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.

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Author Pecher, Pascal
Last Updated November 20, 2019, 16:52 (UTC)
Created November 4, 2019, 17:57 (UTC)
Article Host Type publisher
Article Is Open Access true
Article License Type cc-by
Article Version Type publishedVersion
Citation Report https://scite.ai/reports/10.1371/journal.ppat.1008035
DOI 10.1371/journal.ppat.1008035
Date Last Updated 2019-10-23T03:24:39.106456
Evidence open (via page says license)
Funder code(s) Human Frontier Science Program (RGP0024/2105); Biotechnology and Biological Sciences Research Council (BB/J0045531/1, BB/K002848/1); Biotechnology and Biological Sciences Research Council (BB/J0045531/1, BB/K002848/1); Fundação de Amparo à Pesquisa do Estado de São Paulo (2012/50217-3, 2012/51867-1); Academia Sinica (); Fundação de Amparo à Pesquisa do Estado de São Paulo (2012/50217-3, 2012/51867-1); The P.O.R. Sardegna F.S.E. Operational Programme of the Autonomous Region of Sardinia (European Social Fund 2007.2013-Axis IV Human Resources, Objective I.3, Line of Activity I.3.1)
Journal Is Open Access true
Open Access Status gold
PDF URL https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1008035&type=printable
Publisher URL https://doi.org/10.1371/journal.ppat.1008035