Hostname: page-component-77c89778f8-n9wrp Total loading time: 0 Render date: 2024-07-17T17:21:43.704Z Has data issue: false hasContentIssue false
  • English
  • Français

Induced resistance against the Asian citrus psyllid, Diaphorina citri, by β-aminobutyric acid in citrus

Published online by Cambridge University Press:  16 April 2013

Siddharth Tiwari ,
Wendy L. Meyer  and
Lukasz L. Stelinski
Siddharth Tiwari
Affiliation:
Entomology and Nematology Department, Citrus Research and Education Center, University of Florida, Lake Alfred, FL 33850, USA
Wendy L. Meyer
Affiliation:
Entomology and Nematology Department, Citrus Research and Education Center, University of Florida, Lake Alfred, FL 33850, USA
Lukasz L. Stelinski*
Affiliation:
Entomology and Nematology Department, Citrus Research and Education Center, University of Florida, Lake Alfred, FL 33850, USA
*
*Author for correspondence Phone: +1 863 956 8851 Fax: +1 863 956 4631 E-mail: stelinski@ufl.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

β-Aminobutyric acid (BABA) is known to induce resistance to microbial pathogens, nematodes and insects in several host plant/pest systems. The present study was undertaken to determine whether a similar effect of BABA occurred against the Asian citrus psyllid, Diaphorina citri Kuwayama, in citrus. A 25 mM drench application of BABA significantly reduced the number of eggs/plant as compared with a water control, whereas 200 and 100 mM applications of BABA reduced the numbers of nymphs/plant and adults/plants, respectively. A 5 mM foliar application of BABA significantly reduced the number of adults but not eggs or nymphs when compared with a water control treatment. In addition, leaf-dip bioassays using various concentrations (25–500 mM) of BABA indicated no direct toxic effect on 2nd and 5th instar nymphs or adult D. citri. BABA-treated plants were characterized by significantly lower levels of iron, magnesium, phosphorus, sodium, sulfur and zinc as compared with control plants. The expression level of the PR-2 gene (β-1,3-glucanase) in BABA-treated plants that were also damaged by D. citri adult feeding was significantly higher than in plants exposed to BABA, D. citri feeding alone or control plants. Our results indicate the potential for using BABA as a systemic acquired resistance management tool for D. citri.

Keywords

BABAcitrus greeninggene expressionimidaclopridinduced resistancepathogenesis-related proteinsPR-2 genesystemic acquired resistance
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 103 , Issue 5 , October 2013 , pp. 592 - 600
Copyright
Copyright © Cambridge University Press 2013 

