Australasian Plant Pathology

, Volume 46, Issue 3, pp 239–249 | Cite as

β– amino butyric acid mediated changes in cellular redox homeostasis confers tomato resistance to early blight

  • P. Roylawar
  • A. KambleEmail author
Original Paper


Foliar application of β-aminobutyric acid (BABA) restricted the colonization of Alternaria solani in tomato leaves. The activities of antioxidative enzymes were studied in defence response to oxidative stress generated upon A. solani infection. At 1 dpi (days post inoculation) and 2 dpi, these defence responses are found to be prominent in BABA- primed plants as compared to untreated plants after A. solani infection. Elevated antioxidant enzyme capacity in BABA- primed plants was coupled with less lipid peroxidation. Generation of superoxide radical (O2 ._) and hydrogen peroxide (H2O2) was efficiently modulated in BABA- primed plants in response to pathogen inoculation suggesting there role in restricting fungal growth whereas, in BABA untreated plants increased accumulation of H2O2 at late stage of infection (36 and 48 h post inoculation) resulted in failed defence response. A positive correlation was observed in levels O2 ._, H2O2, and SOD activity. In addition, the activity of phenylalanine ammonia-lyase (PAL) and deposition of callose was studied as a biochemical marker of induced resistance and marker for PAMP-triggered immunity respectively. BABA- primed plants showed an elevated PAL activity over untreated infected plants at all studied time points (1, 2, 3, 5 dpi). Contradictory to previous studies, we found that in BABA- primed plants level of callose deposition is not as much of untreated plants upon A. solani infection. Overall the results indicate that BABA priming triggers changes in oxidative status suitable for the expression of resistance against A. solani.


Induced resistance Priming Antioxidant Callose ß- aminobutyric acid Early blight 



The study was supported by a grant from BCUD, Savitribai Phule Pune University, Pune, India. PR is thankful to UGC, India for the award of RGNF-UGC Fellowship.


