Parasitic modulation of host development by ubiquitin-independent protein degradation

• Published in: Cell Vol. 184; no. 20; pp. 5201 - 5214.e12
• Main Authors: Huang, Weijie, MacLean, Allyson M., Sugio, Akiko, Maqbool, Abbas, Busscher, Marco, Cho, Shu-Ting, Kamoun, Sophien, Kuo, Chih-Horng, Immink, Richard G.H., Hogenhout, Saskia A.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 30-09-2021; Elsevier; Cell Press
• Subjects: Amino Acid Sequence; Animals; Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis - parasitology; Arabidopsis Proteins - chemistry; Arabidopsis Proteins - metabolism; Cellular Biology; developmental phase transition; Ecology, environment; Genetic Engineering; Host-Parasite Interactions - physiology; Humans; insect vectors; Insecta - physiology; Life Sciences; Models, Biological; mycoplasma; Nicotiana; non-culturable bacteria; Parasites - physiology; Phenotype; phloem; Photoperiod; Phylogeny; Phytoplasma - physiology; Plant Development; plant pathogen; Plant Shoots - growth & development; Plants, Genetically Modified; Proteasome Endopeptidase Complex - metabolism; Protein Stability; Proteolysis; Reproduction; Symbiosis; targeted protein degradation; Transcription Factors - metabolism; Transcription, Genetic; ubiquitin-proteasome system; Ubiquitins - metabolism; vasculature-colonizing bacteria; zombie plant; ubiquitin-proteasome system; plant pathogen; zombie plant; insect vectors; non-culturable bacteria; developmental phase transition; phloem; vasculature-colonizing bacteria; targeted protein degradation; mycoplasma
• ISSN: 0092-8674; 1097-4172
• DOI: 10.1016/j.cell.2021.08.029

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.
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•Phytoplasma SAP05 proteins bind plant SPL and GATA transcription factors and RPN10•SAP05 mediates degradation of SPLs and GATAs in a ubiquitin-independent manner•SAP05 decouples plant developmental transitions and induces witches’ broom symptoms•Engineering of plant RPN10 confers resistance to SAP05 activities
A virulence factor from an insect-vectored parasitic phytoplasma induces ubiquitin receptor-mediated developmental changes in the plant host that favor pathogenesis. This effector-receptor interaction can be modulated to engineer plants resistant to parasitic infection.