This underscores the urgent need for genomic surveillance to track and mitigate the spread of wheat blast outside of South America and to guide preemptive wheat breeding for blast resistance.

Correction: Genomic surveillance uncovers a pandemic clonal lineage of the wheat blast fungus.

[This corrects the article DOI: 10.1371/journal.pbio.3002052.].

Characterization of Blast Resistance in a Diverse Rice Panel from Sub-Saharan Africa.

There is a recent unparalleled increase in demand for rice in sub-Saharan Africa, yet its production is affected by blast disease. Characterization of blast resistance in adapted African rice cultivars can provide important information to guide growers and rice breeders. We used molecular markers for known blast resistance genes (Pi genes; n = 21) to group African rice genotypes (n = 240) into similarity clusters. We then used greenhouse-based assays to challenge representative rice genotypes (n = 56) with African isolates (n = 8) of Magnaporthe oryzae which varied in virulence and genetic lineage. The markers grouped rice cultivars into five blast resistance clusters (BRC) which differed in foliar disease severity. Using stepwise regression, we found that the Pi genes associated with reduced blast severity were Pi50 and Pi65, whereas Pik-p, Piz-t, and Pik were associated with increased susceptibility. All rice genotypes in the most resistant cluster, BRC 4, possessed Pi50 and Pi65, the only genes that were significantly associated with reduced foliar blast severity. Cultivar IRAT109, which contains Piz-t, was resistant against seven African M. oryzae isolates, whereas ARICA 17 was susceptible to eight isolates. The popular Basmati 217 and Basmati 370 were among the most susceptible genotypes. These findings indicate that most tested genes were not effective against African blast pathogen collections. Pyramiding genes in the Pi2/9 multifamily blast resistance cluster on chromosome 6 and Pi65 on chromosome 11 could confer broad-spectrum resistance capabilities. To gain further insights into genomic regions associated with blast resistance, gene mapping could be conducted with resident blast pathogen collections. [Formula: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Chitosan inhibits septin-mediated plant infection by the rice blast fungus Magnaporthe oryzae in a protein kinase C and Nox1 NADPH oxidase-dependent manner.

Chitosan is a partially deacetylated linear polysaccharide composed of ß-1,4-linked units of d-glucosamine and N-acetyl glucosamine. As well as a structural component of fungal cell walls, chitosan is a potent antifungal agent. However, the mode of action of chitosan is poorly understood. Here, we report that chitosan is effective for control of rice blast disease. Chitosan application impairs growth of the blast fungus Magnaporthe oryzae and has a pronounced effect on appressorium-mediated plant infection. Chitosan inhibits septin-mediated F-actin remodelling at the appressorium pore, thereby preventing repolarization of the infection cell. Chitosan causes plasma membrane permeabilization of M. oryzae and affects NADPH oxidase-dependent synthesis of reactive oxygen species, essential for septin ring formation and fungal pathogenicity. We further show that toxicity of chitosan to M. oryzae requires the protein kinase C-dependent cell wall integrity pathway, the Mps1 mitogen-activated protein kinase and the Nox1 NADPH oxidase. A conditionally lethal, analogue (PP1)-sensitive mutant of Pkc1 is partially remediated for growth in the presence of chitosan, while ∆nox1 mutants increase their glucan : chitin cell wall ratio, rendering them resistant to chitosan. Taken together, our data show that chitosan is a potent fungicide which requires the cell integrity pathway, disrupts plasma membrane function and inhibits septin-mediated plant infection.

Integrated Strategies for Durable Rice Blast Resistance in Sub-Saharan Africa.

Rice is a key food security crop in Africa. The importance of rice has led to increasing country-specific, regional, and multinational efforts to develop germplasm and policy initiatives to boost production for a more food-secure continent. Currently, this critically important cereal crop is predominantly cultivated by small-scale farmers under suboptimal conditions in most parts of sub-Saharan Africa (SSA). Rice blast disease, caused by the fungus Magnaporthe oryzae, represents one of the major biotic constraints to rice production under small-scale farming systems of Africa, and developing durable disease resistance is therefore of critical importance. In this review, we provide an overview of the major advances by a multinational collaborative research effort to enhance sustainable rice production across SSA and how it is affected by advances in regional policy. As part of the multinational effort, we highlight the importance of joint international partnerships in tackling multiple crop production constraints through integrated research and outreach programs. More specifically, we highlight recent progress in establishing international networks for rice blast disease surveillance, farmer engagement, monitoring pathogen virulence spectra, and the establishment of regionally based blast resistance breeding programs. To develop blast-resistant, high yielding rice varieties for Africa, we have established a breeding pipeline that utilizes real-time data of pathogen diversity and virulence spectra, to identify major and minor blast resistance genes for introgression into locally adapted rice cultivars. In addition, the project has developed a package to support sustainable rice production through regular stakeholder engagement, training of agricultural extension officers, and establishment of plant clinics.