  1. Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Biol 53:1331–1341Google Scholar
  2. Bacic A, Fincher GB, Stone BA (2009) Chemistry, biochemistry and biology of (1→3)-β-glucans and related polysaccharides. Academic Press, AmsterdamGoogle Scholar
  3. Baysal O, Gursoy Y, Ornek H, Duru A (2005) Induction of oxidants in tomato leaves treated with DL-β-aminobutyric acid (BABA) and infected with Clavibacter michiganensis ssp. michiganensis. Eur J Plant Pathol 112:361–369CrossRefGoogle Scholar
  4. Bestwick C, Brown I, Mansfield J (1998) Localised changes in peroxidase activity accompany hydrogen peroxide generation during the development of a non-host hypersensitive reaction in lettuce. Plant Physiol 118:1067–1078CrossRefPubMedPubMedCentralGoogle Scholar
  5. Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287CrossRefPubMedGoogle Scholar
  6. Borges A, Sandalio L (2015) Induced resistance for plant defence. Front Plant Sci 6:109CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bournonville CF, Grellet D-R, Juan C (2011) Quantitative determination of superoxide in plant leaves using a modified NBT staining method. Phytochem Anal 22(3):268–271CrossRefPubMedGoogle Scholar
  8. Chavan V, Bhargava S, Kamble A (2013) Temporal modulation of oxidant and antioxidative responses in Brassica carinata during b-aminobutyric acid-induced resistance against Alternaria brassicae. Physiol Mol Plant Pathol 83:35–39CrossRefGoogle Scholar
  9. Cohen Y, Rubin AE, Vaknin M (2011) Post infection application of DL-3-amino-butyric acid (BABA) induces multiple forms of resistance against Bremia lactucae in lettuce. Eur J Plant Pathol 130:13–27CrossRefGoogle Scholar
  10. Dat JF, Pellinen R, Beeckman T, Kangasjarvi J, Langebartels C, Inze D, Van Breusegem F (2003) Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco. Plant J 33:621–632CrossRefPubMedGoogle Scholar
  11. Debona D, Rodrigues FÁ, Rios JA, Nascimento KJT (2012) Biochemical changes in the leaves of wheat plants infected by Pyricularia oryzae. Phytopathology 102:1121–1129CrossRefPubMedGoogle Scholar
  12. De Gara L, De Pinto M, Tommasi F (2003) The antioxidant system vis-a-vis reactive oxygen species during plant-pathogen interaction. Plant Physiol Biochem 41:863–870CrossRefGoogle Scholar
  13. Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7(7):1085–1097CrossRefPubMedPubMedCentralGoogle Scholar
  14. Doke Y, Wum Y, Sanchez LM, Pk HJ, Ncritke H, Yoshioka H, Krvata K (1996) The oxidative bust protects plants against pathogen attack: mechanism and role as an emergency signal for plant bio-defence - a review. Gene 179:45–51CrossRefPubMedGoogle Scholar
  15. Emelianov VI, Kravchuk ZN, Poliakovskiĭ SA, Dmitriev AP (2008) Callose accumulation during treatment of tomato (Lycopersicon esculentum L.) cells with biotic elicitors. Cytol Genet 42:21–28Google Scholar
  16. Flors V, Leyva MO, Vicedo B, Finiti I, Real MD, García-Agustín P, Bennett AB, González-Bosch C (2007) Absence of the endo-β-1,4-glucanases Cel1 and Cel2 reduces susceptibility to in tomato. Plant J 52 (6):1027–1040Google Scholar
  17. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefPubMedGoogle Scholar
  18. Halliwell B (2006) Reactive species and antioxidants: redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hann DR, Rathjen JP (2007) Early events in the pathogenicity of Pseudomonas syringae on Nicotiana benthamiana. Plant J 49:607–618CrossRefPubMedGoogle Scholar
  20. Heath R, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefPubMedGoogle Scholar
  21. Kamble A, Bhargava S (2007) B-aminobutyric acid- induced resistance in Brassica juncea against the necrotrophic pathogen Alternaria brassicae. J Phytopathol 155:152–158CrossRefGoogle Scholar
  22. Khan N, Vaidyanathan C (1986) A new simple spectrophotometric assay of phenylalanine ammonia-lyase. Curr Sci 55:391–393Google Scholar
  23. Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275CrossRefPubMedGoogle Scholar
  24. Luna E, Pastor V, Robert J, Flors V, Mauch-Mani B, Ton J (2011) Callose deposition: a multifaceted plant defense response. Mol Plant Microbe 24:183–193CrossRefGoogle Scholar
  25. Malolepsza U, Rozalska S (2005) Nitric oxide and hydrogen peroxide in tomato resistance. Nitric oxide modulates hydrogen peroxide level in o-hydroxyethylorutin- induced resistance to Botrytis cinerea in tomato. Plant Physiol Biochem 43:623–635CrossRefPubMedGoogle Scholar
  26. Mittler R, Herr EH, Orvar BL, vanCamp W, Willekens H, Inzé D, Ellis BE (1999) Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyper responsive to pathogen infection. Proc Natl Acad Sci U S A 96:14165–14170CrossRefPubMedPubMedCentralGoogle Scholar
  27. Nagy NE, Fossdal CG, Dalen LS, Lönneborg A, Heldal I, Johnsen O (2004) Effects of Rhizoctonia infection and drought on peroxidase and chitinase activity in Norway spruce (Picea abies). Plant Physiol 120:465–473CrossRefGoogle Scholar
