Membrane fluidity control by the Magnaporthe oryzae acyl-CoA binding protein sets the thermal range for host rice cell colonization.

Following leaf cuticle penetration by specialized appressorial cells, the devastating blast fungus Magnaporthe oryzae grows as invasive hyphae (IH) in living rice cells. IH are separated from host cytoplasm by plant-derived membranes forming an apoplastic compartment and a punctate biotrophic interfacial complex (BIC) that mediate the molecular host-pathogen interaction. What molecular and cellular processes determine the temperature range for this biotrophic growth stage is an unanswered question pertinent to a broader understanding of how phytopathogens may cope with environmental stresses arising under climate change. Here, we shed light on thermal adaptation in M. oryzae by disrupting the ACB1 gene encoding the single acyl-CoA-binding protein, an intracellular transporter of long-chain acyl-CoA esters. Loss of ACB1 affected fatty acid desaturation levels and abolished pathogenicity at optimal (26°C) and low (22°C) but not elevated (29°C) infection temperatures (the latter following post-penetration shifts from 26°C). Relative to wild type, the Δacb1 mutant strain exhibited poor vegetative growth and impaired membrane trafficking at 22°C and 26°C, but not at 29°C. In planta, Δacb1 biotrophic growth was inhibited at 26°C–which was accompanied by a multi-BIC phenotype—but not at 29°C, where BIC formation was normal. Underpinning the Δacb1 phenotype was impaired membrane fluidity at 22°C and 26°C but not at elevated temperatures, indicating Acb1 suppresses membrane rigidity at optimal- and suboptimal- but not supraoptimal temperatures. Deducing a temperature-dependent role for Acb1 in maintaining membrane fluidity homeostasis reveals how the thermal range for rice blast disease is both mechanistically determined and wider than hitherto appreciated. Author summary: A major challenge to global food security lies in anticipating phytopathogen spread due to climate change. Relatedly, how temperature affects pathogen-host plant interactions at the molecular level is poorly understood. Here, using molecular, cellular and biochemical approaches, we investigated thermal adaptation by the devastating rice blast fungus Magnaporthe oryzae. We show that mediation of fungal membrane fluidity by the intracellular lipid-intermediate transporter Acb1 is critical for both axenic growth and host plant cell-associated invasive hyphal growth at optimal and low environmental temperatures. However, at elevated temperatures, Acb1 is dispensable. By uncovering Acb1 as a temperature-dependent determinant of plant cell colonization, we reveal the molecular strategies by which a fungal pathogen adapts to environmental temperatures during host infection. [ABSTRACT FROM AUTHOR]