Phytoplasma SAP11 effector destabilization of TCP transcription factors differentially impact development and defence of Arabidopsis versus maize
Authors: Pecher Pascal , Moro Gabriele , Canale Maria Cristina , Capdevielle Sylvain , Singh Archana , MacLean Allyson , Sugio Akiko , Kuo Chih-Horng , Lopes Joao R. S. , Hogenhout Saskia A. 
Published: March 2019

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 only TB1/CYC TCPs. SAP11MBSPand SAP11AYWBboth induce axillary branching and SAP11AYWBalso alters leaf development ofArabidopsis thalianaand maize. However, only in maize, SAP11MBSPprevents female inflorescence development, phenocopying maizetb1lines, whereas SAP11AYWBprevents male inflorescence development and induces feminization of tassels. SAP11AYWBpromotes fecundity of the AY-WB leafhopper vector onA. thalianaand modulates the expression ofA. thalianaleaf 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.

Author summary

Phytoplasmas are parasites of a wide range of plant species and are transmitted by sap-feeding insects, such as leafhoppers. Phytoplasma-infected plants are often easily recognized because of their dramatic symptoms, including shoot proliferations (witch’s brooms) and altered leaf shapes, leading to severe economic losses of crops, ornamentals and trees worldwide. We previously found that the virulence protein SAP11 of aster yellows witches’ broom phytoplasma (AY-WB) interferes with a specific group of plant transcription factors, named TCPs, leading to witches’ brooms and leaf shape changes of the model plantArabidopsis thaliana. SAP11 has been characterized in a number of other phytoplasmas. However, it is not known how phytoplasmas and their SAP11 proteins modulate processes in crops, including cereals such as maize. We identified a SAP11 homolog in Maize bushy stunt phytoplasma (MBSP), a pathogen that can cause severe yield losses of maize. We found that SAP11 interactions with TCPs are conserved between maize and Arabidopsis, and that MBSP SAP11 interferes with less TCPs compared to AY-WB SAP11. This work provides new insights into how phytoplasmas change maize architecture and corn production. Moreover, we found that TCPs regulate leaf defence responses to phytoplasma leafhopper vectors in Arabidopsis, but not in maize.