Skip to main content
Springer Nature Link
Log in

Post infection application of DL-3-amino-butyric acid (BABA) induces multiple forms of resistance against Bremia lactucae in lettuce

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

DL-3-amino-butyric acid (BABA) induces local and systemic resistance against disease in numerous plant species. In a recent study we showed that preventive application of BABA to lettuce (Lactuca sativa) plants induced resistance against downy mildew caused by the oomycete Bremia lactucae by callose encasement of the primary infection structures of the pathogen. Now we show that post-infection application of BABA to the foliage or the roots, even at progressive stages of disease development, is highly protective against B. lactucae. Resistance induced by BABA is manifested in multiple microscopic forms, depending on the time of its application. When applied at 1 day post inoculation (dpi) BABA induced HR in penetrated epidermal cells; at 2 dpi it caused massive encasement with callose of the primary haustoria; and, at 3 or 4 dpi it enhanced the accumulation of H2O2 in the developing mycelia runners and altered their colour to red. The pronounced change in the colour of the mycelium was visually apparent to the naked eye. In all cases the pathogen failed to sporulate on the treated plants. This is the first indication that an immunizing compound may be protective at advanced stages of disease development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

Abbreviations

ABA:

Abscisic acid

DAB:

Diaminobenzidine

dpi:

Days post inoculation

JA:

Jasmonic acid

NaSA:

Sodium salicylate

ROS:

Reactive oxygen species

PR-1:

Pathogenesis-related protein 1

SA:

Salicylic acid

SAR:

Systemic acquired resistance

References

  • Amzalek, E., & Cohen, Y. (2007). Comparative efficacy of systemic acquired resistance-inducing compounds against rust infection in sunflower plants. Phytopathology, 97, 179–186.

    Article  PubMed  CAS  Google Scholar 

  • Baider, A., & Cohen, Y. (2003). Synergistic interaction between BABA and mancozeb in controlling Phytophthora infestans in potato and tomato and Pseudoperonospora cubensis in cucumber. Phytoparasitica, 31, 399–409.

    Article  CAS  Google Scholar 

  • Baysal, O., Ziya Gursoy, Y., Ornek, H., & Duru, A. (2005). Induction of oxidants in tomato leaves with DL-β-aminobutyric acid (BABA) and infected with Clavibacter michiganensis subp. michiganensis. European Journal of Plant Pathology, 112, 361–369.

    Article  CAS  Google Scholar 

  • Baysal, O., Gursoy, Y. Z., Ornek, H., Cetinel, B., & Da Silva, J. A. T. (2007). Enhanced systemic resistance to bacterial speck disease caused by Pseudomonas syringae pv. tomato by DL-β-aminobutyric acid under salt stress. Physiologia Plantarum, 129, 493–506.

    Article  CAS  Google Scholar 

  • Biton, R., Baider, A., Ovadia, A., Cohen, Y., & Porter, I. J. (2001). Induced resistance against Fusarium oxysporum f. sp. melonis in melon plants in response to β-aminobutyric acid. In Proc. 2nd Aust. Soilborne Dis. Symp., 71–72.

  • Cohen, Y. (1994). 3-aminobutyric acid induces systemic resistance against Peronospora tabacina. Physiological and Molecular Plant Pathology, 44, 273–288.

    Article  CAS  Google Scholar 

  • Cohen, Y. (2002). β-aminobutyric acid-induced resistance against plant pathogens. Plant Disease, 86, 448–457.

    Article  CAS  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.

    Article  CAS  Google Scholar 

  • Cohen, Y., & Ibrahim, R. L. (1975). Changes in phenolic compounds in sunflower infected by Plasmopara halstedii. Canadian Journal of Botany, 53, 2625–2630.

    Article  CAS  Google Scholar 

  • Cohen, Y., Reuveni, M., & Eyal, H. (1979). The systemic antifungal activity of Ridomil against Phytophthora infestans on tomato plants. Phytopathology, 69, 645–649.

    Article  CAS  Google Scholar 

  • Cohen, Y., Eyal, H., Hanania, J., & Malik, Z. (1989). Ultrastructure of Pseudoperonospora cubensis in muskmelon genotype susceptible and resistant to downy mildew. Physiological and Molecular Plant Pathology, 34, 27–40.

    Article  Google Scholar 

  • Cohen, Y., Eyal, H., & Hanania, J. (1990). Ultrastructure, autofluorescence, callose deposition and lignification in susceptible and resistant muskmelon leaves infected with the powdery mildew fungus Sphaerotheca fuliginea. Physiological and Molecular Plant Pathology, 36, 191–204.

    Article  CAS  Google Scholar 

  • Cohen, Y., Baider, A., Gotlieb, D., & Rubin, A. E. (2007). Control of Bremia lactucae in field-grown lettuce by DL-3-amino-n-butanoic acid (BABA). In U. Niggli, C. Leifert, T. Alfoldi, L. Luck, & H. Willer (Eds.), Improving sustainability in organic and low input food production systems. University of Hohenheim, Germany: Proc. 3rd Intn. Cong. European integrated project ‘Quality Low Input Food’ (QLIF).

