Maize Bushy Stunt Phytoplasma Favors Its Spread by Changing Host Preference of the Insect Vector

Plant pathogenic bacteria may influence vector behavior by inducing physiological changes in host plants, with implications for their spread. Here, we studied the effects of maize bushy stunt phytoplasma (MBSP) on the host selection behavior of the leafhopper vector, Dalbulus maidis (DeLong and Wolcott). Choice assays contrasting leaves of healthy (mock-inoculated) vs. infected maize (Zea mays L.) were conducted during the asymptomatic and symptomatic phases of plant infection, with leafhopper males or females previously exposed to infected plants (bacteriliferous insects) or not. In each assay, 40 adults were released in choice arenas where only the leaves of two plants from each treatment were offered and visible, and the insects landed on the leaves were counted 1, 2, 3, 5, 7, 9, 11 and 23 h after release. During the asymptomatic phase of plant infection, an effect was observed only on bacteriliferous females, who preferred leaves of healthy plants 5 h after release or later. The symptomatic phase triggered a pull–push effect on non-bacteriliferous females, who were first attracted to symptomatic leaves but hours later moved to healthy leaves. Non-bacteriliferous males initially preferred symptomatic leaves (up to 5 h after release) and later became equally distributed between treatments. Bacteriliferous males and females initially did not discriminate between healthy and symptomatic leaves, but only the females tended to move to healthy leaves 9 h after release. Oviposition was drastically reduced on symptomatic leaves. The changes in vector behavior induced by MBSP favor its primary spread, since bacteriliferous females prefer healthy leaves at early (asymptomatic) stages of the crop. At later stages, secondary spread may be favored because non-bacteriliferous females are initially attracted to infected (symptomatic) leaves, allowing pathogen acquisition and subsequent transmission as they move to healthy plants.

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 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 summaryPhytoplasmas 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.