Effect of Endophytic Bacteria Bacillus subtilis on Seedling Growth and Root Lignification of Pisum sativum L. under Normal and Sodium Chloride Salt Conditions

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Abstract

The influence of endophytic bacteria Bacillus subtilis (strain 10-4) was studied on the parameters of growth and tolerance as well as the intensity of lignin deposition in the roots of Pisum sativum L. seedlings under conditions of sodium chloride salinity (1% NaCl). It was found that the impact of salinity reduced the germination energy, viability, length of the roots and shoots of seedlings, their wet and dry weight, and also increased the content of proline and the level of lipid peroxidation (LPO). Pretreatment with strain 10-4 had a stimulating effect on seedlings in normal conditions and a protective effect on salinity, which was reflected in the improvement of germination energy and seed viability, root length, and accumulation of their dry mass under saline conditions; however, in terms of shoot growth under stress, there was no significant difference from the control (nonbacterized) variants. At the same time, strain 10-4 promoted earlier formation of lateral roots as well as a decrease in stress-induced LPO and proline content in seedlings, which indicates that cells are protected from oxidative and osmotic damage under saline conditions. Priority data were obtained on the important role of endophytic B. subtilis strain 10-4 in the process of lignification and strengthening of the barrier properties of the cell walls of the roots, which contributes to the reduction of the toxic effect of sodium chloride salinity and the implementation of the protective effect of these bacteria on pea plants.

About the authors

O. V. Lastochkina

Institute of Biochemistry and Genetics, Ufa Federal Research Center, Russian Academy of Sciences

Email: fizrast@mail.ru
Ufa, Russia

S. R. Garipova

Bashkir Research Institute of Agriculture, Ufa Federal Research Center, Russian Academy of Sciences

Email: fizrast@mail.ru
Ufa, Russia

L. I. Pusenkova

Bashkir Research Institute of Agriculture, Ufa Federal Research Center, Russian Academy of Sciences

Email: fizrast@mail.ru
Ufa, Russia

D. Yu. Garshina

Bashkir Research Institute of Agriculture, Ufa Federal Research Center, Russian Academy of Sciences

Email: fizrast@mail.ru
Ufa, Russia

An. Kh. Baymiev

Institute of Biochemistry and Genetics, Ufa Federal Research Center, Russian Academy of Sciences; Bashkir Research Institute of Agriculture, Ufa Federal Research Center, Russian Academy of Sciences

Email: fizrast@mail.ru
Ufa, Russia; Ufa, Russia

I. S. Koryakov

Institute of Biochemistry and Genetics, Ufa Federal Research Center, Russian Academy of Sciences