  • Cohen, Y., Rubin, A., & Gotlieb, D. (2008). Activity of carboxylic acid amide (CAA) fungicides against Bremia lactucae. European Journal of Plant Pathology, 122, 169–183.

    Article  CAS  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.

    Article  CAS  Google Scholar 

  • Conrath, U., Pieterse, C. M. J., & Mauch-Mani, B. (2002). Priming in plant-pathogen interactions. Trends in Plant Science, 7, 210–216.

    Article  PubMed  CAS  Google Scholar 

  • Conrath, U., Beckers, G. J., Flors, V., Garcia-Agustin, P., Jakab, G., Mauch, F., et al. (2006). Priming: getting ready for battle. Molecular Plant-Microbe Interactions, 19, 1062–1071.

    Article  PubMed  CAS  Google Scholar 

  • Crute, I. R., Gordon, P. I., Moss, N. A., Heaney, S., Slawson, D., Hollomon, D. W., et al. 1994. Variation for responses to phenylamides in UK populations of Bremia lactucae (lettuce downy mildew) and Peronospora parasitica (Brassica downy mildew). In British Crop Protection Council Monograph No 60. 155–162.

  • Goellner, K., & Conrath, U. (2008). Priming: it’s all the world to induced disease resistance. European Journal of Plant Pathology, 121, 233–242.

    Article  Google Scholar 

  • Hamiduzzaman, M. M., Jakab, G., Barnavon, L., Neuhaus, J. M., & Mauch-Mani, B. (2005). Beta-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.

    Article  PubMed  CAS  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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Hwang, B. K., Sunwoo, J. Y., Kim, Y. J., & Kim, B. S. (1997). Accumulation of beta-1, 3-glucanase and chitinase isoforms, and salicylic acid in the DL-beta-amino-n-butyric acid-induced resistance response of pepper stems to Phytophthora capsici. Physiological and Molecular Plant Pathology, 51, 305–322.

    Article  CAS  Google Scholar 

  • Jakab, G., Cottier, V., Toquin, V., Rigoli, G., Zimmerli, L., Metraux, J. P., et al. (2001). β-aminobutyric acid-induced resistance in plants. European Journal of Plant Pathology, 107, 29–37.

    Article  CAS  Google Scholar 

  • Jakab, G., Ton, J., Flors, V., Zimmerli, L., Metraux, J. P., & Mauch-Mani, B. (2005). Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiology, 139, 267–274.

    Article  PubMed  CAS  Google Scholar 

  • Kim, J., Kyung, D., Yun, H., Cho, B. K., Seo, J. H., Cha, M., et al. (2007). Cloning and characterization of a novel beta-transaminase from Mesorhizobium sp Strain LUK: a new biocatalyst for the synthesis of enantiomerically pure β-amino acids. Applied and Environmental Microbiology, 73, 1772–1782.

    Article  PubMed  CAS  Google Scholar 

  • Kuc, J. (2001). Concepts and direction of induced systemic resistance in plants and its application. European Journal of Plant Pathology, 107, 7–12.

    Article  Google Scholar 

  • Lebeda, A., Sedlarova, M., Petrivalsky, M., & Prokopova, J. (2008). Diversity of defence mechanisms in plant-oomycete interactions: a case study of Lactuca spp. and Bremia lactucae. European Journal of Plant Pathology, 122, 71–89.

    Article  Google Scholar 

  • Oka, Y., & Cohen, Y. (2001). Induced resistance to cyst and root-knot nematodes in cereals by DL-β-amino-n-butyric acid. European Journal of Plant Pathology, 107, 219–227.

    Article  CAS  Google Scholar 

  • Oka, Y., Cohen, Y., & Spiegel, Y. (1999). Local and systemic induced resistance to the root-knot nematode in tomato by DL-β-amino-n-butyric acid. Phytopathology, 89, 1138–1143.

    Article  PubMed  CAS  Google Scholar 

  • Papavizas, G. C., & Davey, C. B. (1963). Effect of amino compounds and related substances lacking sulfur on Aphanomyces root rot of peas. Phytopathology, 53, 116–122.

    CAS  Google Scholar 

  • Porat, R., Vinokur, V., Weiss, B., Cohen, L., Daus, A., Goldschmidt, E. E., et al. (2003). Induction of resistance to Penicillium digitatum in grapefruit by β-aminobutyric acid. European Journal of Plant Pathology, 109, 901–907.

    Article  CAS  Google Scholar 

  • Reuveni, M., Zahavi, T., & Cohen, Y. (2001). Controlling downy mildew (Plasmopara viticola) in field-grown grapevine with β-aminobutyric acid (BABA). Phytoparasitica, 29, 125–133.

