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The Impact of Phloem Feeding Insects on Leaf Ecophysiology Varies With Leaf Age.

ABSTRACT: Herbivore insects have strong impacts on leaf gas exchange when feeding on the plant. Leaf age also drives leaf gas exchanges but the interaction of leaf age and phloem herbivory has been largely underexplored. We investigated the amplitude and direction of herbivore impact on leaf gas exchange across a wide range of leaf age in the apple tree-apple green aphid (Aphis pomi) system. We measured the gas exchange (assimilation and transpiration rates, stomatal conductance and internal CO₂ concentration) of leaves infested versus non-infested by the aphid across leaf age. For very young leaves up to 15 days-old, the gas exchange rates of infested leaves were similar to those of non-infested leaves. After few days, photosynthesis, stomatal conductance and transpiration rate increased in infested leaves up to about the age of 30 days, and gradually decreased after that age. By contrast, gas exchanges in non-infested leaves gradually decreased across leaf age such that they were always lower than in infested leaves. Aphids were observed on relatively young leaves up to 25 days and despite the positive effect on leaf photosynthesis and leaf performance, their presence negatively affected the growth rate of apple seedlings. Indeed, aphids decreased leaf dry mass, leaf surface, and leaf carbon content except in old leaves. By contrast, aphids induced an increase in leaf nitrogen content and the deviation relative to non-infested leaves increased with leaf age. Overall, the impacts of aphids at multiple levels of plant performance depend on leaf age. While aphids cause an increase in some leaf traits (gas exchanges and nitrogen content), they also depress others (plant growth rate and carbon content). The balance between those effects, as modulated by leaf age, may be the key for herbivory mitigation in plants.

SUBMITTER: Pincebourde S

PROVIDER: S-EPMC8322987 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundOutbreaks of insect pests in paddy fields cause heavy losses in global rice yield annually, a threat projected to be aggravated by ongoing climate warming. Although significant progress has been made in the screening and cloning of insect resistance genes in rice germplasm and their introgression into modern cultivars, improved rice resistance is only effective against either chewing or phloem-feeding insects.ResultsIn this study, the results from standard and modified seedbox screening, settlement preference and honeydew excretion tests consistently showed that Qingliu, a previously known leaffolder-resistant rice variety, is also moderately resistant to brown planthopper (BPH). High-throughput RNA sequencing showed a higher number of differentially expressed genes (DEGs) at the infestation site, with 2720 DEGs in leaves vs 181 DEGs in sheaths for leaffolder herbivory and 450 DEGs in sheaths vs 212 DEGs in leaves for BPH infestation. The leaf-specific transcriptome revealed that Qingliu responds to leaffolder feeding by activating jasmonic acid biosynthesis genes and genes regulating the shikimate and phenylpropanoid pathways that are essential for the biosynthesis of salicylic acid, melatonin, flavonoids and lignin defensive compounds. The sheath-specific transcriptome revealed that Qingliu responds to BPH infestation by inducing salicylic acid-responsive genes and those controlling cellular signaling cascades. Taken together these genes could play a role in triggering defense mechanisms such as cell wall modifications and cuticular wax formation.ConclusionsThis study highlighted the key defensive responses of a rarely observed rice variety Qingliu that has resistance to attacks by two different feeding guilds of herbivores. The leaffolders are leaf-feeder while the BPHs are phloem feeders, consequently Qingliu is considered to have dual resistance. Although the defense responses of Qingliu to both insect pest types appear largely dissimilar, the phenylpropanoid pathway (or more specifically phenylalanine ammonia-lyase genes) could be a convergent upstream pathway. However, this possibility requires further studies. This information is valuable for breeding programs aiming to generate broad spectrum insect resistance in rice cultivars.

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The Impact of Phloem Feeding Insects on Leaf Ecophysiology Varies With Leaf Age.

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