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Oak gall wasp infections of Quercus robur leaves lead to profound modifications in foliage photosynthetic and volatile emission characteristics.

ABSTRACT: Oak trees (Quercus) are hosts of diverse gall-inducing parasites, but the effects of gall formation on the physiology and biochemistry on host oak leaves is poorly understood. The influence of infection by four species from two widespread gall wasp genera, Neuroterus (N. anthracinus and N. albipes) and Cynips (C. divisa and C. quercusfolii), on foliage morphology, chemistry, photosynthetic characteristics, constitutive isoprene, and induced volatile emissions in Q. robur was investigated. Leaf dry mass per unit area (M_A ), net assimilation rate per area (A_A ), stomatal conductance (g_s ), and constitutive isoprene emissions decreased with the severity of infection by all gall wasp species. The reduction in A_A was mainly determined by reduced M_A and to a lower extent by lower content of leaf nitrogen and phosphorus in gall-infected leaves. The emissions of lipoxygenase pathway volatiles increased strongly with increasing infection severity for all 4 species with the strongest emissions in major vein associated species, N. anthracinus. Monoterpene and sesquiterpene emissions were strongly elicited in N. albipes and Cynips species, but not in N. anthracinus. These results provide valuable information for diagnosing oak infections using ambient air volatile fingerprints and for predicting the impacts of infections on photosynthetic productivity and whole tree performance.

SUBMITTER: Jiang Y

PROVIDER: S-EPMC6047732 | biostudies-literature | 2018 Jan

REPOSITORIES: biostudies-literature

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Oak gall wasp infections of Quercus robur leaves lead to profound modifications in foliage photosynthetic and volatile emission characteristics.

Jiang Yifan Y Veromann-Jürgenson Linda-Liisa LL Ye Jiayan J Niinemets Ülo Ü

Plant, cell & environment 20171121 1

Oak trees (Quercus) are hosts of diverse gall-inducing parasites, but the effects of gall formation on the physiology and biochemistry on host oak leaves is poorly understood. The influence of infection by four species from two widespread gall wasp genera, Neuroterus (N. anthracinus and N. albipes) and Cynips (C. divisa and C. quercusfolii), on foliage morphology, chemistry, photosynthetic characteristics, constitutive isoprene, and induced volatile emissions in Q. robur was investigated. Leaf d ...[more]

PMID: 28776716

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Project description:Galls are plant tissues whose development is induced by another organism for the inducer's benefit. 30,000 arthropod species induce galls, and in most cases the inducing effectors and target plant systems are unknown. Cynipid gall wasps are a speciose monophyletic radiation that induce structurally complex galls on oaks and other plants. We used a model system comprising the gall wasp Biorhiza pallida and the oak Quercus robur to characterise inducer and host plant gene expression at defined stages through the development of galled and ungalled plant tissues, and tested alternative hypotheses for the origin and type of galling effectors and plant metabolic pathways involved. Oak gene expression patterns diverged markedly during development of galled and normal buds. Young galls showed elevated expression of oak genes similar to legume root nodule Nod factor-induced early nodulin (ENOD) genes and developmental parallels with oak buds. In contrast, mature galls showed substantially different patterns of gene expression to mature leaves. While most oak transcripts could be functionally annotated, many gall wasp transcripts of interest were novel. We found no evidence in the gall wasp for involvement of third-party symbionts in gall induction, for effector delivery using virus-like-particles, or for gallwasp expression of genes coding for plant hormones. Many differentially and highly expressed genes in young larvae encoded secretory peptides, which we hypothesise are effector proteins exported to plant tissues. Specifically, we propose that host arabinogalactan proteins and gall wasp chitinases interact in young galls to generate a somatic embryogenesis-like process in oak tissues surrounding the gall wasp larvae. Gall wasp larvae also expressed genes encoding multiple plant cell wall degrading enzymes (PCWDEs). These have functional orthologues in other gall inducing cynipids but not in figitid parasitoid sister groups, suggesting that they may be evolutionary innovations associated with cynipid gall induction.

