Sodium alginate potentiates antioxidant defense and PR proteins against early blight disease caused by Alternaria solani in Solanum lycopersicum Linn.

Autoři: Priya Dey aff001;  Ramani Ramanujam aff001;  Ganesan Venkatesan aff002;  Radhakrishnan Nagarathnam aff001
Působiště autorů: Unit of Plant Pathology, Centre for Advance Studies in Botany, University of Madras, Guindy Campus, Chennai, Tamil Nadu, India aff001;  Acme Progen Biotech (India) Pvt. Ltd, Salem, Tamil Nadu, India aff002
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223216


The use of biopolymers as elicitors in controlling plant diseases is gaining momentum world-wide due to their eco-friendly and non-toxic nature. In the present study, we have used an algal biopolymer (sodium alginate) and tested its applicability as an elicitor in inducing resistance factors against Alternaria solani, which causes early blight disease in Solanum lycopersicum (tomato plant). We have pre-treated tomato plants with different concentrations of sodium alginate (0.2%, 0.4%, and 0.6%) before A. solani infection. We found that sodium alginate has effectively controlled the growth of A. solani. In addition, a significant increase in the expression levels of SOD was observed in response to pathogen infection. The increased protease inhibitors activity further suggest that sodium alginate restrict the development of A. solani infection symptoms in tomato leaves. This corroborates well with the cell death analysis wherein increased sodium alginate pre-treatment results in decreased cell death. Also, the expression profile analyses reveal the induction of genes only in sodium alginate-pretreated tomato leaves, which are implicated in plant defense mechanism. Taken together, our results suggest that sodium alginate can be used as an elicitor to induce resistance against A. solani in tomato plants.

Klíčová slova:

Cell death – Infectious disease control – Leaves – Pathogens – Plant pathogens – Tomatoes – Lipid peroxidation – Chymotrypsin


1. Dangl JL, Jones JDG. Plant pathogens and integrated defence responses to infection. Nature. 2001;411: 826–833. doi: 10.1038/35081161 11459065

2. Durrant WE, Dong X. Systemic Acquired Resistance. Annu Rev Phytopathol. 2004;42: 185–209. doi: 10.1146/annurev.phyto.42.040803.140421 15283665

3. Liu P-P, von Dahl CC, Klessig DF. The Extent to Which Methyl Salicylate Is Required for Signaling Systemic Acquired Resistance Is Dependent on Exposure to Light after Infection. Plant Physiol. 2011;157: 2216–2226. doi: 10.1104/pp.111.187773 22021417

4. Loon VLC, Strien E. Van. The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol. 1999;55: 85–97.

5. Lehmann S, Serrano M, L’Haridon F, Tjamos SE, Metraux JP. Reactive oxygen species and plant resistance to fungal pathogens. Phytochemistry. Elsevier Ltd; 2015;112: 54–62. doi: 10.1016/j.phytochem.2014.08.027 25264341

6. Lamb C, Dixon RA. the Oxidative Burst in Plant Disease Resistance. Annu Rev Plant Physiol Plant Mol Biol. 1997;48: 251–275. doi: 10.1146/annurev.arplant.48.1.251 15012264

7. Davies KJA. Oxidative stress, antioxidant defenses, and damage removal, repair, and replacement systems. IUBMB Life. 2000;50: 279–289. doi: 10.1080/713803728 11327322

8. Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 2002;7: 405–410. doi: 10.1016/s1360-1385(02)02312-9 12234732

9. Alscher RG, Erturk N, Heath LS. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot. 2002;53: 1331–1341. 11997379

10. Zhao H, Sun X, Xue M, Zhang X, Li Q. Antioxidant enzyme responses induced by whiteflies in tobacco plants in defense against aphids: Catalase may play a dominant role. PLoS One. 2016; 1–17. doi: 10.1371/journal.pone.0165454 27788203

11. Tayefi-Nasrabadi H, Dehghan G, Daeihassani B, Movafegi A, Samadi A. Some biochemical properties of guaiacol peroxidases as modified by salt stress in leaves of salt-tolerant and salt-sensitive safflower (Carthamus tinctorius cultivars. African J Biotechnol. 2011;10: 751–763. doi: 10.5897/AJB10.1465

12. Bowler C, Camp W Van, Montagu M Van, Inzé D. Superoxide Dismutase in Plants. CRC Crit Rev Plant Sci. 1994;13: 199–218. doi: 10.1080/07352689409701914

13. Thakur M, Sohal BS. Role of Elicitors in Inducing Resistance in Plants against Pathogen Infection: A Review. ISRN Biochem. 2013;2013: 1–10. doi: 10.1155/2013/762412 25969762

