Changing from One Mine to Another

Hering, Erich M.

doi:10.1007/978-94-015-7196-8_5

Cited by 2 publications

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“…host-plant and a complete development within a restricted area of a single leaf (Hering, 1951;145 Pottinger and LeRoux, 1971; Connor and Taverner, 1997;Body et al, 2015). In this species, 146…”

Section: Introductionmentioning

confidence: 99%

“…gall-inducers, and leaf-miners. Their entire life-cycle is indeed usually restricted to the same 130 plant organ without diet switching capacities as observed for free-living external-feeding 131 insects (Hering, 1951;Stone and Schönrogge, 2003;Body et al, 2015). As such, they are the 132 most appropriate feeding-guild in which to examine nutritional constraints imposed by the 133 plant and adaptive strategies adopted by the insect to overcome these constraints.…”

Section: Introductionmentioning

confidence: 99%

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Manipulation of plant primary metabolism by leaf-mining larvae in the race against leaf senescence

Body

Casas

2019

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35 36 Plants are often considered as suboptimal food for phytophagous insects, requiring 37 them to employ various adaptive mechanisms to overcome food nutritional imbalances. This 38 could include host-plant manipulation and/or symbiotic associations. The extensive 39 reconfiguration of plant primary metabolism upon herbivory, as well as its impact on 40 herbivores, have been largely overlooked, while studies investigating secondary metabolites is 41 extensive. Here, we document how the apple leaf-mining caterpillar Phyllonorycter 42 blancardella, a highly-specialized insect which completes development within a restricted 43 area of a single Malus domestica leaf over successive different larval feeding modes, 44 maintains nutrient-rich green tissues in its feeding area on green and senescent leaves. For this 45 purpose, we quantified a large number of compounds involved in plant primary metabolism: 46 starch, total soluble sugars, five individual sugars, twenty protein-bound amino acids and 47 twenty free amino acids. Plant alteration can be observed not only on senescing 48 (photosynthetically inactive) but also normal (photosynthetically active) leaf tissues of its 49 host-plant to compensate for detrimental environmental variations. Our results show a 50 differential control of the primary metabolism depending on the larva developmental stage, 51 itself correlated to the fluid-feeding and tissue-feeding modes. Our results also suggest that 52 leaf amino acid alterations favor a faster insect development. Finally, chemical scores indicate 53 that the most growth-limiting essential amino acids are also common to other phytophagous 54 insects and large herbivores, suggesting that these limitations are a general consequence of 55 using plants as food source. We discuss the possible mechanisms responsible for these 56 different manipulative capacities, as well as their ecological implications. 57 58 Key words 59 60 plant-insect interaction; nutrition; nutritional homeostasis; plant primary metabolism; sugars; 61 essential amino acids; herbivorous insect; leaf-miner; feeding strategies; leaf senescence; 62 plant manipulation. 63 64 65 66Plants are abundantly present on Earth and are at the basis of most food webs. 67However, they are often suboptimal food sources for herbivores for three reasons (Mattson, 68 1980;Schoonhoven et al., 2005;Zhou et al., 2015). First, plant nutrient composition is highly 69 variable according to plant species, organ, season, and other environmental factors (Karasov 70 and Martínez Del Rio, 2007;Schoonhoven et al., 2005;Gündüz and Douglas, 2009). Such 71 variations of plant nutritional quality affect herbivore performance (Karley et al., 2002; 72 Schoonhoven et al., 2005;Larbat et al., 2016). Second, under pathogen infection and 73 herbivore attack, plants mount a defense response and increasing evidence shows an extensive 74reprogramming of plant metabolism (Schwachtje and Baldwin, 2008;Bolton, 2009; Kerchev 75 et al., 2012). Recent studies demonstrate that hundreds of plant ge...

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Manipulation of plant primary metabolism by leaf-mining larvae in the race against leaf senescence

Body

Casas

2019

Preprint

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Field application of the geometric framework reveals a multistep strategy of nutrient regulation in a leaf-miner

Body

Behmer

Pélisson

et al. 2019

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32Animals have evolved a vast array of behavioral and physiological strategies that allow 33 them to achieve a nutritionally balanced diet. Plants as food for herbivores are often considered 34 suboptimal, but phytophagous insects can employ pre-and post-ingestive mechanisms and/or 35 symbiotic associations to help overcome food nutritional imbalances. This is particularly crucial 36 for permanent multivoltine leaf-miner insects such as the caterpillar Phyllonorycter blancardella 37 which completes development within a restricted area of a single leaf and use deciduous leaves to 38 fuel growth and reproduction even under senescing autumnal conditions. Using the geometric 39 framework for nutrition under natural field conditions, we show that this insect has multiple 40 strategies to deal with inadequate food supply from the plant. First, larvae manipulate the protein-41 sugar content of both normal, photosynthetically active, and senescing, photosynthetically 42 inactive, leaf tissues. Control of nutritional homeostasis of mined tissues is however higher for 43 late instars, which differ from younger larval instars in their feeding mode (fluidvs. tissue-44 feeder). Second, slight differences in the protein-sugar environment remain between mined 45 tissues on green and yellow leaves despite this manipulation of the leaf physiology. This insect 46 uses post-ingestive mechanisms to achieve similar body protein, sugar and lipid composition. 47This study demonstrates, for the first time under natural conditions, the ability of an insect 48 herbivore to practice a combination of pre-and post-ingestive compensatory mechanisms to 49 attain similar growth and metabolic outcomes in fundamentally different nutritional 50 environments. Additionally, a comparison of larval nutritional requirements of 117 species from 51 various insect groups further reinforces the hypothesis of a close association between P. 52 blancardella and endosymbiotic bacteria for nutritional purposes. 53 54 55 Body et al. Page 4 of 32 Key words 56 Plant-insect interaction; nutrient acquisition; leaf manipulation; sugar metabolism; endosymbiont. 57 58 470 471This study has been supported by the ANR project to DG ECOREN ANR-JC05-46491 472 and the Région Centre project to DG ENDOFEED 201000047141. We thank L. Ardouin for full 473 access to his orchard, S. Venner for access to his lab, and W. Kaiser, E. Huguet, J.-P. Christidès, 474 and the "Endofeed team" for helpful discussions. 475 476 Conflict of Interest 477The authors declare that they have no conflict of interest. 478 479

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Changing from One Mine to Another

Cited by 2 publications

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Manipulation of plant primary metabolism by leaf-mining larvae in the race against leaf senescence

Manipulation of plant primary metabolism by leaf-mining larvae in the race against leaf senescence

Field application of the geometric framework reveals a multistep strategy of nutrient regulation in a leaf-miner

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