Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts

Kaiser, Wilfried; Huguet, Elisabeth; Casas, Jérôme; Commin, Céline; Giron, David

doi:10.1098/rspb.2010.0214

Cited by 186 publications

(240 citation statements)

References 37 publications

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“…In an interesting manner, some leaf‐mining larvae remain alive in the green islands on the dry or fallen leaves of some deciduous trees in Saihanwula. This provides the larvae with enough food to complete their life cycle before winter (Giron, Kaiser, Imbault, & Casas, 2007; Kaiser, Huguet, Casas, Commin, & Giron, 2010; Liu et al., 2015). …”

Section: Methodsmentioning

confidence: 99%

Are dominant plant species more susceptible to leaf‐mining insects? A case study at Saihanwula Nature Reserve, China

Dai

Long

et al. 2018

Ecology and Evolution

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Dominant species significantly affect interspecific relationships, community structure, and ecosystem function. In the field, dominant species are often identified by their high importance values. Selective foraging on dominant species is a common phenomenon in ecology. Our hypothesis is that dominant plant groups with high importance values are more susceptible to leaf‐mining insects at the regional level. Here, we used the Saihanwula National Nature Reserve as a case study to examine the presence–absence patterns of leaf‐mining insects on different plants in a forest‐grassland ecotone in Northeast China. We identified the following patterns: (1) After phylogenetic correction, plants with high importance values are more likely to host leafminers at the species, genus, or family level. (2) Other factors including phylogenetic isolation, life form, water ecotype, and phytogeographical type of plants have different influences on the relationship between plant dominance and leafminer presence. In summary, the importance value is a valid predictor of the presence of consumers, even when we consider the effects of plant phylogeny and other plant attributes. Dominant plant groups are large and susceptible targets of leaf‐mining insects. The consistent leaf‐mining distribution pattern across different countries, vegetation types, and plant taxa can be explained by the “species‐area relationship” or the “plant apparency hypothesis.”

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Section: Methodsmentioning

confidence: 99%

Are dominant plant species more susceptible to leaf‐mining insects? A case study at Saihanwula Nature Reserve, China

Dai

Long

et al. 2018

Ecology and Evolution

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“…It can be assumed that these species adopted CK biosynthetic machinery and produce their own CKs to influence the growth and development of their host plants. However, a recent study showed that the phytophagous leaf-mining moth Phyllonorycter blancardella (Lepidoptera) relies on CKproducing bacterial endosymbionts, most probably Wolbachia, to manipulate the physiology of its host plant, resulting in photosynthetically active green patches in otherwise senescent leaves and to increase its fitness (Kaiser et al 2010). It is also worth mentioning the work by Tsoupras et al (1983), who published an identification of the predominating maternal conjugate of ecdysone with CK, N 6 -isopentenyladenosine-5 0 -monophosphate (iPRMP) in newly laid eggs of Locusta migratoria.…”

Section: Evolution and Use Of Cks By Plant-interacting Organisms As Tmentioning

confidence: 99%

Cytokinins - recent news and views of evolutionally old molecules

Spíchal¹

2012

Functional Plant Biol.

154

169

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Cytokinins (CKs) are evolutionally old and highly conserved low-mass molecules that have been identified in almost all known organisms. In plants, they evolved into an important group of plant hormones controlling many physiological and developmental processes throughout the whole lifespan of the plant. CKs and their functions are, however, not unique to plants. In this review, the strategies and mechanisms of plants – and phylogenetically distinct plant-interacting organisms such as bacteria, fungi, nematodes and insects employing CKs or regulation of CK status in plants – are described and put into their evolutionary context. The major breakthroughs made in the last decade in the fields of CK biosynthesis, degradation and signalling are also summarised.

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“…A clear example of a CK-induced phenotype is the formation, after pathogen or insect attack, of spectacular green and metabolically active areas in otherwise yellow senescent leaves known as 'green-islands' (Engelbrecht et al 1969;Giron et al 2007;Kaiser et al 2010;Walters and McRoberts 2006;Walters et al 2008). In these islands, nutrientsmainly sugars -are redirected towards the infection site where host cell death is delayed.…”

Section: Introductionmentioning

confidence: 99%

“…Indeed, pathogens and herbivorous insects potentially influence the levels of phytohormones by inducing plant genes involved in CK biosynthesis, degradation, or response, but they also can produce and secrete relevant phytohormones themselves (Farnsworth 2004;Giron et al 2013;Jameson 2000;Robert-Seilaniantz et al 2007;Walters et al 2008). In the case of arthropods, CK-induced phenotypes can be mediated by their bacterial symbionts, giving rise to intricate plantmicrobe-insect interactions (Kaiser et al 2010).…”

Section: Introductionmentioning

confidence: 99%

Leaf-Miners Co-opt Microorganisms to Enhance their Nutritional Environment

et al. 2013

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Organisms make the best of their mother's oviposition choices and utilize specific feeding options that meet energetic requirements and cope with environmental constraints. This is particularly true for leaf-miner insects that develop enclosed in the two epidermis layers of a single leaf for their entire larval life. Cytokinins (CKs) play a central role in plant physiology -including regulation of senescence and nutrient translocation -and, as such, can be the specific target of plant exploiters that manipulate plant primary metabolism. 'Green-islands' are striking examples of a CKinduced phenotype where green areas are induced by plant pathogens/insects in otherwise yellow senescent leaves. Here, we document how the leaf-miner caterpillar Phyllonorycter blancardella, working through an endosymbiotic bacteria, modifies phytohormonal profiles, not only on senescing (photosynthetically inactive) but also on normal (photosynthetically active) leaf tissues of its host plant (Malus domestica). This leaf physiological manipulation allows the insect to maintain sugar-rich green tissues and to create an enhanced nutritional microenvironment in an otherwise degenerating context. It also allows them to maintain a nutritional homeostasis even under distinct leaf environments. Our study also highlights that only larvae harboring bacterial symbionts contain significant amounts of CKs that are most likely not plant-derived. This suggests that insects are able to provide CKs to the plant through their symbiotic association, thus extending further the role of insect bacterial symbionts in plant-insect interactions.

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Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts

Cited by 186 publications

References 37 publications

Are dominant plant species more susceptible to leaf‐mining insects? A case study at Saihanwula Nature Reserve, China

Are dominant plant species more susceptible to leaf‐mining insects? A case study at Saihanwula Nature Reserve, China

Cytokinins - recent news and views of evolutionally old molecules

Leaf-Miners Co-opt Microorganisms to Enhance their Nutritional Environment

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