Project description:Current carbon cycle models attribute rising atmospheric CO2 as the major driver of the increased terrestrial carbon sink, but with substantial uncertainties. The photosynthetic response of trees to elevated atmospheric CO2 is a necessary step, but not the only one, for sustaining the terrestrial carbon uptake, but can vary diurnally, seasonally and with duration of CO2 exposure. Hence, we sought to quantify the photosynthetic response of the canopy-dominant species, Quercus robur, in a mature deciduous forest to elevated CO2 (eCO2) (+150 μmol mol-1 CO2) over the first 3 years of a long-term free air CO2 enrichment facility at the Birmingham Institute of Forest Research in central England (BIFoR FACE). Over 3000 measurements of leaf gas exchange and related biochemical parameters were conducted in the upper canopy to assess the diurnal and seasonal responses of photosynthesis during the 2nd and 3rd year of eCO2 exposure. Measurements of photosynthetic capacity via biochemical parameters, derived from CO2 response curves, (Vcmax and Jmax) together with leaf nitrogen concentrations from the pre-treatment year to the 3rd year of eCO2 exposure, were examined. We hypothesized an initial enhancement in light-saturated net photosynthetic rates (Asat) with CO2 enrichment of ≈37% based on theory but also expected photosynthetic capacity would fall over the duration of the study. Over the 3-year period, Asat of upper-canopy leaves was 33 ± 8% higher (mean and standard error) in trees grown in eCO2 compared with ambient CO2 (aCO2), and photosynthetic enhancement decreased with decreasing light. There were no significant effects of CO2 treatment on Vcmax or Jmax, nor leaf nitrogen. Our results suggest that mature Q. robur may exhibit a sustained, positive response to eCO2 without photosynthetic downregulation, suggesting that, with adequate nutrients, there will be sustained enhancement in C assimilated by these mature trees. Further research will be required to understand the location and role of the additionally assimilated carbon.

Project description:Poplar spiral gall aphid (Pemphigus spyrothecae) forms galls on the petiole in poplars (Populus) and mass infestations are frequent in poplar stands, but how these parasite gall infestations can affect the leaf lamina structure, photosynthetic rate and constitutive and stress volatile emissions is unknown. We investigated how the infestation by the petiole gall aphids affects lamina photosynthetic characteristics (net assimilation rate, stomatal conductance), C and N contents, and constitutive isoprene and induced volatile emissions in Populus × petrovskiana. The dry gall mass per leaf dry mass (M g/M l) was used as a quantitative measure of the severity of gall infestation. Very high fraction of leaf biomass was invested in gall formation with M g/M l varying between 0.5-2. Over the whole range of the infestation severities, net assimilation rate per area, leaf dry mass per unit area and N content decreased with increasing the severity of infestation. In contrast, stomatal conductance, leaf dry mass per fresh mass, constitutive isoprene emissions, and induced green leaf volatile (GLV), monoterpene, sesquiterpene and benzenoid emissions increased with increasing the severity of gall infestation. The rates of induced emissions were low and these emissions were associated with methyl jasmonate release from leaf laminas. The data demonstrate that petiole gall infestations lead to major changes in leaf lamina sink-source relationships and leaf water relations, thereby significantly altering lamina photosynthesis. Modifications in stress-induced emissions likely indicated systemic signaling triggered by jasmonate transported from the petiole galls to the lamina where jasmonate elicited a cascade of volatile emission responses. Enhance isoprene emissions and induced volatile emissions can play a major role in indirect defense against other herbivores, securing the food source for the gall aphids. In conclusion, a massive infestation by petiole gall aphids can profoundly modify the foliage photosynthetic performance and volatile emission profiles in poplars.

Dataset Information

Oak gall wasp infections of Quercus robur leaves lead to profound modifications in foliage photosynthetic and volatile emission characteristics.

Publications

Oak gall wasp infections of Quercus robur leaves lead to profound modifications in foliage photosynthetic and volatile emission characteristics.

Similar Datasets

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