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Plant resistance in different cell layers affects aphid probing and feeding behaviour during non-host and poor-host interactions

Published online by Cambridge University Press:  16 June 2020

Carmen Escudero-Martinez ,
Daniel J. Leybourne  and
Jorunn I.B. Bos Open the ORCID record for Jorunn I.B. Bos [Opens in a new window]
Carmen Escudero-Martinez
Affiliation:
Cell and Molecular Sciences, The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, UK Division of Plant Sciences, School of Life Sciences, University of Dundee, Dundee, Scotland
Daniel J. Leybourne
Affiliation:
Cell and Molecular Sciences, The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, UK Division of Plant Sciences, School of Life Sciences, University of Dundee, Dundee, Scotland
Jorunn I.B. Bos*
Affiliation:
Cell and Molecular Sciences, The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, UK Division of Plant Sciences, School of Life Sciences, University of Dundee, Dundee, Scotland
*
Author for correspondence: Jorunn I.B. Bos, Email: [email protected]
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Abstract

Aphids are phloem-feeding insects that cause economic losses to crops globally. Whilst aphid interactions with susceptible plants and partially resistant genotypes have been well characterized, the interactions between aphids and non-host species are not well understood. Unravelling these non-host interactions can identify the mechanisms which contribute to plant resistance. Using contrasting aphid-host plant systems, including the broad host range pest Myzus persicae (host: Arabidopsis; poor-host: barley) and the cereal pest Rhopalosiphum padi (host: barley; non-host: Arabidopsis), we conducted a range of physiological experiments and compared aphid settling and probing behaviour on a host plant vs either a non-host or poor-host. In choice experiments, we observed that around 10% of aphids selected a non-host or poor-host plant species after 24 h. Using the Electrical Penetration Graph technique, we showed that feeding and probing behaviours differ during non-host and poor-host interactions when compared with a host interaction. In the Arabidopsis non-host interaction with the cereal pest R. padi aphids were unable to reach and feed on the phloem, with resistance likely residing in the mesophyll cell layer. In the barley poor-host interaction with M. persicae, resistance is likely phloem-based as phloem ingestion was reduced compared with the host interaction. Overall, our data suggest that plant resistance to aphids in non-host and poor-host interactions with these aphid species likely resides in different plant cell layers. Future work will take into account specific cell layers where resistances are based to dissect the underlying mechanisms and gain a better understanding of how we may improve crop resistance to aphids.

Keywords

AphidEPG analysesnonhostplant resistanceprobingstylet pathway
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 1 , February 2021 , pp. 31 - 38
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally.

