Leaf-mining by Phyllonorycter blancardella reprograms the host-leaf transcriptome to modulate phytohormones associated with nutrient mobilization and plant defense

Zhang, Hui; Bernonville, Thomas Dugé de; Body, Mélanie; Glévarec, Gaëlle; Reichelt, Michael; Unsicker, Sybille B.; Bruneau, Maryline; Renou, Jean-Pierre; Huguet, Elisabeth; Dubreuil, Géraldine

doi:10.1016/j.jinsphys.2015.06.003

Cited by 45 publications

(44 citation statements)

References 89 publications

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“…proteinaceous effectors, phytohormones or phytohormone analogs secreted with the saliva) with those offered by microbes, as has been observed in other plant-herbivore and plant-plant parasitic nematode interactions (e.g. Favery et al, this issue; Guiguet et al, this issue; Harris et al, 2015; Kazan and Lyons, 2014; Zhang et al, this issue; Zhao et al, this issue). Future field-based experiments such as those described by Humphrey et al (2014) and O’Connor et al (2014) will allow us to gauge the extent and relevance of these associations.…”

Section: Discussionmentioning

confidence: 87%

Pseudomonas syringae enhances herbivory by suppressing the reactive oxygen burst in Arabidopsis

Groen

Humphrey

Chevasco

et al. 2016

Journal of Insect Physiology

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Plant-herbivore interactions have evolved in the presence of plant-colonizing microbes. These microbes can have important third-party effects on herbivore ecology, as exemplified by drosophilid flies that evolved from ancestors feeding on plant-associated microbes. Leaf-mining flies in the genus Scaptomyza, which is nested within the paraphyletic genus Drosophila, show strong associations with bacteria in the genus Pseudomonas, including Pseudomonas syringae. Adult females are capable of vectoring these bacteria between plants and larvae show a preference for feeding on P. syringae-infected leaves. Here we show that Scaptomyza flava larvae can also vector P. syringae to and from feeding sites, and that they not only feed more, but also develop faster on plants previously infected with P. syringae. Our genetic and physiological data show that P. syringae enhances S. flava feeding on infected plants at least in part by suppressing anti-herbivore defenses mediated by reactive oxygen species.

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Section: Discussionmentioning

confidence: 87%

Pseudomonas syringae enhances herbivory by suppressing the reactive oxygen burst in Arabidopsis

Groen

Humphrey

Chevasco

et al. 2016

Journal of Insect Physiology

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“…Unmined green and yellow leaves were used as a control. Field observations and phytohormone quantification show reduced levels of abscisic acid favoring the suppression of abscission during the critical larval feeding stage (Zhang et al, 2016). The nutritional content of yellow leaves is significantly decreased and cannot meet the insect nutritional requirements but the closely related leaf-mining moth P. blancardella was shown to maintain a nutritional homeostasis in mined tissues (Body et al, 2013).…”

Section: Biological Materialsmentioning

confidence: 99%

“…These leaf areas are enriched in CKs, and CKs accumulated in the mined area do not originate from the plant CK-biosynthetic pathway (Zhang et al, 2016). These leaf areas are enriched in CKs, and CKs accumulated in the mined area do not originate from the plant CK-biosynthetic pathway (Zhang et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

“…Increased CK levels can favor cell division but also nutrient translocation toward the insect's feeding site and delay leaf senescence thus contributing to gall induction and a 'green island' phenotype (Mok & Mok, 2001;Balibrea-Lara et al, 2004;Walters & Mcroberts, 2006;Walters et al, 2008;Giron et al, 2013;Schaller et al, 2015). In leaf-miner insects, studies on the nepticulid moths Ectodemia argyropeza (Zeller), Stigmella argyropeza (Zeller), Stigmella argentipedella (Zeller), Stigmella spp., and the gracillariid moth Phyllonorycter blancardella (Fabricius) show large accumulation of CKs in 'green islands' (Engelbrecht et al, 1969;Engelbrecht, 1971;Giron et al, 2007;Body et al, 2013;Zhang et al, 2016). In leaf-miner insects, studies on the nepticulid moths Ectodemia argyropeza (Zeller), Stigmella argyropeza (Zeller), Stigmella argentipedella (Zeller), Stigmella spp., and the gracillariid moth Phyllonorycter blancardella (Fabricius) show large accumulation of CKs in 'green islands' (Engelbrecht et al, 1969;Engelbrecht, 1971;Giron et al, 2007;Body et al, 2013;Zhang et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