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

Beanland, L., Phelan, P.L. & Salminen, S. (2003) Micronutrient interactions on soybean growth and the developmental performance of three insect herbivores. Environmental Entomology 32, 641–651.CrossRefGoogle Scholar
Clancy, K.M. & King, R.M. (1993) Defining the western spruce budworm's nutritional niche with response surface methodology. Ecology 74, 442–454.CrossRefGoogle Scholar
Clancy, K.M., Wagner, M.R. & Tinus, R.W. (1988) Variation in host foliage nutrient concentrations in relation to western spruce budworm herbivory. Canadian Journal of Forest Research 18, 530–539.Google Scholar
Cohen, Y. (1994) 3-Aminobutyric acid induces systemic resistance against Peronospora tabacina. Physiological and Molecular Plant Pathology 44, 273–288.Google Scholar
Cohen, Y. (2002) β-Aminobutyric acid-induced resistance against plant pathogens. Plant Disease 86, 448–457.Google Scholar
Cohen, Y. & Gisi, U. (1994) Systemic translocation of 14C-dl-3-aminobutyric acid in tomato plants in relation to induced resistance against Phytophthora infestans. Physiological and Molecular Plant Pathology 45, 441–456.Google Scholar
Cohen, Y., Niderman, T., Mösinger, E. & Fluhr, R. (1994) β-Aminobutyric acid induces the accumulation of pathogenesis-related proteins in tomato (Lycopersicon esculentum L.) plants and resistance to late blight infection caused by Phytophthora infestans. Plant Physiology 104, 59–66.Google Scholar
Cohen, Y., Reuveni, M. & Baider, A. (1999) Local and systemic activity of BABA (DL-3-aminobutyric acid) against Plasmopara viticola in grapevines. European Journal of Plant Pathology 105, 351–361.Google Scholar
Cohen, Y., Rubin, A.E. & Kilfin, G. (2010) Mechanisms of induced resistance in lettuce against Bremia lactucae by DL-β-amino-butyric acid (BABA). European Journal of Plant Pathology 126, 553–573.Google Scholar
Cohen, Y., Rubin, A.E. & Vaknin, M. (2011) Post infection application of DL-β-amino-butyric acid (BABA) induces multiple forms of resistance against Bremia lactucae. European Journal of Plant Pathology 130, 13–27.Google Scholar
Dicke, M. & Hilker, M. (2003) Induced plant defenses: from molecular biology to evolutionary ecology. Basic and Applied Ecology 4, 3–14.Google Scholar
Edreva, A. (2004) A novel strategy for plant protection: induced resistance. Journal of Cell and Molecular Biology 3, 61–69.Google Scholar
Francis, M.I., Redondo, A., Burns, J.K. & Graham, J.H. (2009) Soil application of imidacloprid and related SAR-inducing compounds produces effective and persistent control of citrus canker. European Journal of Plant Pathology 124, 283–292.Google Scholar
Garnier, M., Danel, N. & Bové, J.M. (1984) The organism is a gram-negative bacterium. pp. 115–124in Garnsey, S.M., Timmer, L.W. & Dodds, J.A. (Eds) Proceedings of 9th Conference of the International Organization of Citrus Virologist. Riverside, University of California.Google Scholar
Halbert, S.E. & Manjunath, K.L. (2004) Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature review and assessment of risk in Florida. Florida Entomologist 87, 330–353.Google Scholar
Hamiduzzaman, M.Md., Jakab, G., Barnavon, L., Neuhaus, J-M. & Mauch-Mani, B. (2005) β-Aminobutyric acid-induced resistance against downy mildew in grapevine acts through the potentiation of callose formation and jasmonic acid signaling. Molecular Plant–Microbe Interactions 18, 819–829.Google Scholar
Hodge, S., Thompson, G.A. & Powell, G. (2005) Application of DL-β-aminobutyric acid (BABA) as a root drench to legumes inhibits the growth and reproduction of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphididae). Bulletin of Entomological Research 95, 449–455.CrossRefGoogle ScholarPubMed
Hodge, S., Pope, T.W., Holaschke, M. & Powell, G. (2006) The effect of β-aminobutyric acid on the growth of herbivorous insects feeding on brassicaceae. Annals of Applied Biology 148, 223–229.Google Scholar
Huang, T., Jander, G. & de Vos, M. (2011) Non-protein amino acids in plant defense against insect herbivores: representative cases and opportunities for further functional analysis. Phytochemistry 72, 1531–1537.Google Scholar
Hwang, B.K., Sunwoo, J.Y., Kim, Y.J. & Kim, B.S. (1997) Accumulation of β-1,3-glucanase and chitinase isoforms, and salicylic acid in the DL-β-amino-n-butyric acid-induced resistance response of pepper stems to Phytophthora capsici. Physiological and Molecular Plant Pathology 51, 305–322.Google Scholar
Jagoueix, S., Bové, J.M. & Garnier, M. (1996) PCR detection of the two Candidatus liberibacter species associated with greening disease of citrus. Molecular and Cellular Probes 10, 43–50.Google Scholar
Jakab, G., Cottier, V., Toquin, V., Rigoli, G., Zimmerli, L., Métraux, J.-P. & Mauch-Mani, B. (2001) β-aminobutyric acid-induced resistance in plants. European Journal of Plant Pathology 107, 29–37.Google Scholar
Kessler, A. & Baldwin, I.T. (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annual Review of Plant Biology 53, 299–328.Google Scholar
Li, W.B., Hartung, J.S. & Levy, L. (2006) Quantitative real-time PCR for detection and identification of Candidatus Liberibacter species associated with citrus huanglongbing. Journal of Microbiological Methods 66, 104–115.Google Scholar
