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Cytoplasmic dynein1 intermediate-chain2 regulates cellular trafficking and physiopathological development in Magnaporthe oryzae.

ABSTRACT: The cytoplasmic dynein 1, a minus end-directed motor protein, is an essential microtubule-based molecular motor that mediates the movement of molecules to intracellular destinations in eukaryotes. However, the role of dynein in the pathogenesis of Magnaporthe oryzae is unknown. Here, we identified cytoplasmic dynein 1 intermediate-chain 2 genes in M. oryzae and functionally characterized it using genetic manipulations, and biochemical approaches. We observed that targeted the deletion of MoDYNC1I2 caused significant vegetative growth defects, abolished conidiation, and rendered the ΔModync1I2 strains non-pathogenic. Microscopic examinations revealed significant defects in microtubule network organization, nuclear positioning, and endocytosis ΔModync1I2 strains. MoDync1I2 is localized exclusively to microtubules during fungal developmental stages but co-localizes with the histone OsHis1 in plant nuclei upon infection. The exogenous expression of a histone gene, MoHis1, restored the homeostatic phenotypes of ΔModync1I2 strains but not pathogenicity. These findings could facilitate the development of dynein-directed remedies for managing the rice blast disease.

SUBMITTER: Lin L

PROVIDER: S-EPMC9971887 | biostudies-literature | 2023 Feb

REPOSITORIES: biostudies-literature

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Cytoplasmic dynein1 intermediate-chain2 regulates cellular trafficking and physiopathological development in Magnaporthe oryzae.

Lin Lily L Tijjani Ibrahim I Guo Hengyuan H An Qiuli Q Cao Jiaying J Chen Xiaomin X Liu Wende W Wang Zonghua Z Norvienyeku Justice J

iScience 20230210 2

The cytoplasmic dynein 1, a minus end-directed motor protein, is an essential microtubule-based molecular motor that mediates the movement of molecules to intracellular destinations in eukaryotes. However, the role of dynein in the pathogenesis of Magnaporthe oryzae is unknown. Here, we identified cytoplasmic dynein 1 intermediate-chain 2 genes in M. oryzae and functionally characterized it using genetic manipulations, and biochemical approaches. We observed that targeted the delet ...[more]

PMID: 36866040

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Project description:Fungi are rich sources of secondary metabolites of pharmaceutical importance, such as antibiotics, antitumor agents, and immunosuppressants, as well as of harmful toxins. Secondary metabolites play important roles in the development and pathogenesis of fungi. LaeA is a global regulator of secondary metabolism and was originally reported in Aspergillus nidulans; however, its role in secondary metabolism in Magnaporthe oryzae has not yet been reported. Here, we investigated the role of a gene homologous to LAEA (loss of AflR expression) of Aspergillus spp. in Magnaporthe oryzae, named M. oryzae LAEA (MoLAEA). Studies on MoLAEA overexpression and knockdown strains have suggested that this gene acts as a negative regulator of sporulation and melanin synthesis. However, it is not involved in the growth and pathogenesis of M. oryzae Transcriptomic data indicated that MoLAEA regulated genes involved in secondary metabolism. Interestingly, we observed (for the first time, to our knowledge) that this gene is involved in benzylpenicillin (penicillin G) synthesis in M. oryzae Overexpression of MoLAEA increased penicillin G production, whereas the silenced strain showed a complete absence of penicillin G compared to its presence in the wild type. We also observed that MoLaeA interacted with MoVeA, a velvet family protein involved in fungal development and secondary metabolism, in the nucleus. This study showed that though MoLAEA may not make any contribution in rice blast fungal pathogenesis, it regulates secondary metabolism in M. oryzae and thus can be further studied for identifying other new uncharacterized metabolites in this fungus.IMPORTANCE M. oryzae causes blast disease, the most serious disease of cultivated rice affecting global rice production. The genome of M. oryzae has been shown to have a number of genes involved in secondary metabolism, but most of them are uncharacterized. In fact, compared to studies of other filamentous fungi, hardly any work has been done on secondary metabolism in M. oryzae It is shown here (for the first time, to our knowledge) that penicillin G is being synthesized in M. oryzae and that MoLAEA is involved in this process. This is the first step in understanding the penicillin G biosynthesis pathway in M. oryzae This study also unraveled the details of how MoLaeA works by forming a nuclear complex with MoVeA in M. oryzae, thus indicating functional conservation of such a gene across filamentous fungi. All these findings open up avenues for more relevant investigations on the genetic regulation of secondary metabolism in M. oryzae.

Project description:Acetylation and deacetylation of histones are key epigenetic mechanisms for gene regulation in response to environmental stimuli. RPD3 is a well-conserved class I histone deacetylase (HDAC) that is involved in diverse biological processes. Here, we investigated the roles of the Magnaporthe oryzae RPD3 (MoRPD3) gene, an ortholog of Saccharomyces cerevisiae Rpd3, during development and pathogenesis in the model plant-pathogenic fungus Magnaporthe oryzae. We demonstrated that the MoRPD3 gene is able to functionally complement the yeast Rpd3 deletion mutant despite the C-terminal extension of the MoRPD3 protein. MoRPD3 localizes primarily to the nuclei of vegetative hyphae, asexual spores, and invasive hyphae. Deletion of MoRPD3 appears to be lethal. Depletion of MoRPD3 transcripts via gene silencing (MoRPD3kd, where "kd" stands for "knockdown") has opposing effects on asexual and sexual reproduction. Although conidial germination and appressorium formation rates of the mutants were almost comparable to those of the wild type, in-depth analysis revealed that the appressoria of mutants are smaller than those of the wild type. Furthermore, the MoRPD3kd strain shows a significant reduction in pathogenicity, which can be attributed to the delay in appressorium-mediated penetration and impaired invasive growth. Interestingly, MoRPD3 does not regulate potassium transporters, as shown for Rpd3 of S. cerevisiae. However, it functioned in association with the target of rapamycin (TOR) kinase pathway, resulting in the dependency of appressorium formation on hydrophilic surfaces and on TOR's inhibition by MoRPD3. Taken together, our results uncovered distinct and evolutionarily conserved roles of MoRPD3 in regulating fungal reproduction, infection-specific development, and virulence. IMPORTANCE RPD3 is an evolutionarily conserved class I histone deacetylase (HDAC) that plays a pivotal role in diverse cellular processes. In filamentous fungal pathogens, abrogation of the gene encoding RPD3 results in either lethality or severe growth impairment, making subsequent genetic analyses challenging. Magnaporthe oryzae is a causal agent of rice blast disease, which is responsible for significant annual yield losses in rice production. Here, we characterized the RPD3 gene of M. oryzae (MoRPD3) in unprecedented detail using a gene-silencing approach. We provide evidence that MoRPD3 is a bona fide HDAC regulating fungal reproduction and pathogenic development by potentially being involved in the TOR-mediated signaling pathway. To the best of our knowledge, this work is the most comprehensive genetic dissection of RPD3 in filamentous fungal pathogens. Our work extends and deepens our understanding of how an epigenetic factor is implicated in the development and virulence of fungal pathogens of plants.

Dataset Information

Cytoplasmic dynein1 intermediate-chain2 regulates cellular trafficking and physiopathological development in Magnaporthe oryzae.

Publications

Cytoplasmic dynein1 intermediate-chain2 regulates cellular trafficking and physiopathological development in <i>Magnaporthe oryzae</i>.

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