Phagocytosis underpins the biotrophic lifestyle of intracellular parasites in the class Phytomyxea (Rhizaria)

Andrea Garvetto, Pedro Murúa, Martin Kirchmair, Willibald Salvenmoser, Michaela Hittorf, Stefan Ciaghi, Srilakshmy L. Harikrishnan, Claire M. M. Gachon, John A. Burns, Sigrid Neuhauser

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Abstract

Phytomyxea are intracellular biotrophic parasites infecting plants and stramenopiles, including the agriculturally impactful Plasmodiophora brassicae and the brown seaweed pathogen Maullinia ectocarpii. They belong to the clade Rhizaria, where phagotrophy is the main mode of nutrition. Phagocytosis is a complex trait of eukaryotes, well documented for free-living unicellular eukaryotes and specific cellular types of animals. Data on phagocytosis in intracellular, biotrophic parasites are scant. Phagocytosis, where parts of the host cell are consumed at once, is seemingly at odds with intracellular biotrophy.
Here we provide evidence that phagotrophy is part of the nutritional strategy of Phytomyxea, using morphological and genetic data (including a novel transcriptome of M. ectocarpii). We document intracellular phagocytosis in P. brassicae and M. ectocarpii by transmission electron microscopy and fluorescent in situ hybridization.
Our investigations confirm molecular signatures of phagocytosis in Phytomyxea and hint at a small specialized subset of genes used for intracellular phagocytosis. Microscopic evidence confirms the existence of intracellular phagocytosis, which in Phytomyxea targets primarily host organelles.
Phagocytosis seems to coexist with the manipulation of host physiology typical of biotrophic interactions. Our findings resolve long debated questions on the feeding behaviour of Phytomyxea, suggesting an unrecognized role for phagocytosis in biotrophic interactions.
Original languageEnglish
Article number18828
Number of pages14
JournalNew Phytologist
DOIs
Publication statusPublished - 24 Mar 2023

Keywords

  • algal pathogen
  • Brassicaeae
  • Ectocarpus siliculosus
  • Maullinia ectocarpii
  • phagotrophy
  • plant pathogen
  • Plasmodiophora brassicae
  • trpohic mode

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