The phytoplasma bacterial plant parasite depends on leafhopper insects to spread and propagate itself. This study reveals how phytoplasma subverts plant development to turn flowers into leaves and thus make its host more attractive to leafhoppers.

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Background and Aims Maize bushy stunt phytoplasma (MBSP) is a bacterial pathogen of maize (Zea mays L.) across Latin America. MBSP belongs to the 16SrI-B sub-group within the genus ‘Candidatus Phytoplasma’. MBSP and its insect vector Dalbulus maidis (Hemiptera: Cicadellidae) are restricted to maize; both are thought to have coevolved with maize during its domestication from a teosinte-like ancestor. MBSP-infected maize plants show a diversity of symptoms. and it is likely that MBSP is under strong selection for increased virulence and insect transmission on maize hybrids that are widely grown in Brazil. In this study it was investigated whether the differences in genome sequences of MBSP isolates from two maize-growing regions in South-east Brazil explain variations in symptom severity of the MBSP isolates on various maize genotypes. Methods MBSP isolates were collected from maize production fields in Guaíra and Piracicaba in South-east Brazil for infection assays. One representative isolate was chosen for de novo whole-genome assembly and for the alignment of sequence reads from the genomes of other phytoplasma isolates to detect polymorphisms. Statistical methods were applied to investigate the correlation between variations in disease symptoms of infected maize plants and MBSP sequence polymorphisms. Key Results MBSP isolates contributed consistently to organ proliferation symptoms and maize genotype to leaf necrosis, reddening and yellowing of infected maize plants. The symptom differences are associated with polymorphisms in a phase-variable lipoprotein, which is a candidate effector, and an ATP-dependent lipoprotein ABC export protein, whereas no polymorphisms were observed in other candidate effector genes. Lipoproteins and ABC export proteins activate host defence responses, regulate pathogen attachment to host cells and activate effector secretion systems in other pathogens. Conclusions Polymorphisms in two putative virulence genes among MBSP isolates from maize-growing regions in South-east Brazil are associated with variations in organ proliferation symptoms of MBSP-infected maize plants.

Parasites can take over their hosts and trigger dramatic changes in host appearance and behavior that are typically interpreted as extended phenotypes that promote parasite survival and fitness. For example, Toxoplasma gondii is thought to manipulate the behaviors of infected rodents to aid transmission to cats and parasitic trematodes of the genus Ribeiroia alter limb development in their amphibian hosts to facilitate predation of the latter by birds. Plant parasites and pathogens also reprogram host development and morphology. However, whereas some parasite-induced morphological alterations may have a direct benefit to the fitness of the parasite and may therefore be adaptive, other host alterations may be side effects of parasite infections having no adaptive effects on parasite fitness. Phytoplasma parasites of plants often induce the development of leaf-like flowers (phyllody) in their host plants, and we previously found that the phytoplasma effector SAP54 generates these leaf-like flowers via the degradation of plant MADS-box transcription factors (MTFs), which regulate all major aspects of development in plants. Leafhoppers prefer to reproduce on phytoplasma-infected and SAP54-trangenic plants leading to the hypothesis that leafhopper vectors are attracted to plants with leaf-like flowers. Surprisingly, here we show that leafhopper attraction occurs independently of the presence of leaf-like flowers. First, the leafhoppers were also attracted to SAP54 transgenic plants without leaf-like flowers and to single leaves of these plants. Moreover, leafhoppers were not attracted to leaf-like flowers of MTF-mutant plants without the presence of SAP54. Thus, the primary role of SAP54 is to attract leafhopper vectors, which spread the phytoplasmas, and the generation of leaf-like flowers may be secondary or a side effect of the SAP54-mediated degradation of MTFs.

Summary Recognition of plant pathogens or herbivores activate a broad‐spectrum plant defense priming in distal leaves against potential future attacks, leading to systemic acquired resistance (SAR). Additionally, attacked plants can release aerial or below‐ground signals that trigger defense responses, such as SAR, in neighboring plants lacking initial exposure to pathogen or pest elicitors. However, the molecular mechanisms involved in interplant defense signal generation in sender plants and decoding in neighboring plants are not fully understood. We previously reported that Pieris brassicae eggs induce intraplant SAR against the foliar pathogen Pseudomonas syringae in Arabidopsis thaliana. Here we extend this effect to neighboring plants by discovering an egg‐induced interplant SAR via mobile root‐derived signal(s). The generation of an egg‐induced interplant SAR signal requires pipecolic acid (Pip) pathway genes ALD1 and FMO1 but occurs independently of salicylic acid (SA) accumulation in sender plants. Furthermore, reception of the signal leads to accumulation of SA in the recipient plants. In response to insect eggs, plants may induce interplant SAR to prepare for potential pathogen invasion following feeding‐induced wounding or to keep neighboring plants healthy for hatching larvae. Our results highlight a previously uncharacterized below‐ground plant‐to‐plant signaling mechanism and reveals genetic components required for its generation.

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Parasites can take over their hosts and trigger dramatic changes in host appearance and behaviour that are typically interpreted as extended phenotypes to promote parasite survival and fitness. For example, Toxoplasma gondii manipulates the behaviour of infected rodents to aid transmission to cats and parasitic trematodes of the genus Ribeiroia alter limb development in their amphibian hosts to facilitate predation by birds. Plant parasites and pathogens also reprogram host development and morphology. Phytoplasma parasites of plants induce extensive leaf-like flower phenotype (phyllody) in their host plants, presumably to attract insect vectors on which these bacteria depend for transmission. However, it remains debatable whether morphological phenotypes, such as phyllody, are directly beneficial to the parasites or are side-products of parasite infection. Previously, we found that phytoplasma virulence protein (effector) SAP54 binds and mediates degradation of host MADS-box transcription factors (MTFs), regulatory hubs of plant development and hormone physiology, to induce phyllody and promote insect vector colonisation. Here we show that plants heterologously expressing SAP54 are strongly attractive to insects, but surprisingly, insect attraction was independent of the presence of leaf-like flowers. Moreover, plants that produce leaf-like flowers in the absence of SAP54 did not attract insects. We conclude that the SAP54 effector mediates insect vector attraction in host plants by exploiting the role of its MTF targets in insect defence and that perturbation of floral development may be a secondary effect of the effector activity.

An insect-transmitted phytoplasma causing Witches’ Broom Disease of Lime (WBDL) is responsible for the drastic decline in lime production in several countries. However, it is unclear how WBDL phytoplasma (WBDLp) induces witches’ broom symptoms and if these symptoms contribute to the spread of phytoplasma. Here we show that the gene encoding SAP11 of WBDLp (SAP11WBDL) is present in all WBDLp isolates collected from diseased trees. SAP11WBDL interacts with acid lime (Citrus aurantifolia) TCP transcription factors, specifically members of the TB1/CYC class that have a role in suppressing axillary branching in plants. Sampling of WBDLp-infected lime trees revealed that WBDLp titers and SAP11WBDL expression levels were higher in symptomatic leaves compared to asymptomatic sections of the same trees. Moreover, the witches’ brooms were found to attract the vector leafhopper. Defense genes that have a role in plant defense responses to bacteria and insects are more downregulated in witches’ brooms compared to asymptomatic sections of trees. These findings suggest that witches’ broom-affected parts of the trees contribute to WBDL epidemics by supporting higher phytoplasma titers and attracting insect vectors.