Liu, T., Jiang, X., Shi, W., Chen, J., Pei, Z. & Zheng, H. (2011) Comparative proteomic analysis of differentially expressed proteins in β-aminobutyric acid enhanced Arabidopsis thaliana tolerance to simulated acid rain. Proteomics 11, 2079–2094.Google Scholar
Livak, K.J. & Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.Google Scholar
Mann, R.S., Ali, J.G., Hermann, S.L., Tiwari, S., Pelz-Stelinski, K.S., Alborn, H.S. & Stelinski, L.L. (2012) Induced release of a plant-defense volatile ‘Deceptively’ attracts insect vectors to plants infected with a bacterial pathogen. PLoS Pathogens 8, e1002610. doi:10.1371/journal.ppat.1002610.Google Scholar
Marcucci, E., Aleandri, M.P., Chilosi, G. & Magro, P. (2010) Induced resistance by β-aminobutyric acid in artichoke against white mould caused by Sclerotinia sclerotiorum. Journal of Phytopathology 158, 659–667.Google Scholar
Moran, P.J. & Thompson, G.A. (2001) Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiology 125, 1074–1085.CrossRefGoogle ScholarPubMed
Oka, Y. & Cohen, Y. (2001) Induced resistance to cyst and root-knot nematodes in cereals by DL-beta-amino-N-butyric acid. European Journal of Plant Pathology 107, 219–227.Google Scholar
Pozo, M.J., Van Loon, L.C. & Pieterse, C.M.J. (2004) Jasmonates – signals in plant–microbe interactions. Journal of Plant Growth Regulation 23, 211–222.Google Scholar
Prabhaker, N., Castle, S.J., Byrne, F.J., Henneberry, T.J. & Toscano, N.C. (2006) Establishment of baseline susceptibility data to various insecticides for glassy-winged sharpshooter, Homalodisca coagulata Say (Homoptera: Cicadellidae) by comparative bioassay techniques. Journal of Economic Entomology 99, 141–154.CrossRefGoogle Scholar
SAS Institute (2004) SAS Users Guide. SAS Institute, Cary, NC.Google Scholar
Siegrist, J., Orober, M. & Buchenauer, H. (2000) β-Aminobutyric acid-mediated enhancement of resistance in tobacco to tobacco mosaic virus depends on the accumulation of salicylic acid. Physiological and Molecular Plant Pathology 56, 95–106.Google Scholar
Silue, D., Pajot, E. & Cohen, Y. (2002) Induction of resistance to downy mildew (Peronospora parasitica) in cauliflower by DL-β-amino-n-butanoic acid (BABA). Plant Pathology 51, 97–102.Google Scholar
Slaughter, A.R., Hamiduzzaman, M.Md., Gindro, K., Neuhaus, J.-M. & Mauch-Mani, B. (2008) Beta-aminobutyric acid-induced resistance in grapevine against downy mildew: involvement of pterostilbene. European Journal of Plant Pathology 122, 185–195.Google Scholar
Steiner, U. & Schönbeck, F. (1997) Induced resistance. pp. 272–297in Hartleb, H., Heitefuss, R. & Hopp, H.H. (Eds) Resistance of Crop Plants Against Fungi. Lubeck, Ulm, Gustav Fischer, Jena, Stuttgart.Google Scholar
Tiwari, S., Lewis-Rosenblum, H., Pelz-Stelinski, K. & Stelinski, L.L. (2010) Incidence of Candidatus Liberibacter asiaticus infection in abandoned citrus occurring in proximity to commercially managed groves. Journal of Economic Entomology 103, 1972–1978.Google Scholar
Tiwari, S., Mann, R.S., Rogers, M.E. & Stelinski, L.L. (2011a) Insecticide resistance in field populations of Asian citrus psyllid in Florida. Pest Management Science 67, 1258–1268.Google Scholar
Tiwari, S., Pelz-Stelinski, K. & Stelinski, L.L. (2011b) Effect of Candidatus Liberibacter asiaticus infection on susceptibility of Asian citrus psyllid, Diaphorina citri, to selected insecticides. Pest Management Science 67, 94–99.Google Scholar
Tiwari, S., Gondhalekar, A.D., Mann, R.S., Scharf, M.E. & Stelinski, L.L. (2011c) Characterization of five CYP4 genes from Asian citrus psyllid and their expression levels in Candidatus Liberibacter asiaticus infected and uninfected psyllids. Insect Molecular Biology 20, 733–744.Google Scholar
Tiwari, S., Stelinski, L.L. & Rogers, M.E. (2012a) Biochemical basis of organophosphate and carbamate resistance in Asian citrus psyllid. Journal of Economic Entomology 105, 540–548.CrossRefGoogle ScholarPubMed
Tiwari, S., Clayson, P.J., Kuhns, E.H. & Stelinski, L.L. (2012b) Effect of buprofezin and diflubenzuron on various developmental stages of Asian citrus psyllid, Diaphorina citri. Pest Management Science 68, 1405–1412.Google Scholar
Ton, J., Jakab, G., Toquin, V., Flors, V., Lavicoli, A., Maeder, M.N., Metraux, J.-P. & Mauch-Mani, B. (2005) Dissecting the b-aminobutyric acid-induced priming phenomenon in Arabidopsis. Plant Cell 17, 987–999.CrossRefGoogle Scholar
van der Ent, S., Koornneef, A., Jurriaan, T. & Pieterse, C.M.J. (2009) Induced resistance – orchestrating defence mechanisms through crosstalk and priming. Annual Plant Reviews 34, 334–370.Google Scholar
Zhang, S., Reddy, M.S., Kokalis-Burelle, N., Wells, L.W., Nightengale, S.P. & Kloepper, J.W. (2001) Lack of induced systemic resistance in peanut to late leaf spot disease by plant growth-promoting rhizobacteria and chemical elicitors. Plant Disease 85, 879–884.Google Scholar
Zimmerli, L., Jakab, G., Métraux, J.P. & Mauch-Mani, B. (2000) Potentiation of pathogen-specific defense mechanisms in Arabidopsis by β-aminobutyric acid. Proceedings of the National Academy of Sciences U.S.A. 97, 12920–12925.CrossRefGoogle ScholarPubMed
Zimmerli, L., Métraux, J.P. & Mauch-Mani, B. (2001) Beta-aminobutyric acid-induced protection of Arabidopsis against necrotrophic fungus Botrytis cinerea. Plant Physiology 126, 517–523.Google Scholar