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

Abstract

28 Phytoplasmas are insect-transmitted bacterial pathogens that colonize a wide range of plant 29 species, including vegetable and cereal crops, and herbaceous and woody ornamentals.30 Phytoplasma-infected plants often show dramatic symptoms, including proliferation of shoots 31 (witch's brooms), changes in leaf shapes and production of green sterile flowers (phyllody). 32 Aster Yellows phytoplasma Witches' Broom (AY-WB) infects dicots and its effector, 33 secreted AYWB protein 11 (SAP11), was shown to be responsible for the induction of shoot 34 proliferation and leaf shape changes of plants. SAP11 acts by destabilizing TEOSINTE 35 BRANCHED 1-CYCLOIDEA-PROLIFERATING CELL FACTOR (TCP) transcription 36 factors, particularly the class II TCPs of the CYCLOIDEA/TEOSINTE BRANCHED 1 37 (CYC/TB1) and CINCINNATA (CIN)-TCP clades. SAP11 homologs are also present in 38 phytoplasmas that cause economic yield losses in monocot crops, such as maize, wheat and 39 coconut. Here we show that a SAP11 homolog of Maize Bushy Stunt Phytoplasma (MBSP), 40 which has a range primarily restricted to maize, destabilizes only TB1/CYC TCPs. 41 SAP11 MBSP and SAP11 AYWB both induce axillary branching and SAP11 AYWB also alters leaf 42 development of Arabidopsis thaliana and maize. However, only in maize, SAP11 MBSP 43 prevents female inflorescence development, phenocopying maize tb1 lines, whereas 44 SAP11 AYWB prevents male inflorescence development and induces feminization of tassels. 45 SAP11 AYWB promotes fecundity of the AY-WB leafhopper vector on A. thaliana and 46 modulates the expression of A. thaliana leaf defence response genes that are induced by this 47 leafhopper, in contrast to SAP11 MBSP . Neither of the SAP11 effectors promote fecundity of 48 AY-WB and MBSP leafhopper vectors on maize. These data provide evidence that class II 49 TCPs have overlapping but also distinct roles in regulating development and defence in a 50 dicot and a monocot plant species that is likely to shape SAP11 effector evolution depending 51 on the phytoplasma host range. 3 52 53 Author summary 57 Phytoplasmas are parasites of a wide range of plant species and are transmitted by sap-58 feeding insects, such as leafhoppers. Phytoplasma-infected plants are often easily recognized 59 because of their dramatic symptoms, including shoot proliferations (witch's brooms) and60 altered leaf shapes, leading to severe economic losses of crops, ornamentals and trees 61 worldwide. We previously found that the virulence protein SAP11 of aster yellows witches' 62 broom phytoplasma (AY-WB) interferes with a specific group of plant transcription factors, 63 named TCPs, leading to witches' brooms and leaf shape changes of the model plant 64 Arabidopsis thaliana. SAP11 has been characterized in a number of other phytoplasmas. 65 However, it is not known how phytoplasmas and their SAP11 proteins modulate processes in 66 crops, including cereals such as maize. We identified a SAP11 homolog in Maize bushy stunt 67 phytoplasma (MBSP), a pathogen that can cause severe yield l...

Functional variation in phyllogen, a phyllody‐inducing phytoplasma effector family, attributable to a single amino acid polymorphism

“…Although functional analyses of several effector homologs of phytoplasma have become areas of active research (Sugawara et al ., 2013; Maejima et al ., 2014; Chang et al ., 2018; Wang et al ., 2018b; Pecher et al ., 2019), the evolutionary dynamics of these homologs have not yet been addressed. In the current study, phylogenetic analyses indicated that the phyllogen family evolved independently of “ Ca .…”

“…Although functional analyses of several effector homologs of phytoplasma have become areas of active research (Sugawara et al, 2013;Maejima et al, 2014;Chang et al, 2018;Wang et al, 2018b;Pecher et al, 2019), the evolutionary dynamics of these homologs…”

Candidatus (Ca.) phytoplasma asteris subgroups display distinct disease progression dynamics during the carrot growing season

“…These normalized read values revealed significant differences in the presence of effectors genes between the two AYp subgroups observed in the investigation (Figure 5). From among the 20 effectors amplified, SAP11, 13,15,19,45, and 68 were found to be specific to the 16SrI-A subgroup and not detected in the 16SrI-B subgroup (above an established threshold). Effectors SAP05, 06, 27, 35, 41, 42, 44, 48, 49, and 66 were present in both subgroups.…”

“…Studies have identified 56 putative SAPs in the AY-WB genome and SAP11 was found to migrate out of the phloem into adjacent tissues, including trichomes, of A. thaliana [17]. Secreted AY-WB11 is a known, destabilizing class II TCP transcription factor of Arabidopsis thaliana leading to the induction of shoot branching resembling witch's broom symptoms and leaf crinkling [16,[18][19][20][21][22]. Moreover, SAP11 suppresses jasmonic acid (JA) synthesis and modulates volatile organic compounds (VOC) originating from glandular trichomes of plants [16,21].…”

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.…”