Phytoplasma SAP11 effector destabilization of TCP transcription factors differentially impact development and defence of Arabidopsis versus maize

Abstract

Phytoplasmas are insect-transmitted bacterial pathogens that colonize a wide range of plant species, including vegetable and cereal crops, and herbaceous and woody ornamentals. Phytoplasma-infected plants often show dramatic symptoms, including proliferation of shoots (witch’s brooms), changes in leaf shapes and production of green sterile flowers (phyllody). Aster Yellows phytoplasma Witches’ Broom (AY-WB) infects dicots and its effector, secreted AYWB protein 11 (SAP11), was shown to be responsible for the induction of shoot proliferation and leaf shape changes of plants. SAP11 acts by destabilizing TEOSINTE BRANCHED 1-CYCLOIDEA-PROLIFERATING CELL FACTOR (TCP) transcription factors, particularly the class II TCPs of the CYCLOIDEA/TEOSINTE BRANCHED 1 (CYC/TB1) and CINCINNATA (CIN)-TCP clades. SAP11 homologs are also present in phytoplasmas that cause economic yield losses in monocot crops, such as maize, wheat and coconut. Here we show that a SAP11 homolog of Maize Bushy Stunt Phytoplasma (MBSP), which has a range primarily restricted to maize, destabilizes specifically TB1/CYC TCPs. SAP11MBSP and SAP11AYWB both induce axillary branching and SAP11AYWB also alters leaf development of Arabidopsis thaliana and maize. However, only in maize, SAP11MBSP prevents female inflorescence development, phenocopying maize tb1 lines, whereas SAP11AYWB prevents male inflorescence development and induces feminization of tassels. SAP11AYWB promotes fecundity of the AY-WB leafhopper vector on A. thaliana and modulates the expression of A. thaliana leaf defence response genes that are induced by this leafhopper, in contrast to SAP11MBSP. Neither of the SAP11 effectors promote fecundity of AY-WB and MBSP leafhopper vectors on maize. These data provide evidence that class II TCPs have overlapping but also distinct roles in regulating development and defence in a dicot and a monocot plant species that is likely to shape SAP11 effector evolution depending on the phytoplasma host range.

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

“…Phytoplasmas infect most vascular plant species and often induce massive changes in plant architecture, such as excessive proliferations of shoots and branches (witches’ brooms) and retrograde development of flowers into leaf-like organs (phyllody) (Hoshi et al, 2009; MacLean et al, 2011; Maejima et al, 2014; Sugio et al, 2011a). Plants exhibiting exhibit extensive architectural changes as the result of pathogen infections are described as ‘Zombies’, as the plants stop reproducing themselves and serve only as a habitat for the pathogens and their insect vectors (Al-Subhi et al, 2020; Cano et al, 2013; Du Toit, 2014; MacLean et al, 2014; Orlovskis and Hogenhout, 2016; Pecher et al, 2019; Rumpler et al, 2015; Sugio et al, 2011a). The three-way interactions among phytoplasmas, plants and insects, provide an excellent system to study the genetic basis of extended phenotypes created by obligate multi-host parasites (Huang et al, 2020; Sugio et al, 2011b).…”

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 ., ). 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 ., ; Pecher et al ., ). 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.…”

Bacterial Vector-Borne Plant Diseases: Unanswered Questions and Future Directions

“…Phytoplasma effectors have dramatic impacts on plant development and induce several distinct symptoms characteristic of diseases. For example, SAP11 effectors from diverse phytoplasmas induce a range of phenotypes when stably expressed in plants, including crinkled leaves and siliques, increased stem proliferation, altered root architecture, and abnormal glandular trichome development ( Sugio et al, 2011b ; Lu et al, 2014 ; Tan et al, 2016 ; Chang et al, 2018 ; Wang et al, 2018 ; Pecher et al, 2019 ). The role of these diverse plant phenotypes induced by phytoplasma effectors remains an important subject of future research.…”