An effector of apple proliferation phytoplasma targets TCP transcription factors—a generalized virulence strategy of phytoplasma?

Abstract

The plant pathogen Candidatus Phytoplasma mali (P. mali) is the causative agent of apple proliferation, a disease of increasing importance in apple-growing areas within Europe. Despite its economic importance, little is known about the molecular mechanisms of disease manifestation within apple trees. In this study, we identified two TCP (TEOSINTE BRANCHED/CYCLOIDEA/PROLIFERATING CELL FACTOR) transcription factors of Malus x domestica as binding partners of the P. mali SAP11-like effector ATP_00189. Phytohormone analyses revealed an effect of P. mali infection on jasmonates, salicylic acid and abscisic acid levels, showing that P. mali affects phytohormonal levels in apple trees, which is in line with the functions of the effector assumed from its binding to TCP transcription factors. To our knowledge, this is the first characterization of the molecular targets of a P. mali effector and thus provides the basis to better understand symptom development and disease progress during apple proliferation. As SAP11 homologues are found in several Phytoplasma species infecting a broad range of different plants, SAP11-like proteins seem to be key players in phytoplasmal infection.

TCP Transcription Factors at the Interface between Environmental Challenges and the Plant’s Growth Responses

“…Additionally, jasmonic acid levels in infected Arabidopsis leaves are significantly reduced in comparison with untreated leaves, indicating that the plant’s defense mechanisms are reduced upon infection by the pathogen. A similar effect has been found in apples, where the plant pathogen Candidatus Phytoplasma mali binds to two TCP transcription factors and induces morphogenetic changes that co-occur with reduction of jasmonic acid, salicylic acid, and abscisic acid levels (Janik et al, 2016). Further studies identified the class I TCPs TCP8 and TCP9 as important factors for the expression of ICS1 , which encodes for a key enzyme in salicylic acid synthesis (Wang X.et al, 2015).…”

Arabidopsis TCP Transcription Factors Interact with the SUMO Conjugating Machinery in Nuclear Foci

“…Other groups also identified many TCPs as interactors in their Y2H screens with unrelated baits, suggesting that these TCPs readily interact in the Y2H. For example, TCP8, TCP14, and TCP15 were found to interact with various effector proteins of unrelated plant pathogens (Sugio et al, 2011 , 2014 ; Weßling et al, 2014 ; Janik et al, 2017 ; Yang et al, 2017 ), but these TCPs also interacted with SUPPRESSOR OF rps4-RLD1 (SRFR1), a negative regulator of effector-triggered immunity (Kim et al, 2014 ). In this latter case, these interactions were only found with one class of TCPs suggesting that they were bona fide interactions.…”

Looking back to look forward: protein–protein interactions and the evolution of development

“…In witches' broom, the phytoplasma effector SAP11 causes the degradation of A. thaliana TCP transcription factors that repress branching and mediate leaf development; this results in branchy plants with crinkly leaves (Sugio et al, 2014). Homologs of these TCP transcription factors and SAP11 also interact in apple and in maize, where phytoplasmas cause witches' broom and disrupted floral development, respectively (Janik et al, 2017;Pecher et al, 2019). Thus, protein-protein interactions between conserved host transcription factors and pathogen effectors can link developmental regulation and proteasome degradation, resulting in large-scale changes to plant form.…”