Hostname: page-component-76fb5796d-wq484 Total loading time: 0 Render date: 2024-04-26T08:57:07.564Z Has data issue: false hasContentIssue false

Seed treatments with thiamine reduce the performance of generalist and specialist aphids on crop plants

Published online by Cambridge University Press:  05 June 2017

A.M. Hamada
Affiliation:
Botany and Microbiology Department, Faculty of Science, Assiut University, Assiut, Egypt
J. Fatehi
Affiliation:
Lantmännen BioAgri AB, Fågelbacksvägen 3, 756 51 Uppsala, Sweden
L.M.V. Jonsson*
Affiliation:
Department of Ecology, Environment and Plant Sciences, Stockholm University, 106 91 Stockholm, Sweden
*
*Author for correspondence: Phone: +46 8 161211 Fax: +46 8 165525 E-mail: lisbeth.jonsson@su.se

Abstract

Thiamine is a vitamin that has been shown to act as a trigger to activate plant defence and reduce pathogen and nematode infection as well as aphid settling and reproduction. We have here investigated whether thiamine treatments of seeds (i.e. seed dressing) would increase plant resistance against aphids and whether this would have different effects on a generalist than on specialist aphids. Seeds of wheat, barley, oat and pea were treated with thiamine alone or in combination with the biocontrol bacteria Pseudomonas chlororaphis MA 342 (MA 342). Plants were grown in climate chambers. The effects of seed treatment on fecundity, host acceptance and life span were studied on specialist aphids bird cherry-oat aphid (Rhopalosiphum padi L.) and pea aphid (Acyrthosiphon pisum Harris) and on the generalist green peach aphid (Myzus persicae, Sulzer). Thiamine seed treatments reduced reproduction and host acceptance of all three aphid species. The number of days to reproduction, the length of the reproductive life, the fecundity and the intrinsic rate of increase were found reduced for bird cherry-oat aphid after thiamine treatment of the cereal seeds. MA 342 did not have any effect in any of the plant-aphid combinations, except a weak decrease of pea aphid reproduction on pea. The results show that there are no differential effects of either thiamine or MA 342 seed treatments on specialist and generalist aphids and suggest that seed treatments with thiamine has a potential in aphid pest management.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahn, I.P., Kim, S. & Lee, Y.H. (2005) Vitamin B1 functions as an activator of plant disease resistance. Plant Physiology 138, 15051515.Google Scholar
Ahn, I.P., Kim, S., Lee, Y.H. & Suh, S.C. (2007) Vitamin B1-induced priming is dependent on hydrogen peroxide and the NPR1 gene in Arabidopsis. Plant Physiology 143, 838848.CrossRefGoogle ScholarPubMed
Avila, C.A., Arevalo-Soliz, L.M., Lorence, A. & Goggin, F.L. (2013) Expression of α-DIOXYGENASE 1 in tomato and Arabidopsis contributes to plant defenses against aphids. Molecular Plant-Microbe Interactions 8, 977986.Google Scholar
Bahuguna, R.N., Joshi, R., Shukla, A., Pandeby, M. & Kumar, J. (2012) Thiamine primed defense provides reliable alternative to systemic fungicide carbendazim against sheath blight disease in rice (Oryza sativa L.). Plant Physiology and Biochemistry 57, 159167.Google Scholar
Ban, L., Ahmed, E., Ninkovic, V., Delp, G. & Glinwood, R. (2008) Infection with an insect virus affects olfactory behaviour and interactions with host plant and natural enemies in an aphid. Entomologia Experimentalis et Applicata 127, 108117.Google Scholar
Bent, A.F. & Mackey, D. (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annual Review of Phytopathology 45, 399436.Google Scholar
Blackman, R.L. & Eastop, V.F. (2000) Aphids on the World's Crops. An Identification and Information Guide. Chichester, UK, Wiley & Sons.Google Scholar
