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Aphid-induced accumulation of trehalose in Arabidopsis thaliana is systemic and dependent upon aphid density

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Abstract

Trehalose is a disaccharide sugar that is now considered to be widely distributed among higher plants. Trehalose has been attributed a number of roles, including control of basic plant processes, such as photosynthesis, and conferring tolerance to abiotic stresses, such as desiccation and high salinity. Trehalose is also a common storage sugar used by insects. In this study, we used laboratory investigations to examine various aspects of trehalose dynamics in an aphid–host plant system (Arabidopsis and the peach potato aphid, Myzus persicae). Trehalose concentrations were measured by [1-H]-NMR. Myzus persicae reared on Arabidopsis, but not on black mustard or spring cabbage, contained considerable quantities of trehalose (5 % w/w dry matter). In Arabidopsis foliage, feeding by aphids induced a density-dependent accumulation of trehalose up to 5 mg g−1 dry weight. Leaves that were not challenged directly by aphids also exhibited increased trehalose concentrations, indicating that this accumulation was systemic. Trehalose was measured at high concentrations in the phloem sap of plants challenged by aphids, suggesting that aphid feeding induced the plant to produce significant quantities of trehalose, which moved through the plant and into the aphids via the phloem sap. Trehalose was also excreted in the aphid honeydew. Further work is required to clarify whether this trehalose accumulation in Arabidopsis has a direct role or a signalling function in plant tolerance of, or resistance to, aphid feeding, and if a similar accumulation of this sugar occurs when other species or genotypes of aphids are reared on this host plant.

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Abbreviations

ANOVA:

Analysis of variance

DW:

Dry weight

EDTA:

Ethylenediaminetetraacetic acid

HPLC:

High performance liquid-chromatography

NMR:

Nuclear magnetic resonance

TSP:

Trimethylsilylpropionate

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Acknowledgments

This work was funded via a Grant from the UK Biotechnology and Biological Sciences Research Council (BBSRC) and [1H]-NMR profiling was carried out by the BBSRC-funded (MET20482) MeT-RO metabolomics centre at Rothamsted Research who also receive grant-aided support from BBSRC. Our thanks go to Dr Martin Selby and Miss Aimee Llewellyn who provided technical support at Imperial College and Rothamsted Research, respectively. We also thank two anonymous reviewers who provided highly insightful comments and detailed questions on an earlier draft of this manuscript.

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Correspondence to Simon Hodge.

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Hodge, S., Ward, J.L., Beale, M.H. et al. Aphid-induced accumulation of trehalose in Arabidopsis thaliana is systemic and dependent upon aphid density. Planta 237, 1057–1064 (2013). https://doi.org/10.1007/s00425-012-1826-4

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  • DOI: https://doi.org/10.1007/s00425-012-1826-4

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