14. Wiesel L, Newton AC, Elliott I, Booty D, Gilroy EM, Birch PRJ, et al. Molecular effects of resistance elicitors from biological origin and their potential for crop protection. Front Plant Sci. 2014;5: 1–13. doi: 10.3389/fpls.2014.00655 25484886

15. Conrath U. Systemic Acquired Resistance. Plant Signal Behav. 2006;1: 179–184. doi: 10.4161/psb.1.4.3221 19521483

16. Regassa D, Tigre W, Shiferaw A. Tomato (Lycopersicon esculentum Mill.) varieties evaluation in Borana zone, Yabello district, southern Ethiopia. J Plant Breed Crop Sci. 2016;8: 206–210. doi: 10.5897/JPBCS2015.0543

17. Barone A, Chiusano ML, Ercolano MR, Giuliano G, Grandillo S, Frusciante L. Structural and functional genomics of tomato. Int J Plant Genomics. 2008;2008: 1–12. doi: 10.1155/2008/820274 18317508

18. Adhikari P, Oh Y, Panthee DR. Current Status of Early Blight Resistance in Tomato: An Update. Int J Mol Sci. 2017; 1–22. doi: 10.3390/ijms18102019 28934121

19. Trouvelot S, Héloir M, Poinssot B, Gauthier A, Paris F, Guillier C, et al. Carbohydrates in plant immunity and plant protection: roles and potential application as foliar sprays. Front Plant Sci. 2014;5: 1–14. doi: 10.3389/fpls.2014.00592 25408694

20. Klarzynski O, Plesse B, Joubert J-M, Yvin J-C, Kopp M, Kloareg B, et al. Linear β-1,3 Glucans Are Elicitors of Defense Responses in Tobacco. Plant Physiol. 2000;124: 1027–1038. doi: 10.1104/pp.124.3.1027 11080280

21. Mercier L, Lafitte C, Borderies G, Briand X, Esquerré-Tugayé MT, Fournier J. The algal polysaccharide carrageenans can act as an elicitor of plant defence. New Phytol. 2001;149: 43–51. doi: 10.1046/j.1469-8137.2001.00011.x

22. Mani SD, Nagarathnam R. Sulfated polysaccharide from Kappaphycus alvarezii (Doty) Doty ex P.C. Silva primes defense responses against anthracnose disease of Capsicum annuum Linn. Algal Res. 2018;32: 121–130. doi: 10.1016/j.algal.2018.02.025

23. Venegas M, Edding ME, Matsuhiro B. Alginate Composition of Lessonia trabeculata (Phaeophyta: Laminariales) Growing in Exposed and Sheltered Habitats. Bot Mar. 1993;36: 47–52. doi: 10.1515/botm.1993.36.1.47

24. XU X, IWAMOTO Y, KITAMURA Y, ODA T, MURAMATSU T. Root Growth-promoting Activity of Unsaturated Oligomeric Uronates from Alginate on Carrot and Rice Plants. Biosci Biotechnol Biochem. 2003;67: 2022–2025. doi: 10.1271/bbb.67.2022 14519996

25. Hu X, Jiang X, Hwang H, Liu S, Guan H. Promotive effects of alginate-derived oligosaccharide on maize seed germination. J Appl Phycol. 2004;16: 73–76. doi: 10.1023/B:JAPH.0000019139.35046.0c

26. Küpper FC, Carpenter LJ, Leblanc C, Toyama C, Uchida Y, Maskrey BH, et al. In vivo speciation studies and antioxidant properties of bromine in Laminaria digitata reinforce the significance of iodine accumulation for kelps. J Exp Bot. 2013;64: 2653–2664. doi: 10.1093/jxb/ert110 23606364

27. Song W, Ma X, Tan H, Zhou J. Abscisic acid enhances resistance to Alternaria solani in tomato seedlings. Plant Physiol Biochem. Elsevier Masson SAS; 2011;49: 693–700. doi: 10.1016/j.plaphy.2011.03.018 21530290

28. Dugyala S, Borowicz P, Acevedo M. Rapid protocol for visualization of rust fungi structures using fluorochrome Uvitex 2B. Plant Methods. BioMed Central; 2015;11: 19–21. doi: 10.1186/s13007-015-0096-0 26692889

29. Spricigo D. A., Cortes P., Moranta D., Barbe J., Bengoechea J. A., & Llagostera M. Signifi cance of tagI and mfd genes in the virulence of non-typeable Haemophilus infl uenzae. Int Microbiol. 2014;17: 159–164. doi: 10.2436/20.1501.01.218 26419455