References

Alvarez, AE, Tjallingii, WF, Garzo, E, Vleeshouwers, V, Dicke, M and Vosman, B (2006) Location of resistance factors in the leaves of potato and wild tuber-bearing Solanum species to the aphid Myzus persicae. Entomologia Experimentalis Et Applicata 121, 145–157.CrossRefGoogle Scholar
Bellande, K, Bono, JJ, Savelli, B, Jamet, E and Canut, H (2017) Plant lectins and lectin receptor-like kinases: how Do they sense the outside? International Journal of Molecular Sciences 18, 1164.CrossRefGoogle ScholarPubMed
Blackman, RL and Eastop, VF (2000) Aphids on the World's Crops. Chichester: Wiley & sons, p. 466.Google Scholar
Boyes, DC, Zayed, AM, Ascenzi, R, Mccaskill, AJ, Hoffman, NE, Davis, KR and Gorlach, J (2001) Growth stage-based phenotypic analysis of arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13, 1499–1510.Google Scholar
Debokx, JA and Piron, PGM (1990) Relative efficiency of a number of aphid species in the transmission of Potato Virus-YN in the Netherlands. Netherlands Journal of Plant Pathology 96, 237–246.Google Scholar
Doring, TF (2014) How aphids find their host plants, and how they don't. Annals of Applied Biology 165, 3–26.CrossRefGoogle Scholar
Doring, TF and Chittka, L (2007) Visual ecology of aphids-a critical review on the role of colours in host finding. Arthropod-Plant Interactions 1, 3–16.CrossRefGoogle Scholar
Dreyer, DL and Campbell, BC (1987) Chemical basis of host-plant resistance to aphids. Plant Cell and Environment 10, 353–361.Google Scholar
Dreyer, DL and Jones, KC (1981) Feeding deterrency of flavonoids and related phenolics towards Schizaphis-Graminum and Myzus-Persicae - aphid feeding deterrents in wheat. Phytochemistry 20, 2489–2493.CrossRefGoogle Scholar
Escudero-Martinez, CM, Morris, JA, Hedley, PE and Bos, JIB (2017) Barley transcriptome analyses upon interaction with different aphid species identify thionins contributing to resistance. Plant Cell and Environment 40, 2628–2643.CrossRefGoogle ScholarPubMed
Garbys, B and Pawluk, M (1999) Acceptability of different species of Brassicaeceae as hosts for the cabbage aphid. Entomologia Expertimentalis et Applicata 91, 105–109.Google Scholar
Giordanengo, P (2014) EPG-Calc: a PHP-based script to calculate electrical penetration graph (EPG) parameters. Arthropod-Plant Interactions 8, 163–169.CrossRefGoogle Scholar
Hopkins, DP, Cameron, DD and Butlin, RK (2017) The chemical signatures underlying host plant discrimination by aphids. Scientific Reports 7, 8498.CrossRefGoogle ScholarPubMed
Jaber, K, Haubruge, E and Francis, F (2010) Development of entomotoxic molecules as control agents: illustration of some protein potential uses and limits of lectins. Biotechnologie Agronomie Societe Et Environnement 14, 225–241.Google Scholar
Jaouannet, M, Morris, JA, Hedley, PE and Bos, JI (2015) Characterization of Arabidopsis transcriptional responses to different aphid Species reveals genes that contribute to host susceptibility and non-host resistance. PLoS Pathogens 11, e1004918.CrossRefGoogle ScholarPubMed
Katis, N and Gibson, RW (1985) Transmission of potato virus-y by cereal aphids. Potato Research 28, 65–70.CrossRefGoogle Scholar
Kehr, J (2006) Phloem sap proteins: their identities and potential roles in the interaction between plants and phloem-feeding insects. Journal of Experimental Botany 57, 767–774.CrossRefGoogle ScholarPubMed
Lenth, RV (2016) Least-Squares means: the R package lsmeans. Journal of Statistical Software 69, 1–33.CrossRefGoogle Scholar
Leybourne, DJ, Bos, JIB, Valentine, TA and Karley, AJ (2020) The price of protection: a defensive endosymbiont impairs nymph growth in the bird cherry-oat aphid, Rhopalosiphum padi. Insect Science 27, 69–85.CrossRefGoogle Scholar
Mallinger, RE, Hogg, DB and Gratton, C (2011) Methyl salicylate attracts natural enemies and reduces populations of soybean aphids (Hemiptera: Aphididae) in soybean agroecosystems. Journal of Economic Entomology 104, 115–124.CrossRefGoogle Scholar
Mayoral, AM, Tjallingii, WF and Castanera, P (1996) Probing behaviour of Diuraphis noxia on five cereal species with different hydroxamic acid levels. Entomologia Experimentalis Et Applicata 78, 341–348.CrossRefGoogle Scholar
Medina-Ortega, KJ and Walker, GP (2015) Faba bean forisomes can function in defence against generalist aphids. Plant Cell and Environment 38, 1167–1177.CrossRefGoogle ScholarPubMed
Neal, JJ, Tingey, WM and Steffens, JC (1990) Sucrose esters of carboxylic-acids in Glandular Trichomes of Solanum-Berthaultii deter settling and probing by green peach aphid. Journal of Chemical Ecology 16, 487–497.CrossRefGoogle Scholar
Nottingham, SF, Hardie, J, Dawson, GW, Hick, AJ, Pickett, JA, Wadhams, LJ and Woodcock, CM (1991) Behavioral and electrophysiological responses of aphids to host and nonhost plant volatiles. Journal of Chemical Ecology 17, 1231–1242.CrossRefGoogle ScholarPubMed
Nowak, H and Komor, E (2010) How aphids decide what is good for them: experiments to test aphid feeding behaviour on Tanacetum vulgare (L.) using different nitrogen regimes. Oecologia 163, 973–984.CrossRefGoogle ScholarPubMed