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Modulation of plant cytokinin levels in the Wolbachia‐free leaf‐mining species Phyllonorycter mespilella

Zhang

Dubreuil

Faivre

et al. 2018

Entomologia Exp Applicata

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As phytohormones lie at the very core of molecular mechanisms controlling the plant physiology and development, they have long been hypothesized to be involved in insect-induced plant manipulations. Cytokinins (CKs) are phytohormones now widely recognized to be utilized by leaf-mining and gall-inducing insects in the control of the physiology of their host plant. In some leaf-mining moth species, larvae can supply the hormones themselves, bacterial symbionts contributing to the production of CKs. Our objective was to investigate whether closely related leaf-miner species sharing the same ecological niche but differing in their Wolbachia infection status develop similar strategies to manipulate their host plant. An extensive identification and quantification of CKs has been used to elucidate physiological patterns relevant for the plant-insect interactions. Our results show that modulation of plant CK levels is impaired in the Wolbachia-free leaf-mining moth Phyllonorycter mespilella (H€ ubner) (Lepidoptera: Gracillariidae) contrasting with results previously observed in the closely related moth species Phyllonorycter blancardella (Fabricius) that produce and deliver CKs to the plant through an intricate interaction with Wolbachia. Our study suggests that mechanisms underlying colonization of the host plant and adaptation to fluctuating environmental conditions are different between the two leaf-miner species and that P. mespilella larvae most likely do not produce CKs. This species rather only buffers the degradation of CKs naturally occurring during the senescence of leaves leading to few active CKs being maintained at a sufficiently high level to induce and maintain a 'green island' phenotype (photosynthetically active green patches in otherwise senescing leaves). This study further provides converging experimental evidence pointing toward the influence of bacterial symbionts in the ability of leaf-mining moths to control the physiology of their host plant with consequences for their ecology and evolutionary diversification.

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“…One example of this integrated approach was demonstrated by Zhang et al [58]. The authors examined phytohormone dynamics during the interaction between apple ( Malus domestica ) and a leaf-mining lepidopteran, Phyllonorycter blancardella (Lepidoptera: Gracillariidae) using liquid chromatography coupled to tandem mass spectrometry (LC-MS-MS) and microarray expression profiling.…”

Section: The Molecular Mechanisms Of Gall Inductionmentioning

confidence: 99%

Insect Gallers and Their Plant Hosts: From Omics Data to Systems Biology

Oates

Denby

Myburg

et al. 2016

IJMS

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Gall-inducing insects are capable of exerting a high level of control over their hosts’ cellular machinery to the extent that the plant’s development, metabolism, chemistry, and physiology are all altered in favour of the insect. Many gallers are devastating pests in global agriculture and the limited understanding of their relationship with their hosts prevents the development of robust management strategies. Omics technologies are proving to be important tools in elucidating the mechanisms involved in the interaction as they facilitate analysis of plant hosts and insect effectors for which little or no prior knowledge exists. In this review, we examine the mechanisms behind insect gall development using evidence from omics-level approaches. The secretion of effector proteins and induced phytohormonal imbalances are highlighted as likely mechanisms involved in gall development. However, understanding how these components function within the system is far from complete and a number of questions need to be answered before this information can be used in the development of strategies to engineer or breed plants with enhanced resistance.

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Leaf-mining by Phyllonorycter blancardella reprograms the host-leaf transcriptome to modulate phytohormones associated with nutrient mobilization and plant defense

Cited by 45 publications

References 89 publications

Pseudomonas syringae enhances herbivory by suppressing the reactive oxygen burst in Arabidopsis

Pseudomonas syringae enhances herbivory by suppressing the reactive oxygen burst in Arabidopsis

Modulation of plant cytokinin levels in the Wolbachia‐free leaf‐mining species Phyllonorycter mespilella

Insect Gallers and Their Plant Hosts: From Omics Data to Systems Biology

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