30. Kumar D, Yusuf M, Singh P, Sardar M, Sarin N. Histochemical Detection of Superoxide and H2O2 Accumulation in Brassica juncea Seedlings. Bio-Protocol. 2014;4. doi: 10.21769/BioProtoc.1108

31. Daudi A. O’Brien JA. Detection of Hydrogen Peroxide by DAB Staining in Arabidopsis Leaves. Bio Protoc. 2012;2: 1–4. doi: 10.21769/BioProtoc.263

32. Sellers RM. Spectrophotometric determination of hydrogen peroxide using potassium titanium(IV) oxalate. Analyst. 1980;105: 950–954. doi: 10.1039/an9800500950

33. Heath RL PL. Photoperoxidation in isolated Chloroplasts of Fatty Acid Peroxidation chlorophyll. Arch Biochem biophisics. 1968;125: 189–198.

34. Bradford MM. A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Anal Biochem. 1976;72: 248–254. doi: 10.1006/abio.1976.9999 942051

35. Volk S, Feierabend J. Photoinactivation of catalase at low temperature and its relevance to photosynthetic and peroxide metabolism in leaves. Plant Cell Environ. 1989;12: 701–712. doi: 10.1111/j.1365-3040.1989.tb01630.x

36. Davis BJ. DISC ELECTROPHORESIS—II METHOD AND APPLICATION TO HUMAN SERUM PROTEINS*. 2006;121: 404–427. doi: 10.1111/j.1749-6632.1964.tb14213.x

37. Beauchamp C., Fridovich I. Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Anal Biochem. 1971;44: 276–287. doi: 10.1016/0003-2697(71)90370-8 4943714

38. Schwert G. W., Takenaka Y. A spectrophotometric determination of trypsin and chymotrypsin. Biochim Biophys Acta. 1955;16: 570–575. doi: 10.1016/0006-3002(55)90280-8 14389277

39. Levine A, Tenhaken R, Dixon R, Lamb C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell. 1994;79: 583–593. doi: 10.1016/0092-8674(94)90544-4 7954825

40. Battacharyya D, Babgohari MZ, Rathor P, Prithiviraj B. Seaweed extracts as biostimulants in horticulture. Sci Hortic (Amsterdam). Elsevier B.V.; 2015;196: 39–48. doi: 10.1016/j.scienta.2015.09.012

41. Luan LQ, Nagasawa N, Ha VTT, Hien NQ, Nakanishi TM. Enhancement of plant growth stimulation activity of irradiated alginate by fractionation. Radiat Phys Chem. Elsevier; 2009;78: 796–799. doi: 10.1016/j.radphyschem.2009.05.001

42. Ali A, Khan MMA, Uddin M, Naeem M, Idrees M, Hashmi N, et al. Radiolytically depolymerized sodium alginate improves physiological activities, yield attributes and composition of essential oil of Eucalyptus citriodora Hook. Carbohydr Polym. Elsevier Ltd.; 2014;112: 134–144. doi: 10.1016/j.carbpol.2014.05.070 25129727

43. Aftab T, Khan MMA, Idrees M, Naeem M, Moinuddin, Hashmi N, et al. Enhancing the growth, photosynthetic capacity and artemisinin content in Artemisia annua L. by irradiated sodium alginate. Radiat Phys Chem. Elsevier; 2011;80: 833–836. doi: 10.1016/j.radphyschem.2011.03.004

44. Idrees M, Naeem M, Alam M, Aftab T, Hashmi N, Khan MMA, et al. Utilizing the γ-Irradiated Sodium Alginate as a Plant Growth Promoter for Enhancing the Growth, Physiological Activities, and Alkaloids Production in Catharanthus roseus L. Agric Sci China. Chinese Academy of Agricultural Sciences; 2011;10: 1213–1221. doi: 10.1016/S1671-2927(11)60112-0

45. Idrees M, Dar TA, Naeem M, Aftab T, Khan MMA, Ali A, et al. Effects of gamma-irradiated sodium alginate on lemongrass: Field trials monitoring production of essential oil. Ind Crops Prod. Elsevier B.V.; 2015;63: 269–275. doi: 10.1016/j.indcrop.2014.09.037

46. Sano Y. Antiviral activity of alginate against infection by tobacco mosaic virus. Carbohydr Polym. 1999;38: 183–186. doi: 10.1016/S0144-8617(98)00119-2

47. Valko M, Morris H, Cronin MTD. Metals, Toxicity and Oxidative Stress. Curr Med Chem. 2005;12: 1161–1208. doi: 10.2174/0929867053764635 15892631

48. Das K, Roychoudhury A. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci. 2014;2: 1–13. doi: 10.3389/fenvs.2014.00053

