doi: 10.15389/agrobiology.2018.5.958eng

UDC 633.41:632.4:578.1:58.071

 

EFFECT OF Bacillus subtilis BASED MICRROBIALS ON PHYSIOLOGICAL
AND BIOCHEMICAL PARAMETERS OF SUGAR BEET (Beta vulgaris L.)
PLANTS INFECTED WITH Alternaria alternata

O.V. Lastochkina1, 2, L.I. Pusenkova1, R.A. Yuldashev1, 2, E.Yu. Ilyasova1, S. Aliniaeifard3

1Bashkir Research Institute of Agriculture, Subdivision of the Ufa Federal Research Centre RAS, Federal Agency for Scientific Organizations, 19, ul. Riharda Zorge, Ufa, 450059 Russia, e-mail oksanaibg@gmail.com (✉ corresponding author);
2Institute of Biochemistry and Genetics, Subdivision of the Ufa Federal Research Centre RAS, Federal Agency for Scientific Organizations, 71, prosp. Oktyabrya, Ufa, 450054 Russia, e-mail yuldashevra@gmail.com;
3University of Tehran, Aburaihan campus, PC 3391653775 Pakdasht, Tehran, Iran, e-mail aliniaeifard@ut.ac.ir

ORCID:
Lastochkina O.V. orcid.org/0000-0003-3398-1493
Pusenkova L.I. orcid.org/0000-0001-6341-0486
Yuldashev R.A. orcid.org/0000-0001-9033-6867
Ilyasova E.Y. orcid.org/0000-0001-5737-5469
Aliniaeifard S. orcid.org/0000-0001-9572-2839
The authors declare no conflict of interests

Received February 9, 2018

 

Phytopathogenic Alternaria fungi are economically important causative agents of sugar beet (Beta vulgaris L.) leaf diseases which significantly reduce root yield and quality. Promising agents for plant disease biocontrol are Bacillus subtilis based biologicals due to the ability to stimulate plant growth and immunity to many biotic stressors. Starting our experiments, we could not find publications on B. subtilis effects towards physiological parameters of sugar beet plants affected by Alternaria. This paper is the first to report that B. subtilis-based biologicals including novel Bashkirian isolate B. subtilis 10-4 prevent a decrease in leaf photosynthetic activity in sugar beet plants affected by A. alternata, activate hydrolytic enzyme inhibitors, suppress proline production, and increase sugar content in roots. Our objective was to estimate effects of Fitosporin-M, Vitaplan, and endophytic strain B. subtilis10-4 on leaf photosynthetic pigments (chlorophyll a, b and carotenoids), leaf area index, activity of hydrolases (proteases and amylases) and their inhibitors, as well as proline and sugar levels in leaves, root level of sucrose, and productivity in healthy plants as compared to those artificially infected with A. alternata. Our results show that Vitaplan, Fitosporin-M and strain B. subtilis 10-4 when used twice increase the concentrations of photosynthetic pigments (chlorophyll a, b and carotenoids) 1.2-1.9-fold in healthy plants whereas a decrease in photosynthetic activity in A. alternata-infected plants is 1.2-1.5 times lower, the leaf area is 30 % higher and leaf weight increases 1.8-2.9 times compared to the untreated plants. A. alternata infection increased the activity of hydrolases (proteinase, amylase) and suppressed their inhibitors, which indicates the intensive development of the pathogen and a decrease in plant resistance to enzymes produced by pathogen during plant tissue colonization. On contrary, biologicals suppress hydrolases and increase activity of their inhibitors both in infected and healthy leaves, which points out to the induction of protective reactions against A. alternata in plants. Interestingly, B. subtilis 10-4 and Fitosporin-M ensure the maximum activation of protective proteins. Furthermore, biologicals decrease stress-induced accumulation of proline and sugar, the markers of plant resistance to extremal factors in plants, which is in line with protective effect as well. Also, proline and sugar levels slightly elevated in healthy plants treated with the biologicals, which accentuate the role of these substances in induced resistance to A. alternata. Ultimately, larger roots with higher sucrose content confirm the positive effect of the used biologicals among which Fitosporin-M and strain B. subtilis 10-4 provide the maximum effect.

Keywords: Bacillus subtilis, photosynthetic pigments, hydrolases, sugar, proline, sucrose, Alternaria alternata, resistance, productivity, Beta vulgaris L., sugar beet.

