Defence gene expression and phloem quality contribute to mesophyll and phloem resistance to aphids in wild barley

Daniel J. Leybourne, Tracy A. Valentine, Jean A. H . Robertson , Estefania Pérez-Fernández, Angela M . Main , Alison J. Karley, Jorunn Bos (Lead / Corresponding author)

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

Aphids, including the bird cherry-oat aphid (Rhopalosiphum padi), are significant agricultural pests. The wild relative of barley, Hordeum spontaneum 5 (Hsp5), has been described to be partially resistant to R. padi, with this resistance proposed to involve higher thionin and lipoxygenase gene expression. However, the specificity of this resistance to aphids and its underlying mechanistic processes are unknown. In this study, we assessed the specificity of Hsp5 resistance to aphids and analysed differences in aphid probing and feeding behaviour on Hsp5 and a susceptible barley cultivar (Concerto). We found that partial resistance in Hsp5 to R. padi extends to two other aphid pests of grasses. Using the electrical penetration graph technique, we show that partial resistance is mediated by phloem- and mesophyll-based resistance factors that limit aphid phloem ingestion. To gain insight into plant traits responsible for partial resistance, we compared non-glandular trichome density, defence gene expression, and phloem composition of Hsp5 with those of the susceptible barley cultivar Concerto. We show that Hsp5 partial resistance involves elevated basal expression of thionin and phytohormone signalling genes, and a reduction in phloem quality. This study highlights plant traits that may contribute to broad-spectrum partial resistance to aphids in barley.

Original languageEnglish
Pages (from-to)4011-4026
Number of pages16
JournalJournal of Experimental Botany
Volume70
Issue number15
Early online date10 Apr 2019
DOIs
Publication statusPublished - 1 Aug 2019

Fingerprint

Hordeum vulgare subsp. spontaneum
Phloem
Aphids
Hordeum
mesophyll
phloem
Aphidoidea
Rhopalosiphum padi
barley
Gene Expression
gene expression
Thionins
pests
Diuraphis noxia
wild relatives
cultivars
lipoxygenase
plant hormones
trichomes
feeding behavior

Keywords

  • Amino acid composition
  • Hordeum spontaneum
  • Rhopalosiphum padi
  • Sitobion avenae
  • Utamphorophora humboldti
  • defence gene expression
  • electrical penetration graph (EPG)
  • partial resistance

Cite this

Leybourne, D. J., Valentine, T. A., Robertson , J. A. H. ., Pérez-Fernández, E., Main , A. M. ., Karley, A. J., & Bos, J. (2019). Defence gene expression and phloem quality contribute to mesophyll and phloem resistance to aphids in wild barley. Journal of Experimental Botany, 70(15), 4011-4026. https://doi.org/10.1093/jxb/erz163
Leybourne, Daniel J. ; Valentine, Tracy A. ; Robertson , Jean A. H . ; Pérez-Fernández, Estefania ; Main , Angela M . ; Karley, Alison J. ; Bos, Jorunn. / Defence gene expression and phloem quality contribute to mesophyll and phloem resistance to aphids in wild barley. In: Journal of Experimental Botany. 2019 ; Vol. 70, No. 15. pp. 4011-4026.
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abstract = "Aphids, including the bird cherry-oat aphid (Rhopalosiphum padi), are significant agricultural pests. The wild relative of barley, Hordeum spontaneum 5 (Hsp5), has been described to be partially resistant to R. padi, with this resistance proposed to involve higher thionin and lipoxygenase gene expression. However, the specificity of this resistance to aphids and its underlying mechanistic processes are unknown. In this study, we assessed the specificity of Hsp5 resistance to aphids and analysed differences in aphid probing and feeding behaviour on Hsp5 and a susceptible barley cultivar (Concerto). We found that partial resistance in Hsp5 to R. padi extends to two other aphid pests of grasses. Using the electrical penetration graph technique, we show that partial resistance is mediated by phloem- and mesophyll-based resistance factors that limit aphid phloem ingestion. To gain insight into plant traits responsible for partial resistance, we compared non-glandular trichome density, defence gene expression, and phloem composition of Hsp5 with those of the susceptible barley cultivar Concerto. We show that Hsp5 partial resistance involves elevated basal expression of thionin and phytohormone signalling genes, and a reduction in phloem quality. This study highlights plant traits that may contribute to broad-spectrum partial resistance to aphids in barley.",
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Leybourne, DJ, Valentine, TA, Robertson , JAH, Pérez-Fernández, E, Main , AM, Karley, AJ & Bos, J 2019, 'Defence gene expression and phloem quality contribute to mesophyll and phloem resistance to aphids in wild barley', Journal of Experimental Botany, vol. 70, no. 15, pp. 4011-4026. https://doi.org/10.1093/jxb/erz163