49. Mishra S, Jha AB, Dubey RS. Arsenite treatment induces oxidative stress, upregulates antioxidant system, and causes phytochelatin synthesis in rice seedlings. Protoplasma. 2011;248: 565–577. doi: 10.1007/s00709-010-0210-0 20857150

50. Han C, Liu Q, Yang Y. Short-term effects of experimental warming and enhanced ultraviolet-B radiation on photosynthesis and antioxidant defense of Picea asperata seedlings. Plant Growth Regul. 2009;58: 153–162. doi: 10.1007/s10725-009-9363-2

51. Yi S, Yu S, Choi D. Involvement of Hydrogen Peroxide in Repression of Catalase in TMV-infected Resistant Tobacco. Mol Cells. 2003;15: 364–369. 12872994

52. Blackman LM, Hardham AR. Regulation of catalase activity and gene expression during Phytophthora nicotianae development and infection of tobacco. Mol Plant Pathol. 2008;9: 495–510. doi: 10.1111/j.1364-3703.2008.00478.x 18705863

53. Chavan V, Bhargava S, Kamble A. Temporal modulation of oxidant and antioxidative responses in Brassica carinata during β-aminobutyric acid-induced resistance against Alternaria brassicae. Physiol Mol Plant Pathol. Elsevier Ltd; 2013;83: 35–39. doi: 10.1016/j.pmpp.2013.03.002

54. Spanu P, Bonfante-Fasolo P. Cell-wall-bound peroxidase activity in roots of mycorrhizal Allium porrum. New Phytol. 1988;109: 119–125.

55. Fries LM, Pacovsky S, Safir GR. Expression of isoenzymes altered by both Glomus intraradices colonization and formononetin application in corn (Zea mays L.) roots. soil Biol Biochem. 1996;28: 981–988.

56. Lambais AMR, Andrade RM, The S, Phytologist N, Nov N, Lambais MR, et al. Antioxidant Responses in Bean (Phaseolus vulgaris) Roots Colonized by Arbuscular Mycorrhizal Fungi. New Phytol. 2003;160: 421–428. doi: 10.1046/j.1469-8137.2003.00881.x

57. Bela K, Horváth E, Gallé Á, Szabados L, Tari I, Csiszár J. Plant glutathione peroxidases: Emerging role of the antioxidant enzymes in plant development and stress responses. J Plant Physiol. Elsevier GmbH.; 2015;176: 192–201. doi: 10.1016/j.jplph.2014.12.014 25638402

58. Scandalios JG. Oxygen Stress and Superoxide Dismutases. Plant Physiol. 1993;101: 7–12. doi: 10.1104/pp.101.1.7 12231660

59. Wang S, Lin J, Ye M, Ng TB, Rao P, Ye X. Isolation and characterization of a novel mung bean protease inhibitor with antipathogenic and anti-proliferative activities. Peptides. 2006;27: 3129–3136. doi: 10.1016/j.peptides.2006.07.013 16971020

60. Tian M, Benedetti B, Kamoun S. Bubnova2012.Pdf. 2005;138: 1785–1793. doi: 10.1104/pp.105.061226.1

61. Radhakrishnan N, Balasubramanian R. Salicylic acid induced defence responses in Curcuma longa (L.) against Pythium aphanidermatum infection. Crop Prot. Elsevier Ltd; 2009;28: 974–979. doi: 10.1016/j.cropro.2009.07.010

62. Radhakrishnan N, Alphonse AJ, Balasubramanian R. Effect of Acibenzolar-S-methyl (ASM) pre-treatment in inducing resistance against Pythium aphanidermatum infection in Curcuma longa. Crop Prot. 2011;30: 24–32. doi: 10.1016/j.cropro.2010.08.020

63. Baysal Ö, Gürsoy YZ, Örnek H, Duru A. Enhanced tomato resistance to bacterial canker by application of turtle oil. J Gen Plant Pathol. 2005;71: 204–210. doi: 10.1007/s10327-005-0194-3

64. Dong X. NPR1, all things considered. Curr Opin Plant Biol. 2004;7: 547–552. doi: 10.1016/j.pbi.2004.07.005 15337097

65. Lawrence CB, Singh NP, Qiu J, Gardner RG, Tuzun S. Constitutive hydrolytic enzymes are associated with polygenic resistance of tomato to Alternaria solani and may function as an elicitor release mechanism. Physiol Mol Plant Pathol. 2000;57: 211–220. doi: 10.1006/pmpp.2000.0298

66. Porta H, Rocha-sosa M. Plant Lipoxygenases. Physiological and Molecular Features. Plant Physiol. 2002;130: 15–21. doi: 10.1104/pp.010787 12226483

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