The basidiomycete Sporisorium scitamineum causes sugarcane smut disease, leading to a significant impairment in the quality and yield of sugarcane. Polyamines affect the intracellular redox balance, which is important for the pathogenic development of S. scitamineum, including sexual mating, dikaryotic hyphae growth, and host invasion. In the present study, we identified a polyamine transporter, SsTPO1, in S. scitamineum. Deletion or overexpression of SsTPO1 led to the disruption of intracellular levels of putrescine, spermidine, and spermine in opposite directions. SsTPO1-based polyamine homeostasis contributes to dikaryotic hyphal growth and host invasion after sexual mating, likely by affecting the cAMP-PKA signaling pathway and collaboratively regulating redox homeostasis. Environmental pH affected SsTPO1-mediated polyamine transport, so S. scitamineum hyphae growth favoured neutral to alkaline environments rather than acidic conditions. The SsTPO1-based polyamine transport also participates in stress resistance and autophagy induction. In summary, our work revealed that SsTPO1 facilitates polyamine transport to regulate cell growth, differentiation, and fungal pathogenicity in S. scitamineum.

Rice blast is one of the most devastating diseases and a serious threat to global food security. It is caused by the ascomycetous fungus Magnaporthe oryzae. During the pathogenic development of M. oryzae, ferroptotic death of conidial cells is critical for appressorium formation and infection to host rice. In this study, we identified and functionally characterised orthologs of fatty acid desaturase (Fad2) and acyl-CoA synthetase long-chain family (Acsl4) in M. oryzae. Pathogenicity was impaired in the fad2Δ or acsl4Δ mutant and targeted lipidomics analysis demonstrated that Fad2 and Acsl4 were involved in the production of polyunsaturated fatty acids (PUFAs)-containing phospholipids (PUFA-PLs) potentially contributing to ferroptosis. Treatment with FeCl₃, an oxidative agent to cause lipid peroxidation, could partially restore fad2Δ pathogenicity. Fad2 was also found to potentially interact with proteins involved in cellular redox homoeostasis. Overall, our results elucidate the role of PUFA-PLs biosynthesis in fungal cell death and fungal pathogenicity, providing a theoretical basis for the development of specific pesticides/drugs targeting ferroptosis caused by lipid peroxidation.

Rice blast, caused by Magnaporthe oryzae, is a fungal disease that causes devastating damage to rice production worldwide. During infection, pathogens secrete effector proteins that modulate plant immunity. Disulfide bond formation catalyzed by protein disulfide isomerases (PDI) is essential for protein folding and maturation. However, the biological function of Pdi1 in M. oryzae has not yet been characterized. In this study, we identified the endoplasmic reticulum (ER)-located protein, MoPdi1, in M. oryzae. MoPdi1 regulates conidiation, cell wall stress, and pathogenicity of M. oryzae. Furthermore, the CGHC active sites in the a and a' redox domain of MoPdi1 were essential for the biological function of MoPDI1. Further tests demonstrated that MoPdi1 was involved in the regulation of ER stress and positively regulated ER phagy. We also found that MoPdi1 interacted with MoHut1. Deletion of MoPDI1 led to the bereft of MoHut1 dimerization, which depends on the formation of disulfide bonds. In addition, MoPdi1 affected the normal secretion of the cytoplasmic effector AVR-Pia. We provided evidence that MoHut1 is important for the vegetative growth, conidiation, and pathogenicity in M. oryzae. Therefore, our findings could provide a suitable target point for designing antifungal agrochemicals against rice blast fungus.

Phytohormones (also named as plant hormones) are chemicals produced by plants in order to modulate various aspects of plant development, stress responses and defence. Recent studies revealed that fungi can also produce phytohormones or phytohormone-mimiking molecules, while it remains poorly understood about the details in the role and regulatory mechanism of such fungal produced phytohormonal molecules in plant-fungus interactions. The rice-blast fungus Magnaporthe oryzae imposes a great threat to global food security. Intensive investigation has been conducted to elucidate M. oryzae pathogenicity and rice (Oryza sativa L.) defense mechanism against blast disease, in order to provide theoretical basis and/or identify potential target(s) for developing novel disease control strategies, as well as for breeding of resistance varieties. Phytohormones have been demonstrated to play conserved and divergent roles in fine-tuning the balance of rice growth and immunity towards M. oryzae. Meanwhile, M. oryzae evolved elaborate strategy to manipulate the rice phytohormones metabolism, or even directly produce and secrete phytohormones, during their invasion process. In this review, we discuss the chemical communication in term of phytohormones in M. oryzae-rice pathosystem.