Pegadaraju, V, Louis, J, Singh, V, Reese, JC, Bautor, J, Feys, BJ, Cook, G, Parker, JE and Shah, J (2007) Phloem-based resistance to green peach aphid is controlled by Arabidopsis Phytoalexin Deficient4 without its signaling partner enhanced disease Susceptibility1. Plant Journal 52, 332–341.CrossRefGoogle ScholarPubMed
Pompon, J, Quiring, D, Giordanengo, P and Pelletier, Y (2010) Role of xylem consumption on osmoregulation in Macrosiphum euphorbiae (Thomas). Journal of Insect Physiology 56, 610–615.CrossRefGoogle Scholar
Powell, G, Tosh, CR and Hardie, J (2006) Host plant selection by aphids: behavioral, evolutionary, and applied perspectives. Annual Review of Entomology 51, 309–330.CrossRefGoogle ScholarPubMed
Prado, E and Tjallingii, WF (1994) Aphid activities during sieve element punctures. Entomologia Experimentalis Et Applicata 72, 157–165.CrossRefGoogle Scholar
Prado, E and Tjallingii, WF (1997) Effects of previous plant infestation on sieve element acceptance by two aphids. Entomologia Experimentalis Et Applicata 82, 189–200.CrossRefGoogle Scholar
R Core Team (2017). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/.Google Scholar
Ramirez, CC and Niemeyer, HM (2000) The influence of previous experience and starvation on aphid feeding behavior. Journal of Insect Behavior 13, 699–709.CrossRefGoogle Scholar
Read, SM and Northcote, DH (1983) Subunit structure and interactions of the Phloem proteins of Cucurbita-Maxima (Pumpkin). European Journal of Biochemistry 134, 561–569.CrossRefGoogle Scholar
Sauvion, N, Rahbe, Y, Peumans, WJ, Vandamme, EJM, Gatehouse, JA and Gatehouse, AMR (1996) Effects of GNA and other mannose binding lectins on development and fecundity of the peach-potato aphid Myzus persicae. Entomologia Experimentalis Et Applicata 79, 285–293.CrossRefGoogle Scholar
Schwarzkopf, A, Rosenberger, D, Niebergall, M, Gershenzon, J and Kunert, G (2013) To feed or not to feed: plant factors located in the epidermis, mesophyll, and sieve elements influence pea aphid's ability to feed on legume species. PLoS One 8, e75298.CrossRefGoogle ScholarPubMed
Spiller, NJ, Koenders, L and Tjallingii, WF (1990) Xylem ingestion by aphids - a strategy for maintaining water-balance. Entomologia Experimentalis Et Applicata 55, 101–104.CrossRefGoogle Scholar
Thorpe, P, Escudero-Martinez, C, Cock, P, Laetsch, D, Eves-Van Den Akker, S and Bos, J (2018) Shared transcriptional control and disparate gain and loss of aphid parasitism genes and loci acquired via horizontal gene transfer. bioRxiv, 246801.CrossRefGoogle Scholar
Tjallingii, WF (1978) Electronic recording of penetration behavior by aphids. Entomologia Experimentalis Et Applicata 24, 721–730.CrossRefGoogle Scholar
Tjallingii, WF (1985a) Electrical nature of recorded signals during stylet penetration by aphids. Entomologia Experimentalis Et Applicata 38, 177–186.CrossRefGoogle Scholar
Tjallingii, WF (1985b) Membrane-potentials as an indication for plant-cell penetration by aphid stylets. Entomologia Experimentalis Et Applicata 38, 187–193.CrossRefGoogle Scholar
Tjallingii, WF (1995) Aphid-plant interactions: what goes on in the depth of the tissues? Proceedings of the Section Experimental and Applied Entomology of the Netherlands Entomological Society (N.E.V.), Vol 6, 1995, 163–169.Google Scholar
Tjallingii, WF (2006) Salivary secretions by aphids interacting with proteins of phloem wound responses. Journal of Experimental Botany 57, 739–745.CrossRefGoogle ScholarPubMed
Tjallingii, WF and Esch, TH (1993) Fine-structure of aphid stylet routes in plant-tissues in correlation with EPG signals. Physiological Entomology 18, 317–328.CrossRefGoogle Scholar
Turlings, TCJ and Ton, J (2006) Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests. Current Opinion in Plant Biology 9, 421–427.CrossRefGoogle ScholarPubMed
Verbeek, M, Piron, PGM, Dullemans, AM, Cuperus, C and Van Der Vlugt, RAA (2010) Determination of aphid transmission efficiencies for N, NTN and Wilga strains of Potato virus Y. Annals of Applied Biology 156, 39–49.CrossRefGoogle Scholar
Weisberg, S and Fox, J (2011) An R Companion to Applied Regression. Thousand Oaks: Sage.Google Scholar
Will, T and Van Bel, AJE (2006) Physical and chemical interactions between aphids and plants. Journal of Experimental Botany 57, 729–737.CrossRefGoogle ScholarPubMed
Zadoks, JC, Chang, TT and Konzak, CF (1974) Decimal code for growth stages of cereals. Weed Research 14, 415–421.CrossRefGoogle Scholar
Zhang, CL, Shi, HJ, Chen, L, Wang, XM, Lu, BB, Zhang, SP, Liang, YA, Liu, RX, Qian, J, Sun, WW, You, ZZ and Dong, HS (2011) Harpin-induced expression and transgenic overexpression of the phloem protein gene AtPP2-A1 in Arabidopsis repress phloem feeding of the green peach aphid Myzus persicae. Bmc Plant Biology 11, 19.CrossRefGoogle ScholarPubMed
Züst, T and Agrawal, AA (2016) Mechanisms and evolution of plant resistance to aphids. Nature Plants 2, 15206.CrossRefGoogle ScholarPubMed
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