Influence of Aster Yellows Phytoplasma on the Fitness of Aster Leafhopper (Homoptera: Cicadellidae)

Beanland, LeAnn; Hoy, Casey W.; Miller, Sally A.; Nault, L. R.

doi:10.1603/0013-8746(2000)093[0271:ioaypo]2.0.co;2

Cited by 89 publications

(63 citation statements)

References 17 publications

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“…1A), flowers that become leafy, and various other morphological changes indicating that AY-WB interferes with plant developmental pathways (27). Previously, it was shown that leafhopper fecundity was increased on AY bolt-infected plants but not AY severe-infected plants (4). We determined if AY-WB induces similar phenotypes in Arabidopsis.…”

Section: Phytoplasma Infection Of Arabidopsis Changes Plant Morphologmentioning

confidence: 89%

“…Beanland et al (4) found that isolate bolt increased leafhopper reproduction, whereas isolate severe did not. Hence, bolt would be expected to have a competitive advantage over severe.…”

Section: Sap11 Binds To and Destabilizes Arabidopsis Tcp Transcriptionmentioning

confidence: 99%

“…Indeed, there are spectacular examples of alterations of host phenotypic traits in response to vector-borne pathogen infection. These include malaria parasites, which make humans more attractive to mosquito vectors, particularly at the plasmodium transmissible stage (1); several vector-borne animal pathogens, which alter blood viscosity to facilitate blood ingestion by vectors (2); the fungus Puccinia monoica, which induces the formation of pseudoflowers to attract insects that enable the reproduction of the fungus (3); and phytoplasmas and viruses that improve plant host quality for their insect vectors (4,5) and alter volatile emission of host plants to attract insect vectors (6,7). It is well documented that pathogens produce effectors that modify specific processes in the host and alter the host-pathogen interface, often to the advantage of the pathogen (8,9).…”

mentioning

confidence: 99%

“…These morphological changes in the plant may attract insect vectors that preferentially lay eggs in leaves and stems, and some in roots (14). Furthermore, M. quadrilineatus leafhoppers survive longer and produce more progeny on AY phytoplasma-infected plants (4), suggesting that the phytoplasmas down-regulate plant defense against the leafhopper. However, the two phytoplasma isolates ("bolt" and "severe") involved in the study were field isolates that were not formally classified, and the mechanisms by which these bacteria impair host defenses are not yet understood.…”

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confidence: 99%

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Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis

Sugio

Kingdom

MacLean

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

397

425

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Phytoplasmas are insect-transmitted phytopathogenic bacteria that can alter plant morphology and the longevity and reproduction rates and behavior of their insect vectors. There are various examples of animal and plant parasites that alter the host phenotype to attract insect vectors, but it is unclear how these parasites accomplish this. We hypothesized that phytoplasmas produce effectors that modulate specific targets in their hosts leading to the changes in plant development and insect performance. Previously, we sequenced and mined the genome of Aster Yellows phytoplasma strain Witches' Broom (AY-WB) and identified 56 candidate effectors. Here, we report that the secreted AY-WB protein 11 (SAP11) effector modulates plant defense responses to the advantage of the AY-WB insect vector Macrosteles quadrilineatus. SAP11 binds and destabilizes Arabidopsis CINCINNATA (CIN)-related TEOSINTE BRANCHED1, CYCLOIDEA, PROLIFERATING CELL FAC-TORS 1 and 2 (TCP) transcription factors, which control plant development and promote the expression of lipoxygenase (LOX) genes involved in jasmonate (JA) synthesis. Both the Arabidopsis SAP11 lines and AY-WB-infected plants produce less JA on wounding. Furthermore, the AY-WB insect vector produces more offspring on AY-WB-infected plants, SAP11 transgenic lines, and plants impaired in CIN-TCP and JA synthesis. Thus, SAP11-mediated destabilization of CIN-TCPs leads to the down-regulation of LOX2 expression and JA synthesis and an increase in M. quadrilineatus progeny. Phytoplasmas are obligate inhabitants of their plant host and insect vectors, in which the latter transmits AY-WB to a diverse range of plant species. This finding demonstrates that pathogen effectors can reach beyond the pathogen-host interface to modulate a third organism in the biological interaction.Arabidopsis development | insect herbivore | jasmonic acid | symbiosis | Hemiptera