Boubakri, H., Wahab, M.A., Chong, J., Bertsch, C., Mliki, A. & Soustre-Gacougnolle, I. (2012) Thiamine induced resistance to Plasmopara viticola in grapevine and elicited host-defense responses, including HR-like-cell death. Plant Physiology and Biochemistry 57, 120133.Google Scholar
Cabanás, C.G.L., Schilirò, E., Valverde-Corredor, A. & Mercado-Blanco, J. (2014) The biocontrol endophytic bacterium Pseudomonas fluorescens PICF7 induces systemic defense responses in aerial tissues upon colonization of olive roots. Frontiers in Microbiology 5, article 427. doi: 10.3389/fmicb.2014.00427.Google Scholar
Chaudhary, R., Atamian, H., Shen, Z., Briggs, S.P. & Kaloshian, I. (2014) GroEL from the endosymbiont Buchnera aphidicola betrays the aphid by triggering plant defense. Proceedings of the National Academy of Sciences of the United States of America 111, 89198924.Google Scholar
Chisholm, S.T., Coaker, G., Day, B. & Staskawicz, B.J. (2006) Host-microbe-interactions: shaping the evolution of the plant immunity response. Cell 124, 803814.Google Scholar
Conrath, U., Beckers, G.J.M., Langenbach, C.J.G. & Jaskiewicz, M.R. (2015) Priming for enhanced defense. Annual Review of Phytopathology 53, 97119.Google Scholar
Couldridge, C., Newbury, H.J., Ford-Lloyd, B., Bale, J.& Pritchard, J. (2007) Exploring plant responses to aphid feeding using a full Arabidopsis microarray reveals a small number of genes with significantly altered expression. Bulletin of Entomological Research 97, 523532.Google Scholar
Dancewicz, K., Sznajder, K., Zaluski, D., Kordan, B. & Gabrýs, B. (2016) Behavioral sensitivity of Myzus persicae to volatile isoprenoids in plant tissues. Entomologia Experimentalis et Applicata 160, 229240.CrossRefGoogle Scholar
Davis, J.A. & Radcliffe, E.B. (2008) Reproduction and feeding behavior of Myzus persicae on four cereals. Journal of Economic Entomology 101, 916.CrossRefGoogle ScholarPubMed
Delp, G., Gradin, T., Åhman, I. & Jonsson, L.M.V. (2009) Microarray analysis of the interaction between the aphid Rhopalosiphum padi and host plants reveals both differences and similarities between susceptible and partially resistant barley lines. Molecular Genetics and Genomics 281, 233248.Google Scholar
Edwards, O.R. (2001) Interspecific and intraspecific variation in the performance of three pest aphid species on five grain legume hosts. Entomologia Experimentalis et Applicata 100, 2130.Google Scholar
El-Zawahry, A.M. & Hamada, A.M. (1994) The effect of soaking seeds in ascorbic acid, pyridoxine or thiamine solutions on nematode (Meloidogyne javanica) infection and on some metabolic processes in egg plant. Assiut Journal of Agricultural Sciences 25, 233248.Google Scholar
Giordanengo, P., Brunissen, L., Rusterucci, C., Vincent, C., van Bel, A., Dinant, S., Girousse, C., Faucher, M. & Bonnemain, J-L. (2010) Compatible plant-aphid interactions: how aphids manipulate plant responses. Comptes Rendus Biologies 333, 516523.Google Scholar
Glinwood, R.T. & Pettersson, J. (2000) Change in response of Rhopalosiphum padi spring migrants to the repellent winter host component methyl salicylate. Entomologia Experimentalis et Applicata 94, 325330.CrossRefGoogle Scholar
Gosset, V., Harmel, N., Göbel, C., Francis, F., Haubruge, E., Wathelet, J-P., du Jardin, P., Feussner, I. & Fauconnier, M-L. (2009) Attacks by a piercing-sucking insect (Myzus persicae Sultzer) or a chewing insect (Leptinotarsa decemlineata Say) on potato plants (Solanum tuberosum L.) induce differential changes in volatile compound release and oxylipin synthesis. Journal of Experimental Botany 60, 12311240.Google Scholar
