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

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.植原体（Phytoplasma）是一类昆虫传播的细菌性病原菌，可定殖于多种植物宿主，包括蔬菜、谷类作物，以及草本和木本观赏植物。感染植原体的植株常表现出显著病症，包括枝条过度增生（丛枝病，witch’s broom）、叶片形态改变，以及产生绿色不育花的叶化现象（phyllody）。Aster黄化植原体丛枝株系（Aster Yellows phytoplasma Witches’ Broom, AY-WB）可侵染双子叶植物，其分泌效应蛋白AYWB分泌蛋白11（secreted AYWB protein 11, SAP11）被证实可诱导植株枝条增生与叶片形态改变。SAP11通过降解TEOSINTE BRANCHED 1-CYCLOIDEA-PROLIFERATING CELL FACTOR（TCP）转录因子发挥作用，尤其靶向CYCLOIDEA/TEOSINTE BRANCHED 1（CYC/TB1）与CINCINNATA（CIN）-TCP进化支的II类TCP转录因子。在导致玉米、小麦和椰子等单子叶作物经济产量损失的植原体中，同样存在SAP11同源蛋白。本研究发现，主要定殖于玉米的玉米丛矮植原体（Maize Bushy Stunt Phytoplasma, MBSP）的SAP11同源蛋白，可特异性降解TB1/CYC类TCP转录因子。SAP11MBSP与SAP11AYWB均可诱导拟南芥（Arabidopsis thaliana）和玉米的腋芽分枝，且SAP11AYWB还可改变叶片发育进程。但仅在玉米中，SAP11MBSP可抑制雌花序发育，表型模拟玉米tb1突变体株系；而SAP11AYWB则抑制雄花序发育并诱导雄穗雌化。SAP11AYWB可提升叶蝉介体在拟南芥上的繁殖力，并调控拟南芥中被该叶蝉诱导的叶片防御响应基因的表达，而SAP11MBSP无此功能。两类SAP11效应蛋白均无法提升AY-WB和MBSP叶蝉介体在玉米上的繁殖力。本研究数据表明，II类TCP转录因子在双子叶与单子叶植物的发育与防御调控中存在功能重叠，但也存在特异性差异，这种差异可能会根据植原体的宿主范围塑造SAP11效应蛋白的进化轨迹。