Parasitic modulation of host development by ubiquitin-independent protein degradation

Cell. 2021 Sep 30;184(20):5201-5214.e12. doi: 10.1016/j.cell.2021.08.029. Epub 2021 Sep 17.

Abstract

Certain obligate parasites induce complex and substantial phenotypic changes in their hosts in ways that favor their transmission to other trophic levels. However, the mechanisms underlying these changes remain largely unknown. Here we demonstrate how SAP05 protein effectors from insect-vectored plant pathogenic phytoplasmas take control of several plant developmental processes. These effectors simultaneously prolong the host lifespan and induce witches' broom-like proliferations of leaf and sterile shoots, organs colonized by phytoplasmas and vectors. SAP05 acts by mediating the concurrent degradation of SPL and GATA developmental regulators via a process that relies on hijacking the plant ubiquitin receptor RPN10 independent of substrate ubiquitination. RPN10 is highly conserved among eukaryotes, but SAP05 does not bind insect vector RPN10. A two-amino-acid substitution within plant RPN10 generates a functional variant that is resistant to SAP05 activities. Therefore, one effector protein enables obligate parasitic phytoplasmas to induce a plethora of developmental phenotypes in their hosts.

Keywords: developmental phase transition; insect vectors; mycoplasma; non-culturable bacteria; phloem; plant pathogen; targeted protein degradation; ubiquitin-proteasome system; vasculature-colonizing bacteria; zombie plant.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Arabidopsis / genetics
  • Arabidopsis / growth & development*
  • Arabidopsis / parasitology*
  • Arabidopsis Proteins / chemistry
  • Arabidopsis Proteins / metabolism
  • Genetic Engineering
  • Host-Parasite Interactions / physiology*
  • Humans
  • Insecta / physiology
  • Models, Biological
  • Nicotiana
  • Parasites / physiology*
  • Phenotype
  • Photoperiod
  • Phylogeny
  • Phytoplasma / physiology
  • Plant Development
  • Plant Shoots / growth & development
  • Plants, Genetically Modified
  • Proteasome Endopeptidase Complex / metabolism
  • Protein Stability
  • Proteolysis*
  • Reproduction
  • Transcription Factors / metabolism
  • Transcription, Genetic
  • Ubiquitins / metabolism*

Substances

  • Arabidopsis Proteins
  • Transcription Factors
  • Ubiquitins
  • Proteasome Endopeptidase Complex