Witches’ Broom Disease of Lime Contributes to Phytoplasma Epidemics and Attracts Insect Vectors

Abstract

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.

Parasitic modulation of host development by ubiquitin-independent protein degradation

“…Finally, a delay in plant senescence and death increases the likelihood of plants being visited and colonized by phytoplasma insect vectors, promoting the number of insects that can transmit the phytoplasmas. This effect may be intensified by insect vectors being more attracted to symptomatic phytoplasma-infected plants and the activities of SAP11 and SAP54 effectors that enhance insect attraction and colonization ( Al-Subhi et al., 2020 ; MacLean et al., 2014 ; Orlovskis & Hogenhout, 2016 ; ( Sugio et al., 2011a )).…”

Parasite co-opts a ubiquitin receptor to induce a plethora of developmental changes

“…One group of plant pathogens that are notorious for reprogramming their host development are members of Candidatus (Ca.) Phytoplasma (Al-Subhi et al, 2020; Doi et al, 1967; IRPCM, 2004; Lee et al, 2000; Sugio et al, 2011b), which comprises a diverse genus of bacteria that cause global socioeconomically important insect-transmitted diseases (EPPO, 2021). Phytoplasmas infect most vascular plant species and often induce massive changes in plant architecture, such as excessive proliferations of shoots and branches (witches’ brooms) and retrograde development of flowers into leaf-like organs (phyllody) (Hoshi et al, 2009; MacLean et al, 2011; Maejima et al, 2014; Sugio et al, 2011a).…”

“…Phytoplasmas infect most vascular plant species and often induce massive changes in plant architecture, such as excessive proliferations of shoots and branches (witches’ brooms) and retrograde development of flowers into leaf-like organs (phyllody) (Hoshi et al, 2009; MacLean et al, 2011; Maejima et al, 2014; Sugio et al, 2011a). Plants exhibiting exhibit extensive architectural changes as the result of pathogen infections are described as ‘Zombies’, as the plants stop reproducing themselves and serve only as a habitat for the pathogens and their insect vectors (Al-Subhi et al, 2020; Cano et al, 2013; Du Toit, 2014; MacLean et al, 2014; Orlovskis and Hogenhout, 2016; Pecher et al, 2019; Rumpler et al, 2015; Sugio et al, 2011a). The three-way interactions among phytoplasmas, plants and insects, provide an excellent system to study the genetic basis of extended phenotypes created by obligate multi-host parasites (Huang et al, 2020; Sugio et al, 2011b).…”

Interfering with plant developmental timing promotes susceptibility to insect vectors of a bacterial parasite

“…Visual cues, such as yellowing, have been shown to promote leafhopper attraction (Todd et al ., 1990; Al-Subhi et al ., 2021), it is possible that morphological attributes of the spl and gata mutants impacted leafhopper reproduction choice. The spl9 spl11 spl13 spl15 quadruple mutant, the gnc gnl double mutant and the gnc gnl gata17 gata17l quadruple mutant all have yellower foliage (Fig.…”