 

Full article (Rus)

Full article (Eng)

 

REFERENCES

  1. Shamilev R.V., Shamilev S.R. Sovremennye problemy nauki i obrazovaniya, 2011, 6: 1-7 (in Russ.).
  2. Stognienko O.I., Selivanova G.A. Bolezni sakharnoi svekly, ikh vozbuditeli [Diseases and pathogens of sugar beet plants]. Voronezh, 2008 (in Russ.).
  3. Zavalin A.A. Biopreparaty, udobreniya i urozhai [Biologicals, fertilizers and crop yield]. Moscow, 2005 (in Russ.).
  4. Berg G. Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl. Microbiol. Biot., 2009, 84(1): 11-18 CrossRef
  5. Perez-Garcia A., Romero D., de Vicente A. Plant protection and growth stimulation by microorganisms: biotechnological applications of Bacilli in agriculture. Curr. Opin. Biotech., 2011, 22: 187-193 CrossRef
  6. Pusenkova L.I., Il'yasova E.Yu., Maksimov I.V., Lastochkina O.V. Enhancement of adaptive capacity of sugar beet crops by microbial biopreparations under biotic and abiotic stresses. Agricultural Biology], 2015, 50(1): 115-123 CrossRef
  7. Esitken A., Yildiz H.E., Ercisli S., Donmez M.F., Turan M., Gunes A. Effects of plant growth promoting bacteria (PGPB) on yield, growth and nutrient contents of organically grown strawberry. Scientia Horticulturae, 2010, 124: 62-66 CrossRef
  8. Lastochkina O., Pusenkova L., Yuldashev R., Babaev M., Garipova S., Blagova D., Khairullin R., Aliniaeifard S. Effects of Bacillus subtilis on some physiological and biochemical parameters of Triticum aestivum L. (wheat) under salinity. Plant Physiol. Bioch., 2017, 121: 80-88 CrossRef
  9. Turan M., Ekinci M., Yildirim E., Günes A., Karagöz K., Kotan R., Dursun A. Plant growth-promoting rhizobacteria improved growth, nutrient, and hormone content of cabbage (Brassica oleracea) seedlings. Turk. J. Agric. For., 2014, 38: 327-333 CrossRef
  10. Abeer H., Asma A.H., Allah A., Qarawi A., Shalawi A., Dilfuza E. Impact of plant growth promoting Bacillus subtilis on growth and physiological parameters of Bassia indica (Indian Bassia) grown under salt stress. Pak. J. Bot., 2015, 47(5): 1735-1741.
  11. Shternshis M.V., Belyaev A.A., Shpatova T.V., Lelyak A.A. Influence of Bacillus spp. on strawberry gray-mold causing agent and host plant resistance to disease. Contemp. Probl. Ecol., 2015, 8(3): 390-396 CrossRef
  12. Ivanchina N.V., Garipova S.R. Agrokhimiya, 2012, 7: 87-95 (in Russ.).
  13. Gutierrez-Manero F.J., Ramos-Solano B., Probanza A., Mehouachi J., Tadeo F.R., Talon M. The plant growth promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiologia Plantarum, 2008, 111(2): 206-211 CrossRef
  14. Malfanova N., Franzil L., Lugtenberg B., Chebotar V., Ongena M. Cyclic lipopeptide profile of the plant-beneficial endophytic bacterium Bacillus subtilis HC8. Arch. Microbiol., 2012, 194(11): 893-899 CrossRef
  15. Bottini R., Cassan F., Piccoli P. Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Appl. Microbiol. Biot., 2004, 65(5): 497-503 CrossRef
  16. Grichko V.P., Glick B.R.Amelioration of flooding stress by ACC deaminase-containing plant growth-promoting bacteria. Plant Physiol. Bioch., 2001, 39(1): 11-17 CrossRef
  17. Choudhary D.K., Johri B.N. Interactions of Bacillus sp. and plants — with special reference to induced systemic resistance (ISR). Microbiol. Res., 2009, 164: 493-513 CrossRef
  18. Niu D.D., Liu H.X., Jiang C.H., Wang Y.P., Wang Q.Y., Jin H.L., Guo J.H. The plant growth-promoting rhizobacterium Bacillus cereus AR156 induces systemic resistance in Arabidopsis thaliana by simultaneously activating salicylate- and jasmonate/ethylene-dependent signaling pathways. Mol. Plant Microbe. In., 2011, 24(5): 533-542 CrossRef
  19. García-Gutiérrez L., Zeriouh H., Romero D., Cubero J., de Vicente A., Pérez-García A. The antagonistic strain Bacillus subtilis UMAF6639 also confers protection to melon plants against cucurbit powdery mildew by activation of jasmonate- and salicylic acid-dependent defense responses. Microb. Biotechnol., 2013, 6: 264-274 CrossRef
