Long-term, sustained feeding by Asian citrus psyllid disrupts salicylic acid homeostasis in sweet orange

Freddy Ibanez,Joon Hyuk Suh,Lukasz L Stelinski,Yu Wang

doi:10.1186/s12870-019-2114-2

Freddy Ibanez, Joon Hyuk Suh + Show 2 more

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https://doi.org/10.1186/s12870-019-2114-2

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Abstract

BackgroundPhloem-feeding insects are known to modulate the salicylic acid (SA) signaling pathway in various plant-insect interaction models. Diaphorina citri is a phloem feeding vector of the deadly phytopathogens, Candidatus Liberibacter americanus and Candidatus Liberibacter asiaticus, and the interactions of D. citri with its host that may modulate plant defenses are not well understood. The objectives of this study were to investigate the molecular mechanisms involved in transcriptional regulation of SA modification and activation of defense-associated responses in sweet orange (Citrus sinensis) exposed to various durations (7-, 14- and 150- days) of continuous feeding by D. citri.ResultsWe quantified expression of genes involved in SA pathway activation and subsequent modification, as well as, associated SA metabolites (SA methyl ester, 2,3-DHBA, and SA 2-O-β-D-glucoside). NPR1 and PR-1 expression was upregulated in plants exposed to continuous feeding by D. citri for 14 days. Expression of BSMT-like, MES1-like and DMR6-like oxygenase, as well as, accumulation of their respective SA metabolites (SA methyl ester, 2,3-DHBA) was significantly higher in plants exposed to continuous feeding by D. citri for 150 days than in those without D. citri infestation. Concomitantly, expression of UGT74F2-like was significantly downregulated and its metabolite, SA 2-β-D-glucoside, was highly accumulated in trees exposed to 150 d of feeding compared to control trees without D. citri.ConclusionsD. citri herbivory differentially regulated transcription and SA-metabolite accumulation in citrus leaves, depending on duration of insect feeding. Our results suggest that prolonged and uninterrupted exposure (150 d) of citrus to D. citri feeding suppressed plant immunity and inhibited growth, which may highlight the importance of vector suppression as part of huanglongbing (HLB) management in citrus.

Highlights

Phloem-feeding insects are known to modulate the salicylic acid (SA) signaling pathway in various plant-insect interaction models
The overaccumulation of SA observed in leaves of citrus plants following prolonged exposure to D. citri feeding may Conclusions We described the molecular mechanisms involved in: i) transcriptional regulation of SA modification, and ii) activation of defense-associated responses in leaves of C. sinensis challenged by various durations of D. citri feeding injury
We propose two scenarios that describe transcriptional regulation of SA modification and activation of defense-associated responses via NONEXPRESSER OF PATHOGENESIS RELATED GENES 1 (NPR1) in C. sinensis depending on duration of plant exposure to insect injury (Fig. 6a, b)

Summary

Introduction

Phloem-feeding insects are known to modulate the salicylic acid (SA) signaling pathway in various plant-insect interaction models. Diaphorina citri is a phloem feeding vector of the deadly phytopathogens, Candidatus Liberibacter americanus and Candidatus Liberibacter asiaticus, and the interactions of D. citri with its host that may modulate plant defenses are not well understood. A number of salivary effector proteins have been identified in aphids, planthoppers, and spider mites. These effectors modulate several processes such as, fecundity, host colonization, and modulation of plant-defense signaling pathways, as reviewed in Kaloshian and Walling [12] and Xu, Qian [13]. It is known that D. citri feeding on citrus triggers the release of methyl salicylate (MeSA), [14], implicating the SA pathway in the Citrus sinensis - D. citri interaction

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