  28. Nakano Y, Assada K (1981) Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  29. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–729CrossRefPubMedGoogle Scholar
  30. Passardi F, Penel C, Dunand C (2004) Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci 9:534–540CrossRefPubMedGoogle Scholar
  31. Pandey KK, Pandey PK, Kallo G, Banerjee MK (2003) Resistance to early blight of tomato with respect to various parameters of disease epidemics. J Gen Plant Pathol 69:364–371CrossRefGoogle Scholar
  32. Patykowski J, Urbanek H (2003) Activity of enzymes related to H2O2 generation and metabolism in leaf apoplastic fraction of tomato leaves infected with Botrytis cinerea. J Phytopathol 151:153–161CrossRefGoogle Scholar
  33. Pina A, Errea P (2008) Differential induction of phenylalanine ammonia-lyase gene expression in response to in vitro callus unions of Prunus spp. J Plant Physiol 165:705–714CrossRefPubMedGoogle Scholar
  34. Reimers PJ, Leach JE (1991) Race-specific resistance to Xanthomonas oryzae pv. oryzae conferred by bacterial blight resistance gene Xa-10 in rice (Oryza sativa) involves accumulation of a lignin-like substance in host tissues. Physiol Mol Plant Pathol 38:39–55CrossRefGoogle Scholar
  35. Romero D, Rivera ME, Cazorla FM, Codina JC, Fernández-Ortuño D, Torés JA (2008) Comparative histochemical analyses of oxidative burst and cell wall reinforcement in compatible and incompatible melon-powdery mildew (Podosphaera fusca) interactions. J Plant Physiol 165:1895–1905CrossRefPubMedGoogle Scholar
  36. Sairam RK, Srivastava GC (2000) Induction of oxidative stress and antioxidant activity by hydrogen peroxide treatment in tolerant and susceptible wheat genotypes. Biol Plant 43:381–386CrossRefGoogle Scholar
  37. Siegrist J, Orober M, Buchenauer H (2000) B-aminobutyric acid- mediated enhancement of resistance in tobacco to tobacco mosaic virus depends on the accumulation of salicylic acid. Physiol Mol Plant Pathol 56:95–106CrossRefGoogle Scholar
  38. Slaughter AR, Hamiduzzaman MM, Gindro K, Neuhaus JM, Mauch-Mani B (2008) Beta-aminobutyric acid-induced resistance in grapevine against downy mildew: involvement of pterostilbene. Eur J Plant Pathol 122:185–195CrossRefGoogle Scholar
  39. Srivastava S, Dubey RS (2011) Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings. Plant Growth Regul 64:1–16CrossRefGoogle Scholar
  40. Tian S, Qin G, Li B (2013) Reactive oxygen species involved in regulating fruit senescence and fungal pathogenicity. Plant Mol Biol 82:593–602CrossRefPubMedGoogle Scholar
  41. Ton J, Mauch-Mani B (2004) β-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J 38:119–130CrossRefPubMedGoogle Scholar
  42. Ton J, Jakab G, Toquin V, Flors V, Iavicoli A, Maeder MN et al (2005) Dissecting the beta-aminobutyric acid-induced priming phenomenon in Arabidopsis. Plant Cell 17:987–999CrossRefPubMedPubMedCentralGoogle Scholar
  43. Van Breusegem F, Vranova E, Dat JF, Inze D (2001) The role of active oxygen species in plant signal transduction. Plant Sci 161:405–414CrossRefGoogle Scholar
  44. Vanitha SC, Niranjana SR, Mortensen CN, Umesha S (2009) Bacterial wilt of tomato in Karnataka and its management by Pseudomonas fluorescens. BioControl 54 (5):685–695Google Scholar
  45. Velikova V, Yordanov I, Edereva A (2000) Oxidative stress and some antioxidant systems in acid rain- treated bean plants. Protective role of exogenous polyamines. Plant Sci 151:59–66CrossRefGoogle Scholar
  46. Volk S, Feierabend J (1989) Photoinactivation of catalase at low temperature and its relevance to photosynthetic and peroxide metabolism in leaves. Plant Cell Environ 12:701–712CrossRefGoogle Scholar
  47. Walters D, Ratsep J, Havis N (2014) Controlling crop diseases using induced resistance: challenges for the future. J Exp Bot 64:1263–1280CrossRefGoogle Scholar
  48. Xu HW, Lu Y, Tong SY, Song FB (2011) Lipid peroxidation, antioxidant enzyme activity and osmotic adjustment changes in husk leaves of maize in black soils region of Northeast China. Afr J Agric Res 6:3098–3102Google Scholar
  49. Zeier J, Delledonne M, Mishina T, Severi E, Sonoda M, Chris L (2004) Genetic elucidation of nitric oxide signaling in incompatible plant-pathogen interaction. Plant Physiol 136:2875–2886CrossRefPubMedPubMedCentralGoogle Scholar
  50. Zhong Y, Wang B, Yan J, Cheng L, Yao L, Xiao L, Wu T (2014) DL-β-aminobutyric acid-induced resistance in soybean against Aphis glycines Matsumura (Hemiptera: Aphididae). PLoS One 9:e85Google Scholar

Copyright information

© Australasian Plant Pathology Society Inc. 2017

Authors and Affiliations

  1. 1.Department of BotanySavitribai Phule Pune UniversityPuneIndia

Personalised recommendations