  20. González-Gallegos E., Laredo-Alcalá E., Ascacio-Valdés J., Jasso de Rodríguez D., Hernández-Castillo F.D. Changes in the production of salicylic and jasmonic acid in potato plants (Solanum tuberosum) as response to foliar application of biotic and abiotic inductors. American Journal of Plant Sciences, 2015, 6(11): 1785-1791 CrossRef
  21. Shpirnaya I.A., Ibragimov R.I., Umarov I.A. Vestnik BGU, 2006, 3(11): 49-52 (in Russ.).
  22. Demirevska-Kepova K., Simova-Stoilova L., Petrova Stoyanova Z., Feller U. Cadmium stress in barley: growth, leaf pigment, and protein composition and detoxification of reactive oxygen species. J. Plant Nutr., 2006, 29(3): 451-468 CrossRef
  23. Ievleva E.V., Revina T.A., Kudryavtseva N.N., Sof'in A.V., Valueva T.A. Prikladnaya biokhimiya i mikrobiologiya, 2006, 42(3): 338-344 (in Russ.).
  24. Kolupaev Yu.E., Yastreb T.O. Vestnik KHNU. Seriya Biologiya, 2015, 2(35): 6-25 (in Russ.).
  25. Molinari H.B.C., Marur C.J., Daros E., de Campos M.K.F., de Carvalho J.F.R.P., Filho B.J.C., Pereira L.F.P., Vieira L.G.E. Evaluation of the stress-inducible production of proline in transgenic sugarcane (Saccharum spp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiologia Plantarum, 2007, 130(2): 218-229 CrossRef
  26. Shakirova F.M., Avalbaev A.M., Bezrukova M.V., Fatkhutdinova R.A., Maslennikova D.R., Yuldashev R.A., Allagulova Ch.R., Lastochkina O.V. Phytohormones and abiotic stress tolerance in plants. N. Khan, R. Nazar, N. Iqbal, N. Anjum (eds.). Springer, Berlin Heidelberg, 2012 CrossRef
  27. Jefferey S.W., Humphrey G.F. New spectrophotometric equations for determining chlorophylls a, b, c1, and c2 in higher plants, algae, and natural phytoplankton. Biochem. Physiol. Pfl., 1975, 167: 191-194.
  28. Wettstein P. Chrofyll — letal und der submiscopische Form wechsel der Plastiden. Exp. Cell Res., 1957, 12(4): 427-431.
  29. Bates L.S., Waldern. R.P., Teare D. Rapid determination of free proline for water-stress studies. Plant Soil, 1973, 39: 205-207.
  30. Kalinkina L.G. Fiziologiya rastenii, 1985, 32: 42-52 (in Russ.).
  31. Erlanger B.F., Kokowski N., Cohen W. The preparation and properties of two new chromogenic substrates of trypsin. Arch. Biochem. Biophys, 1961, 95: 271-278.
  32. Metodika opredeleniya khimicheskogo sostava i pokazatelei kachestva sakharnoi svekly [Analysis of chemical composition and quality indicators of sugar beet plants]. Kursk, 2001(in Russ.).
  33. Litvinov S.S. Metodika polevogo opyta v ovoshchevodstve [Field trials in olericulture]. Moscow, 2011 (in Russ.).
  34. Andriyanova Yu.E., Tarchevskii I.A. Khlorofill i produktivnost' rastenii [Chlorophyll and plant productivity]. Moscow, 2000 (in Russ.).
  35. Cuttriss A.J., Pogson B.J. Carotenoids. Plant pigments and their manipulation. K.M. Davies (ed.). CRC Press, Boca Raton, 2004.
  36. Gill S.S., Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Bioch., 2010, 48: 909-930 CrossRef
  37. Edge R., Truscott G. Properties of carotenoid radicals and excited states and their potential role in biological systems. In: Carotenoids: physical, chemical, and biological functions and properties. J.T. Landrum (ed.). Kluwer, Dordrecht, 2010.
  38. Smolikova G.N., Medvedev S.S. Fiziologiya rastenii, 2015, 62(1): 3-16 (in Russ.).
  39. Jahns P., Holzwarth A.R. The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. BBA-Bioenergetics, 2012, 1817(1): 182-193 CrossRef
  40. Kim Y., Mosier N.S., Ladisch M.R.Enzymatic digestion of liquid hot water pretreated hybrid poplar. Biotechnol. Progr., 2009, 25(2): 340-348 CrossRef
  41. Piskureva V.A., Pavlovskaya N.E., Gor'kova I.V., Zhitnikova B.C. Pishchevaya promyshlennost', 2009, 6: 50-51 (in Russ.).
  42. Karpets Yu.V., Kolupaev Yu.E. Vestnik KHNU. Seriya biologiya, 2009, 1(16): 19-38 (in Russ.).
  43. Szabados L., Savoure A. Proline: a multifunctional amino acid. Trends Plant Sci., 2010, 15(2): 89-97 CrossRef

back