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. 2023 Nov 30;19(11):e1011762.
doi: 10.1371/journal.ppat.1011762. eCollection 2023 Nov.

The RNA world of fungal pathogens

Srimeenakshi Sankaranarayanan  1 , Seomun Kwon  1 , Kai Heimel  2 , Michael Feldbrügge  1
Affiliations

The RNA world of fungal pathogens

Srimeenakshi Sankaranarayanan et al. PLoS Pathog. .
No abstract available

PubMed Disclaimer

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. In fungal hyphae, mRNA-dependent processes drive membrane trafficking.
Schematic depiction of U. maydis hyphae (left) interacting with its plant host, Zea mays (right). Distinct cellular processes within the hyphae have been marked and magnified. (A) Early endosomes act as a platform for the transport of mRNAs. Rrm4 (red) facilitates the mRNA transport by hitchhiking onto Rab5-positive early endosomes. Interactions between Rrm4, the poly (A)-binding protein, Pab1, and the FYVE domain-containing adapter protein Upa1 enable the attachment of mRNAs to early endosomes. The scaffold protein Upa2 stabilizes the transport complex. This bidirectional movement relies on motor proteins, kinesin, and dynein, traveling along antiparallel microtubules. The local translation of the cargo mRNAs like septin (blueish gray) on early endosomes is essential to generate higher-order septin filaments extending from the hyphal tip. (B) Khd4 (red) orchestrates membrane trafficking by regulating the subcellular levels of regulatory proteins crucial for this process. The RBP coordinates the destabilization of mRNAs encoding membrane trafficking regulators (gray) into an mRNA regulon through the recognition of the AUACCC motif present in their 3′ UTRs. This mRNA decay process determines the induction kinetics of these mRNAs, fine-tuning their steady-state levels following transcriptional induction. Pacmans in bluish-gray depict mRNA decay factors. (C) Unconventional splicing of cib1 mRNA in the cytoplasm elicits the UPR, required to preserve ER homeostasis during infection. Upon ER stress, the ER membrane-localized Ire1 kinase/RNAse (red) is activated through its direct interaction with unfolded or misfolded proteins (orange) or by reduced Ire1-Bip1 interaction. This activation prompts the splicing of an intron from the cib1 mRNA (brown) in the cytoplasm. The resulting spliced cib1 mRNA is translationally active, leading to the production of the Cib1 protein (brown)—a bZIP transcription factor, which in turn, induces the expression of UPR genes to restore ER homeostasis and secretion. These include genes such as pit1, pit2, and pep1, encoding effector proteins vital for fungal infection. (D, E) Posttranscriptional regulation determines the dual targeting of peroxisomal proteins. (D) Alternative splicing of gapdh mRNA leads to the expression of an isoform containing peroxisomal targeting sequence (blue), which facilitates peroxisomal targeting after translation. The spliceosome complex is represented in red (gapdh-glyceraldehyde-3-phosphate dehydrogenase). (E) Ribosomal readthrough past stop codon (red box) of pgk1 mRNA integrates cryptic peroxisomal targeting sequence (blue) at the C-terminus, facilitating peroxisomal entry. The ribosome executing the stop-codon readthrough is depicted in red (pgk1-3-phosphoglycerate kinase). (F) Fungal mRNAs (red) encoding effector proteins are packaged within EVs as a means to transport into the host plant. The internalization of these fungal EVs into the plant host (light green) might be aided by clathrin-mediated endocytosis. Following their entry into plant cells, the delivered fungal mRNAs are subsequently translated using the plant’s own translation machinery, thus outsourcing the production of fungal effector proteins within the plant for pathogenic development. In addition to RNAs, the cargoes of fungal EVs encompass proteins, and secondary metabolites, both depicted in gray.
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References

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