Author for correspondence.
Email: fizrast@mail.ru
Ufa, Russia

References

  1. Mukhopadhyay R., Sarkar B., Jat H.S., Sharma P.C., Bolan N.S. Soil salinity under climate change: Challenges for sustainable agriculture and food security // J. Environ. Manage. 2021. V. 280: e111736. https://doi.org/10.1016/j.jenvman.2020.111736
  2. Isayenkov S.V., Maathuis F.J. Plant salinity stress: many unanswered questions remain // Front. Plant Sci. 2019. V. 10: e80. https://doi.org/10.3389/fpls.2019.00080
  3. Numan M., Bashir S., Khan Y., Mumtaz R., Shinwari Z.K., Khan A.L., Khan A., AL-Harrasi A. Plant growth promoting bacteria as an alternative strategy for salt tolerance in plants: a review // Microbiol. Res. 2018. V. 209. P. 21. https://doi.org/10.1016/j.micres.2018.02.003
  4. Lastochkina O., Aliniaeifard S., Garshina D., Garipova S., Pusenkova L., Allagulova Ch., Fedorova K., Baymiev A., Koryakov I., Sobhani M. Seed priming with endophytic Bacillus subtilis strain-specifically improves growth of Phaseolus vulgaris plants under normal and salinity conditions and exerts anti-stress effect through induced lignin deposition in roots and decreased oxidative and osmotic damages // J. Plant Physiol. 2021. V. 263: e153462. https://doi.org/10.1016/j.jplph.2021.153462
  5. Lastochkina O. Bacillus subtilis-mediated abiotic stress tolerance in plants // Bacilli and agrobiotechnology: phytostimulation and biocontrol / Eds. M.T. Islam et al. Springer. 2019. P. 97. https://doi.org/10.1007/978-3-030-15175-1_6
  6. Benedetto N.A., Corbo M.R., Campaniello D., Cataldi M.P., Bevilacqua A., Sinigaglia M., Flagella Z. The role of plant growth promoting bacteria in improving nitrogen use efficiency for sustainable crop production: a focus on wheat // AIMS Microbiol. 2017. V. 3. P. 413. https://doi.org/10.3934/microbiol.2017.3.413
  7. Abd El-Daim I.A., Bejai S., Fridborg I., Meijer J. Identifying potential molecular factors involved in Bacillus amyloliquefaciens 5113 mediated abiotic stress tolerance in wheat // Plant Biol. 2018. V. 20. P. 271. https://doi.org/10.1111/plb.12680
  8. Abd El-Daim I.A., Bejai S., Meijer J. Bacillus velezensis 5113 induced metabolic and molecular reprogramming during abiotic stress tolerance in wheat // Sci. Rep. 2019. V. 9. P. 16282. https://doi.org/10.1038/s41598-019-52567-x
  9. Blake C., Christensen M.N., Kovács Á. Molecular aspects of plant growth promotion and protection by Bacillus subtilis // MPMI. 2021. V. 34. P. 15. https://doi.org/10.1094/MPMI-08-20-0225-CR
  10. Gupta A., Bano A., Rai S., Kumar M., Ali J., Sharma S., Pathak N. ACC deaminase producing plant growth promoting rhizobacteria enhance salinity stress tolerance in Pisum sativum // Biotech. 2021. V. 11: e514. https://doi.org/10.1007/s13205-021-03047-5
  11. Eichmann R., Richards L., Schäfer P. Hormones as go-betweens in plant microbiome assembly // Plant J. 2021. V. 105. P. 518. https://doi.org/10.1111/tpj.15135
  12. Shobana N., Sugitha T., Sivakumar U. Plant growth-promoting Bacillus sp. cahoots moisture stress alleviation in rice genotypes by triggering antioxidant defense system // Microbiol. Res. 2020. V. 239: e126518. https://doi.org/10.1016/j.micres.2020.126518
  13. Barnawal D., Bharti N., Pandey S.S., Pandey A., Chanotiya C.S., Kalra A. Plant growth promoting rhizobacteria enhances wheat salt and drought stress tolerance by altering endogenous phytohormone levels and TaCTR1/TaDREB2 expression // Physiol. Plant. 2017. V. 161. P. 502. https://doi.org/10.1111/ppl.12614
  14. 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. Biochem. 2017. V. 121. P. 80. https://doi.org/10.1016/j.plaphy.2017.10.020
  15. Vasileva E.N., Akhtemova G.A., Zhukov V.A., Tikhonovich I.A. Endophytic microorganisms in fundamental research and agriculture // Ecological Genetics. 2019. V. 17. P. 19. https://doi.org/10.17816/ecogen17119-32
  16. Pandey P.K., Singh M.C., Singh S.S., Kumar M., Pathak M., Shakywar R.C., Pandey A.K. Inside the plants: endophytic bacteria and their functional attributes for plant growth promotion // Int. J. Curr. Microbiol. Appl. Sci. 2017. V. 6. P. 11. https://doi.org/10.20546/ijcmas.2017.602.002
  17. Hardoim P.R., van Overbeek L.S., Berg G., Pirttilä A.M., Compant S., Campisano A., Döring M., Sessitsch A. The hidden world within plants: Ecological and evolutionary considerations for defining functioning of microbial endophytes // Microbiol. Mol. Biol. Rev. 2015. V. 79. P. 293. https://doi.org/10.1128/MMBR.00050-14
  18. Tikhonovich I.A., Andronov E.E., Borisov A.Yu., Dolgikh E.A., Zhernakov A.I., Zhukov V.A., Provorov N.A., Rumyantseva M.L., Simarov B.V. The principle of complementarity of genomes in expanding the adaptive potential of plants // Genetics. 2015. V. 51. P. 973. https://doi.org/10.1134/S1022795415090124
  19. Vasileva E.N., Akhtemova G.A., Afonin A.M., Borisov A.Yu., Tikhonovich I.A., Zhukov V.A. Culturable endophytic bacteria from stems and leaves of garden pea (Pisum sativum L.) // Ecological Genetics. 2020. V. 18. P. 169. https://doi.org/10.17816/ecogen17915
  20. Гарипова С.Р., Маркова О.В., Гарифуллина Д.В., Иванчина Н.В., Хайруллин Р.М. Региональная коллекция бактериальных эндофитов клубеньков бобовых растений как основа создания биопрепаратов для агробиотехнологии // Известия Уфимского научного центра Российской академии наук. 2017. Т. 3. С. 56.