    Article  CAS  Google Scholar 

  • Reuveni, M., Sheglov, D., & Cohen, Y. (2003). Control of moldy-core decay in apple fruits by beta-aminobutyric acids and potassium phosphites. Plant Disease, 87, 933–936.

    Article  CAS  Google Scholar 

  • Schornack, S., Huitema, E., Cano, L. M., Bozkurt, T. O., Oliva, R., Van Damme, M., et al. (2009). Ten things to know about oomycete effectors. Molecular Plant Pathology, 10, 795–803.

    Article  PubMed  CAS  Google Scholar 

  • Shailasree, S., Sarosh, B. R., Vasanthi, N. S., & Shetty, H. S. (2001). Seed treatment with beta-aminobutyric acid protects Pennisetum glaucum systemically from Sclerospora graminicola. Pest Management Science, 57, 721–728.

    Article  PubMed  CAS  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.

    Article  CAS  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.

    Article  CAS  Google Scholar 

  • Slaughter, A. R., Hamiduzzaman, M. M., Gindro, K., Neuhaus, J. M., & Mauch-Mani, B. (2008). β-aminobutyric acid-induced resistance in grapevine against downy mildew: involvement of pterostilbene. European Journal of Plant Pathology, 122, 185–195.

    Article  CAS  Google Scholar 

  • Sticher, L., Mauch-Mani, B., & Metraux, J. P. (1997). Systemic acquired resistance. Annual Review of Phytopathology, 35, 235–270.

    Article  PubMed  CAS  Google Scholar 

  • Thordal-Christensen, H., Zhang, Z. G., Wei, Y. D., & Collinge, D. B. (1997). Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. The Plant Journal, 11, 1187–1194.

    Article  CAS  Google Scholar 

  • Ton, J., & Mauch-Mani, B. (2004). β-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. The Plant Journal, 38, 119–130.

    Article  PubMed  CAS  Google Scholar 

  • Tosi, L., Luigetti, R., & Zazzerini, A. (1998). Induced resistance against Plasmopara helianthi in sunflower plants by DL-beta-amino-n-butyric acid. Journal of Phytopathology, 146, 295–299.

    Article  CAS  Google Scholar 

  • Van Der Ent, S., Van Hulten, M., Pozo, M. J., Czechowski, T., Udvardi, M. K., Pieterse, C. M. J., et al. (2009). Priming of plant innate immunity by rhizobacteria and beta-aminobutyric acid: differences and similarities in regulation. The New Phytologist, 183, 419–431.

    Article  PubMed  Google Scholar 

  • Van Loon, L. C. (1997). Induced resistance in plants and the role of pathogenesis-related proteins. European Journal of Plant Pathology, 103, 753–765.

    Article  Google Scholar 

  • Walters, D., Walsh, D., Newton, A., & Lyon, G. (2005). Induced resistance for plant disease control: maximizing the efficacy of resistance elicitors. Phytopathology, 95, 1368–1373.

    Article  PubMed  CAS  Google Scholar 

  • Walz, A., & Simon, O. (2009). β-Aminobutyric acid-induced resistance in cucumber against biotrophic and necrotrophic pathogens. Journal of Phytopathology, 157, 356–361.

    Article  CAS  Google Scholar 

  • Wu, C. C., Singh, P., Chen, M. C., & Zimmerli, L. (2009). L-Glutamine inhibits beta-aminobutyric acid-induced stress resistance and priming in Arabidopsis. Journal of Experimental Botany, 61, 995–1002.

    Article  PubMed  Google Scholar 

  • Zimmerli, L., Jakab, C., Metraux, 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 of the United States of America, 97, 12920–12925.

    Article  PubMed  CAS  Google Scholar 

  • Zimmerli, L., Metraux, J. P., & Mauch-Mani, B. (2001). β-aminobutyric acid-induced protection of Arabidopsis against the necrotrophic fungus Botrytis cinerea. Plant Physiology, 126, 517–523.

    Article  PubMed  CAS  Google Scholar 

  • Zimmerli, L., Hou, B. H., Tsai, C. H., Jakab, G., Mauch-Mani, B., & Somerville, S. (2008). The xenobiotic beta-aminobutyric acid enhances Arabidopsis thermotolerance. The Plant Journal, 53, 144–156.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. The Mina & Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan, 52900, Israel

    Yigal Cohen, Avia E. Rubin & Moshe Vaknin

Authors
  1. Yigal Cohen
    View author publications

    Search author on:PubMed Google Scholar

  2. Avia E. Rubin
    View author publications

    Search author on:PubMed Google Scholar

  3. Moshe Vaknin
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Yigal Cohen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cohen, Y., Rubin, A.E. & Vaknin, M. Post infection application of DL-3-amino-butyric acid (BABA) induces multiple forms of resistance against Bremia lactucae in lettuce. Eur J Plant Pathol 130, 13–27 (2011). https://doi.org/10.1007/s10658-010-9724-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-010-9724-8

Keywords