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Section: Phytoplasma Infection Of Arabidopsis Changes Plant Morphologmentioning

confidence: 89%

“…Beanland et al (4) found that isolate bolt increased leafhopper reproduction, whereas isolate severe did not. Hence, bolt would be expected to have a competitive advantage over severe.…”

Section: Sap11 Binds To and Destabilizes Arabidopsis Tcp Transcriptionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis

Sugio

Kingdom

MacLean

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

397

425

View full text Add to dashboard Cite

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“…First, the pathogen causes nutritional changes in infected plants, resulting in improved fitness of the vectors. Second, the pathogen increases plant attractiveness and suitability to the vectors by overcoming plant defenses against the vector species, thereby promoting vector performance and increasing pathogen spread (Beanland et al, 2000;Eigenbrode et al, 2002;Lacroix et al, 2005;Jiu et al, 2007;Wang et al, 2012;Luan et al, 2014). To date, only a few reports have examined the host plant genes that are involved in pathogen-vector-plant interactions.…”

Section: Introductionmentioning

confidence: 99%

Virulence Factors of Geminivirus Interact with MYC2 to Subvert Plant Resistance and Promote Vector Performance

et al. 2014

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A pathogen may cause infected plants to promote the performance of its transmitting vector, which accelerates the spread of the pathogen. This positive effect of a pathogen on its vector via their shared host plant is termed indirect mutualism. For example, terpene biosynthesis is suppressed in begomovirus-infected plants, leading to reduced plant resistance and enhanced performance of the whiteflies (Bemisia tabaci) that transmit these viruses. Although begomovirus-whitefly mutualism has been known, the underlying mechanism is still elusive. Here, we identified bC1 of Tomato yellow leaf curl China virus, a monopartite begomovirus, as the viral genetic factor that suppresses plant terpene biosynthesis. bC1 directly interacts with the basic helix-loop-helix transcription factor MYC2 to compromise the activation of MYC2-regulated terpene synthase genes, thereby reducing whitefly resistance. MYC2 associates with the bipartite begomoviral protein BV1, suggesting that MYC2 is an evolutionarily conserved target of begomoviruses for the suppression of terpene-based resistance and the promotion of vector performance. Our findings describe how this viral pathogen regulates host plant metabolism to establish mutualism with its insect vector.

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Survival relative to new and ancestral host plants, phytoplasma infection, and genetic constitution in host races of a polyphagous insect disease vector

Maixner

Albert²,

Johannesen³

2014

Ecology and Evolution

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Dissemination of vectorborne diseases depends strongly on the vector's host range and the pathogen's reservoir range. Because vectors interact with pathogens, the direction and strength of a vector's host shift is vital for understanding epidemiology and is embedded in the framework of ecological specialization. This study investigates survival in host-race evolution of a polyphagous insect disease vector, Hyalesthes obsoletus, whether survival is related to the direction of the host shift (from field bindweed to stinging nettle), the interaction with plant-specific strains of obligate vectored pathogens/symbionts (stolbur phytoplasma), and whether survival is related to genetic differentiation between the host races. We used a twice repeated, identical nested experimental design to study survival of the vector on alternative hosts and relative to infection status. Survival was tested with Kaplan–Meier analyses, while genetic differentiation between vector populations was quantified with microsatellite allele frequencies. We found significant direct effects of host plant (reduced survival on wrong hosts) and sex (males survive longer than females) in both host races and relative effects of host (nettle animals more affected than bindweed animals) and sex (males more affected than females). Survival of bindweed animals was significantly higher on symptomatic than nonsymptomatic field bindweed, but in the second experiment only. Infection potentially had a positive effect on survival in nettle animals but due to low infection rates the results remain suggestive. Genetic differentiation was not related to survival. Greater negative plant-transfer effect but no negative effect of stolbur in the derived host race suggests preadaptation to the new pathogen/symbiont strain before strong diversifying selection during the specialization process. Physiological maladaptation or failure to accept the ancestral plant will have similar consequences, namely positive assortative mating within host races and a reduction in the likelihood of oviposition on the alternative plant and thus the acquisition of alternative stolbur strains.

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Influence of Aster Yellows Phytoplasma on the Fitness of Aster Leafhopper (Homoptera: Cicadellidae)

Cited by 89 publications

References 17 publications

Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis

Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis

Virulence Factors of Geminivirus Interact with MYC2 to Subvert Plant Resistance and Promote Vector Performance

Survival relative to new and ancestral host plants, phytoplasma infection, and genetic constitution in host races of a polyphagous insect disease vector

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