Greenslade, A.F.C., Ward, J.L., Martin, J.L., Corol, D.I., Clark, S.J., Smart, L.E. & Aradottir, G.I. (2016) Triticum monococcum lines with distinct metabolic phenotypes and phloem-based partial resistance to the bird cherry-oat aphid Rhopalosiphum padi . Annals of Applied Biology 168, 435449.Google Scholar
Hamada, A.M. & Jonsson, L.M.V. (2013) Thiamine treatments alleviate aphid infestations in barley and pea. Phytochemistry 94, 135141.Google Scholar
Hamada, A.M., El-Zawahry, A.M. & Al-Hakimi, A.M. (2001) Vitamin treatments for control of Meloidogyne javanica on egg plants. Journal of Russian Phytopathology Society 2, 6774.Google Scholar
Hewer, A., Becker, A. & van Bel, A. J. E. (2011) An aphid´s Odyssey- the cortical quest for the vascular bundle. Journal of Experimental Biology 214, 38683879.CrossRefGoogle ScholarPubMed
Hogenhout, S.A. & Bos, J.I.B. (2011) Effector proteins that modulate plant-insect interactions. Current Opinion in Plant Biology 14, 422428.Google Scholar
Huang, W.K., Ji, H.L., Gheysen, G. & Kyndt, T. (2016) Thiamine-induced priming against root-knot nematode infection in rice involves lignification and hydrogen peroxide generation. Molecular Plant Pathology 17, 614624.Google Scholar
Jaouannet, M., Morris, J.A., Hedley, P.E. & Bos, J.I.B. (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.Google Scholar
Johnsson, L., Hökeberg, M. & Gerhardson, B. (1998) Performance of the Pseudomonas chlororaphis biocontrol agent MA 342 against cereal seed-borne diseases in field experiments. European Journal of Plant Pathology 104, 701711.Google Scholar
Klingler, J., Powell, G., Thompson, G.A. & Isaacs, R. (1998) Phloem specific aphid resistance in Cucumis melo line AR5:effects on feeding behaviour and performance of Aphis gossypii . Entomologia Experimentalis et Applicata 86, 7988.Google Scholar
Klingler, J., Creasy, R., Gao, L., Nair, R.M., Calix, A.S., Jacob, H.S., Edwards, O.R. & Singh, K.B. (2005) Aphid resistance in Medicago truncatula involves antixenosis and phloem-specific, inducible antibiosis, and maps to a single locus flanked by NBS-LRR resistance gene analogs. Plant Physiology 137, 14451455.CrossRefGoogle ScholarPubMed
Louis, J. & Shah, J. (2013) Arabidopsis thaliana - Myzus persicae interaction: shaping the understanding of plant defense against phloem-feeding aphids. Frontiers in Plant Science 4, 118.Google Scholar
Pangesti, N., Pineda, A., Dicke, M. & van Loon, J.J.A. (2015) Variation in plant-mediated interactions between rhizobacteria and caterpillars: potential role of soil composition. Plant Biology 17, 474483.Google Scholar
Pieterse, C.M.J., Zamioudis, C., Berendsen, R.L., Weller, D.M., van Wees, S.C.M. & Bakker, P.A.H.M. (2014) Induced systemic resistance by beneficial microbes. Annual Review of Phytopathology 52, 347375.Google Scholar
Pineda, A., Zheng, S.J., van Loon, J.J.A., Pieterse, C.M.J. & Dicke, M. (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends in Plant Science 15, 507514.CrossRefGoogle ScholarPubMed
Pineda, A., Zheng, S.J., van Loon, J.J.A. & Dicke, M. (2012) Rhizobacteria modify plant-aphid interactions: a case of induced systemic susceptibility. Plant Biology 14, 8390.Google Scholar
Pitino, M. & Hogenhout, S.A. (2013) Aphid protein effectors promote aphid colonization in a plant species-specific manner. Molecular Plant-Microbe Interactions 26, 130139.Google Scholar
Pompon, J., Quiring, D., Giordanengo, P. & Pelletier, Y. (2010) Role of xylem consumption in Macrosiphum euphorbiae (Thomas). Journal of Insect Physiology 56, 610615.CrossRefGoogle ScholarPubMed
Pushpalatha, H.G., Sudisha, J., Geetha, N.P., Amruthesh, K.N. & Shetty, H.S. (2011) Thiamine seed treatment enhances LOX expression, promotes growth and induces downy mildew disease resistance in pearl millet. Biologia Plantarum 55, 522527.CrossRefGoogle Scholar
