Parasite co-opts a ubiquitin receptor to induce a plethora of developmental changes

Abstract

Obligate parasites can induce complex and substantial phenotypic changes in their hosts in ways that favour their transmission to other trophic levels. However, 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 to simultaneously prolong host lifespan and induce witch's 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 uniquely relies on hijacking the plant ubiquitin receptor RPN10 independently of substrate lysine 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.

Comparative Genome Analysis of ‘Candidatus Phytoplasma luffae’ Reveals the Influential Roles of Potential Mobile Units in Phytoplasma Evolution

“…An important feature of phytoplasmas is their ability to modulate host plant development through effectors, which are small secreted proteins (Sugio et al, 2011b; Sugio and Hogenhout, 2012). To date, four phytoplasma effectors have been experimentally characterized, including SAP05 (Gamboa et al, 2019; Huang and Hogenhout, 2019; Huang et al, 2021), SAP11/SWP1 (Bai et al, 2009; Sugio et al, 2011a; Lu et al, 2014; Chang et al, 2018; Wang et al, 2018c, 2018b), SAP54/PHYL1 (MacLean et al, 2011; Maejima et al, 2014; Orlovskis and Hogenhout, 2016), and TENGU (Hoshi et al, 2009; Sugawara et al, 2013; Minato et al, 2014). The expanded genome sequence availability allowed us to investigate the phylogenetic distribution of homologous effector genes among diverse phytoplasmas.…”

Novel effector recognition capacity engineered into a paired NLR complex

“…S1). For example, the phytoplasma effector SAP11 interacts with and destabilizes multiple TEOSINTE BRANCHED 1-CYCLOIDEA-PROLIFERATING CELL FACTOR (TCP) transcription factors [36][37][38] , SAP54 directly binds and promotes degradation of MADS domain transcription factor (MTF) family proteins, including SEP3, AP1 or SOC1 39 , and SAP05 directly binds the zinc finger domains of SQUAMOSA promoter-binding proteins (SBP) and GATA domain transcription factors and mediates their degradation 35 . Pseudomonas syringae Type III Effector HopBB1 promotes the degradation of TCP14 by direct binding 40 , and HopX1 eliminates JAZ proteins by cleaving the ZIM domain 41 .…”

“…To create this, we selected several effectors and their corresponding targets. SAP05, an effector from insect-transmitted phytopathogenic bacteria, degrades GATA zinc finger domain transcription factor proteins 35 . We fused a GATA SAP05-dependent degron domain to RRS1-R. Co-expression of this fusion protein represses autoimmunity of RRS1-R slh1 ; this is derepressed by coexpression with SAP05, restoring the RRS1-R slh1 -induced-RPS4-dependent hypersensitive response (HR) in transient assays.…”

Spotlight on the Roles of Whitefly Effectors in Insect–Plant Interactions

“…Although the majority of effectors are secreted from salivary glands, effectors may come from other sources as well, including from other organisms. For example, effectors of bacterial plant pathogens such as phytoplasmas promote plant colonization of their insect vectors like leafhoppers, planthoppers, and psyllids (reviewed in Tomkins et al, 2018;Huang et al, 2021). Bemisia tabaci depends on endosymbionts to produce essential amino acids that phloem lacks.…”