  21. Hasanuzzaman M., Bhuyan M.H.M.B., Zulfiqar F., Raza A., Mohsin S.M., Mahmud J.A., Fujita M., Fotopoulos V. Reactive oxygen species and antioxidant defense in plants under abiotic stress: Revisiting the crucial role of a universal defense regulator // Antioxidants. 2020. V. 9. P. 681. https://doi.org/10.3390/antiox9080681
  22. Morales M., Munné-Bosch S. Malondialdehyde: Facts and Artifacts // Plant Physiol. 2019. V. 180. P. 1246. https://doi.org/10.1104/pp.19.00405
  23. Kavi K.P.B., Hima K.P., Sunita M.S., Sreenivasulu N. Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny // Front. Plant Sci. 2015. V. 66: e544. https://doi.org/10.3389/fpls.2015.00544
  24. Garipova S.R., Markova O.V., Fedorova K.A., Dedova M.A., Iksanova M.A., Kamaletdinova A.A., Lastochkina O.V., Pusenkova L.I. Malondialdehyde and proline content in bean cultivars following the inoculation with endophytic bacteria // Acta Physiol. Plant. 2022. V. 44. P. 89. https://doi.org/10.1007/s11738-022-03427-1
  25. Xie M., Zhang J., Tschaplinski T.J., Tuskan G.A., Chen J.-G., Muchero W. Regulation of lignin biosynthesis and its role in growth-defense tradeoffs // Front. Plant Sci. 2018. V. 9. P. 1427. https://doi.org/10.3389/fpls.2018.01427
  26. Гарипова С.Р., Маркова О.В., Вахитова Р.К., Гарифуллина Д.В., Каримов И.К., Давлетов Ф.А. Сравнение морфометрических показателей симбиоза, продуктивности и устойчивости к корневым гнилям и плодожорке у усатых и листочковых сортов гороха в условиях Предуралья // Вестник Башкирского университета. 2015. Т. 20. С. 460.
  27. Heath R.L., Packer L. Photoperoxidation in isolated chloroplasts. Kinetics and stoichiometry of fatty acid peroxidation // Arch. Biochem. Bioph. 1968. V. 125. P. 189. https://doi.org/10.1016/0003-9861(68)90654-1
  28. Bates L.S., Waldern. R.P., Teare D. Rapid determination of free proline for water-stress studies // Plant Soil. 1973. V. 39. P. 205. https://doi.org/10.1007/BF00018060
  29. Фурст Г.Г. Методы анатомо-гистохимических исследований растений. Москва: Наука, 1979. 155 с.
  30. Abd Allah E.F., Alqarawi A.A., Hashem A., Radhakrishnan R., Al-Huqail A.A., Al-Otibi F.O.N., Malik J.A., Alharbi R.I., Egamberdieva D. Endophytic bacterium Bacillus subtilis (BERA 71) improves salt tolerance in chickpea plants by regulating the plant defense mechanisms // J. Plant Inter. 2018. V. 13. P. 37. https://doi.org/10.1080/17429145.2017.1414321
  31. Gupta A., Rai S., Bano A., Khanam A., Sharma S., Pathak N. Comparative evaluation of different salt-tolerant plant growth-promoting bacterial isolates in mitigating the induced adverse effect of salinity in Pisum sativum // Biointerface Res. Appl. Chem. 2021. V. 11. P. 13141. https://doi.org/10.33263/briac115.1314113154
  32. Sofy M.R., Aboseidah A.A., Heneidak S.A., Ahmed H.R. ACC deaminase containing endophytic bacteria ameliorate salt stress in Pisum sativum through reduced oxidative damage and induction of antioxidative defense systems // Environ. Sci. Pollut. Res. 2021. V. 28. P. 40971. https://doi.org/10.1007/s11356-021-13585-3
  33. Tamošiūnė I., Stanienė G., Haimi P., Stanys V., Rugienius R., Baniulis D. Endophytic Bacillus and Pseudomonas spp. modulate apple shoot growth, cellular redox balance, and protein expression under in vitro conditions // Front. Plant Sci. 2018. V. 9: e889. https://doi.org/10.3389/fpls.2018.00889
  34. Deivanai S., Bindusara A.S., Prabhakaran G., Bhore S.J. Culturable bacterial endophytes isolated from Mangrove tree (Rhizophora apiculata Blume) enhance seedling growth in rice // J. Nat. Sci. Biol. Med. 2014. V. 5. P. 437. https://doi.org/10.4103/0976-9668.136233
  35. Schmid-Siegert E., Loscos J., Farmer E.E. Inducible malondialdehyde pools in zones of cell proliferation and developing tissues in Arabidopsis // J. Biol. Chem. 2012. V. 287. P. 8954. https://doi.org/10.1074/jbc.M111.322842
  36. Wang G., Zhang J., Wang G., Fan X., Sun X., Qin H., Xu N., Zhong M., Qiao Z., Tang Y., Song R. Proline responding plays a critical role in regulating general protein synthesis and the cell cycle in maize // Plant Cell. 2014. V. 26. P. 2582. https://doi.org/10.1105/tpc.114.125559
  37. Guan C., Cen H.F., Cui X., Tian D.Y., Tadesse D., Zhang Y.W. Proline improves switchgrass growth and development by reduced lignin biosynthesis // Sci. Rep. 2019. V. 9: e20117. https://doi.org/10.1038/s41598-019-56575-9
  38. Moura J.C.M.S., Bonine C.A.V., Viana J.O.F., Dornelas M.C., Mazzafera P. Abiotic and biotic stresses and changes in the lignin content and composition in plants // J. Integr. Plant Biol. 2010. V. 52. P. 360. https://doi.org/10.1111/j.1744-7909.2010.00892.x
  39. Четина О.А., Еремченко О.З., Боталова Е.И., Середа А.М. Изменение в содержании пролина в растениях при воздействии NaCl-засоления и щелочности корневой среды // Современные проблемы науки и образования. 2016. Т. 6. С. 582.
  40. Jha Y. Cell water content and lignification in maize regulated by rhizobacteria under salinity // Braz. J. Biol. Sci. 2017. V. 4. P. 9. https://doi.org/10.21472/bjbs.040702

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