A Bacterial Parasite Effector Mediates Insect Vector Attraction in Host Plants Independently of Developmental Changes

Abstract

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.

Phytoplasma Infection of Cranberries Benefits Non-vector Phytophagous Insects

“…Phytoplasma infection can also alter diverse aspects of host plant chemistry (Oliveira et al, 2005;Musetti, 2009;Sugio et al, 2011a). For example, infection by phytoplasmas can alter carbohydrate and amino acid levels (Lepka et al, 1999;Tan and Whitlow, 2001), induce changes in volatile emissions (Mayer et al, 2008a,b;Orlovskis and Hogenhout, 2016), and affect defense signaling (Sugio et al, 2011b) in plants. Phytoplasma infection has also been shown to increase levels of plant secondary metabolites, including phenolic compounds and hydrogen peroxide (Junqueira et al, 2004;Musetti et al, 2004;Musetti, 2009).…”

Phytoplasma Infection Influences Gene Expression in American Cranberry

“…The suppression of SA-and/or JA-mediated responses in the phytoplasmainfected plants may facilitate feeding by herbivorous insects. In addition, phytoplasma-encoded effector proteins can increase volatiles that attract the insect vectors (Orlovskis and Hogenhout, 2016). Thus, modification of host plant phytochemical processes (such as nutrient translocation, chemical defense production, and volatile production) not only affects the host plant growth and development, but also influences the host plant-insect vector interaction.…”

A few sequence polymorphisms among isolates of Maize bushy stunt phytoplasma associate with organ proliferation symptoms of infected maize plants

“…Functional characterizations are available for effectors tengu-su, SAP11 and SAP54/phyllogen from AY-WB (16SrIA sub-group) and Onion Yellows phytoplasma strain M (OY-M; 16SrIB sub-group) (Sugio et al , 2011 a , b ; Sugawara et al , 2013; Lu et al , 2014; MacLean et al , 2014; Maejima et al , 2014; Minato et al , 2014; Orlovskis et al , 2015; Orlovskis and Hogenhout, 2016). The SAP11 and SAP54 effectors induce stem proliferation and leaf-like flowers that resemble witch’s broom and phyllody symptoms, respectively, of phytoplasma-infected plants (Bai et al , 2009; Hoshi et al , 2009; MacLean et al , 2011; Sugio et al , 2011 a ).…”

“…The SAP11 and SAP54 effectors induce stem proliferation and leaf-like flowers that resemble witch’s broom and phyllody symptoms, respectively, of phytoplasma-infected plants (Bai et al , 2009; Hoshi et al , 2009; MacLean et al , 2011; Sugio et al , 2011 a ). Phytoplasma effectors SAP11 and SAP54/phyllogen act by interacting with specific plant transcription factors and degrade/destabilize them, leading to the changes in leaf, stem and flower development, and the downregulation of defence responses that promote attraction of phytoplasma insect vectors (Sugio et al , 2011 a , b ; Lu et al , 2014; MacLean et al , 2014; Maejima et al , 2014; Orlovskis et al , 2015; Orlovskis and Hogenhout, 2016). …”