Defence gene expression and phloem quality contribute to mesophyll and phloem resistance to aphids in wild barley. / Leybourne, Daniel J.; Valentine, Tracy A.; Robertson , Jean A. H .; Pérez-Fernández, Estefania ; Main , Angela M .; Karley, Alison J.; Bos, Jorunn (Lead / Corresponding author).

In: Journal of Experimental Botany, Vol. 70, No. 15, 01.08.2019, p. 4011-4026.

Research output: Contribution to journalArticle

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T1 - Defence gene expression and phloem quality contribute to mesophyll and phloem resistance to aphids in wild barley

AU - Leybourne, Daniel J.

AU - Valentine, Tracy A.

AU - Robertson , Jean A. H .

AU - Pérez-Fernández, Estefania

AU - Main , Angela M .

AU - Karley, Alison J.

AU - Bos, Jorunn

N1 - D.J.L was funded by the James Hutton Institute and the Universities of Aberdeen and Dundee through a Scottish Food Security Alliance (Crops) PhD studentship. A.J.K, T.A.V, A.H.J.R, A.M.M, and E.P-F were supported by the strategic research programme funded by the Scottish Government’s Rural and Environment Science and Analytical Services Division. J.I.B.B. was supported by the European Research Council (310190-APHIDHOST). We would like to thank Dr Freddy Tjallingii (EPG Systems, The Netherlands), Professor Alberto Fereres (CSIC, Spain) and Professor Gregory Walker (University of California, Riverside, USA) for providing EPG training and Gaynor Malloch (James Hutton Institute) for kindly providing COI barcoding primers.

PY - 2019/8/1

Y1 - 2019/8/1

N2 - Aphids, including the bird cherry-oat aphid (Rhopalosiphum padi), are significant agricultural pests. The wild relative of barley, Hordeum spontaneum 5 (Hsp5), has been described to be partially resistant to R. padi, with this resistance proposed to involve higher thionin and lipoxygenase gene expression. However, the specificity of this resistance to aphids and its underlying mechanistic processes are unknown. In this study, we assessed the specificity of Hsp5 resistance to aphids and analysed differences in aphid probing and feeding behaviour on Hsp5 and a susceptible barley cultivar (Concerto). We found that partial resistance in Hsp5 to R. padi extends to two other aphid pests of grasses. Using the electrical penetration graph technique, we show that partial resistance is mediated by phloem- and mesophyll-based resistance factors that limit aphid phloem ingestion. To gain insight into plant traits responsible for partial resistance, we compared non-glandular trichome density, defence gene expression, and phloem composition of Hsp5 with those of the susceptible barley cultivar Concerto. We show that Hsp5 partial resistance involves elevated basal expression of thionin and phytohormone signalling genes, and a reduction in phloem quality. This study highlights plant traits that may contribute to broad-spectrum partial resistance to aphids in barley.

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KW - Amino acid composition

KW - Hordeum spontaneum

KW - Rhopalosiphum padi

KW - Sitobion avenae

KW - Utamphorophora humboldti

KW - defence gene expression

KW - electrical penetration graph (EPG)

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Leybourne DJ, Valentine TA, Robertson JAH, Pérez-Fernández E, Main AM, Karley AJ et al. Defence gene expression and phloem quality contribute to mesophyll and phloem resistance to aphids in wild barley. Journal of Experimental Botany. 2019 Aug 1;70(15):4011-4026. https://doi.org/10.1093/jxb/erz163