Shavit, R., Ofek-Lalzar, M., Burdman, S. & Morin, S. (2013) Inoculation of tomato plants with rhizobacteria enhances the performance of the phloem-feeding insect Bemisia tabaci . Frontiers in Plant Science 4, 306.Google Scholar
Singh, V., Louis, J., Ayre, B.G., Reese, J.C. & Shah, J. (2011). Trehalose phosphate synthase11-dependent trehalose metabolism promotes Arabidopsis thaliana defense against the phloem-feeding insect Myzus persicae . Plant Journal 67, 94104.Google Scholar
Smith, C.M. & Chuang, W-P. (2014) Plant resistance to aphid feeding: behavioral, physiological, genetic and molecular cues regulate aphid host selection and feeding. Pest Management Science 70, 528540.CrossRefGoogle ScholarPubMed
Sun, Y., Huang, X., Ning, Y., Jing, W., Bruce, T.J.A., Qi, F., Xu, Q., Wu, K., Zhang, Y. & Guo, Y. (2017) TPS46, a rice terpene synthase conferring natural resistance to bird cherry-oat aphid, Rhopalosiphum padi (Linnaeus). Frontiers in Plant Science 8, 110. doi: 10.3389/fpls.2017.00110.CrossRefGoogle ScholarPubMed
Thorpe, P., Cock, P.J.A. & Bos, J. (2016) Comparative transcriptomics and proteomics of three different aphid species identifies core and diverse effector sets. BMC Genomics 17, 172.Google Scholar
Tjallingii, W.F. (2006) Salivary secretions by aphids interacting with proteins of phloem wound responses. Journal of Experimental Botany 57, 739745.Google Scholar
Tombolini, R., van der Gaag, D.J., Gerhardson, G. & Jansson, J.K. (1999) Colonization pattern of the biocontrol strain Pseudomonas chlororaphis MA 342 on barley seeds visualized by using green fluorescent protein. Applied and Environmental Microbiology 65, 36743680.Google Scholar
Tzin, V., Fernandez-Pozo, N., Richter, A., Schmelz, E.A., Schoettner, M., Schäfer, M., Ahern, K.R., Meihls, L.N., Kaur, H., Huffaker, A., Mori, N., Degenhardt, J., Mueller, L.A. & Jander, G. (2015) Dynamic maize responses to aphid feeding are revealed by a time series of transcriptomic and metabolomic assays. Plant Physiology 169, 17271743.Google Scholar
Van Bel, A.J.E. & Will, T. (2016) Functional evaluation of proteins in watery and gel saliva of aphids. Frontiers in Plant Science 7, 1840. doi: 10.3389/fpls.2016.01840.Google Scholar
Vancanneyt, G., Sanz, C., Farmaki, T., Paneque, M., Ortego, F., Castañera, P. & Sánchez-Serrano, J.J. (2001) Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance. Proceedings of the National Academy of Sciences of the United States of America 98, 81398144.Google Scholar
Van Emden, H.F. & Harrington, R. (2007) Aphids as Crop Pests. Wallingford, UK, CABI Publishing.Google Scholar
Van Loon, L.C. (2007) Plant responses to plant growth-promoting rhizobacteria. European Journal of Plant Pathology 119, 243254.Google Scholar
Walters, D.R., Ratsep, J. & Havis, N.D. (2013) Controlling crop disease using induced resistance: challenges for the future. Journal of Experimental Botany 64, 12631280.Google Scholar
Will, T., Steckbauer, K., Hardt, M. & van Bel, A.J.E. (2012) Aphid gel saliva: sheath structure, protein composition and secretory dependence on stylet-tip milieu. PLoS ONE 7, e46903.Google Scholar
Wyatt, I.J. & White, P.F. (1977) Simple estimation of intrinsic increase rates for aphids and tetranychid mites. Journal of Applied Ecology 14, 757766.Google Scholar
Zhu, J. & Park, K-C. (2005) Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata . Journal of Chemical Ecology 31, 17331746.Google Scholar
Supplementary material: File

Hamada supplementary material

Figure S1

Download Hamada supplementary material(File)
File 922.6 KB