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Petiole gall aphid (Pemphigus spyrothecae) infestation of Populus × petrovskiana leaves alters foliage photosynthetic characteristics and leads to enhanced emissions of both constitutive and stress-induced volatiles

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Abstract

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Massive infection of Populus × petrovskiana leaves by petiole gall aphids (Pemphigus spyrothecae) significantly decreased leaf dry mass per unit area, N content per dry mass and net assimilation rate per area, and increased stomatal conductance, leaf dry mass per fresh mass, and constitutive emissions of isoprene. The infection also induced emissions of green leaf volatiles, monoterpenes and benzenoids. The emissions scaled with the infection severity as assessed by dry gall mass per leaf dry mass.

Abstract

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 (Mg/Ml) was used as a quantitative measure of the severity of gall infestation. Very high fraction of leaf biomass was invested in gall formation with Mg/Ml varying between 0.5 and 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. Enhanced 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.

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Acknowledgements

This study has been funded by the European Research Council (Advanced Grant 322603, SIP-VOL+), the Estonian Ministry of Science and Education (Institutional Grant IUT-8-3) and the European Commission through the European Regional Fund (Center of Excellence EcolChange).

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  1. Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Kreutzwaldi 1, 51014, Tartu, Estonia

    Jiayan Ye, Yifan Jiang, Linda-Liisa Veromann-Jürgenson & Ülo Niinemets

  2. Estonian Academy of Sciences, Kohtu 6, 10130, Tallinn, Estonia

    Ülo Niinemets

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  1. Jiayan Ye
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Correspondence to Yifan Jiang.

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Fig. S1

. Schematic overview of the two-channel custom-designed gas-exchange system applied for measurements of photosynthesis, transpiration and trace gas emissions in Populus × petrovskiana leaf infested by Pemphigus spyrothecae aphid galls. (DOCX 22 KB)

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Ye, J., Jiang, Y., Veromann-Jürgenson, LL. et al. Petiole gall aphid (Pemphigus spyrothecae) infestation of Populus × petrovskiana leaves alters foliage photosynthetic characteristics and leads to enhanced emissions of both constitutive and stress-induced volatiles. Trees 33, 37–51 (2019). https://doi.org/10.1007/s00468-018-1756-2

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