Influence of endophytic and epiphytic nitrogen-fixing bacteria on the content of negative allelopathic compounds in root exudates of pea (Pisum sativum L.) seedlings

Cover Page

Cite item

Full Text

Abstract

Substances that have a harmful effect on living organisms include N-phenyl-2-naphthalamine and phthalates, which are synthesized and widely used in the chemical industry. At the same time, N-phenyl-2-naphthylamine was found in the aerial parts and in the roots of some plant species, phthalates were found in many plant species and in bacteria. The aim of this research was to study the protective (antimicrobial) reaction of pea (Pisum sativum L.) seedlings of the Torsdag variety to the inoculation with bacteria Rhizobium leguminosarum bv. viceae (endosymbiont) and Azotobacter chroococcum (ectosymbiont) introduced into the aqueous medium of root growth were studied. Changes in the content of negative allelopathic compounds (pisatin, N-phenyl-2-naphthylamine, phthalates) in root exudates were the reaction indicators. After the inoculation, the seedlings grew for 24 h in the BINDER KBW-240 chamber at 21 °C, with lighting of 81 μM.m-2 . sec-1 and a 16/8 h day/night photoperiod. In ethyl acetate extracts from the aqueous medium where the seedling roots were immersed, the content of the compounds was determined by HPLC, while changes in the composition and ratio of phthalates were determined by GC-MS. Data indicating the different ability of both bacterial species to degrade N-phenyl-2-naphthylamine to phthalates and the dependence of this process activity in the bacteria studied on its concentration in the medium were presented. N-phenyl-2-naphthylamine differently but negatively affected the viability and growth of the bacteria used in the experiments. A different effect of rhizobia and azotobacter on the content of the above named compounds and on the ratio of types of phthalates in root exudates was elicited.

About the authors

L. E. Makarova

Siberian Institute of Plant Physiology and Biochemistry SB RAS

Email: makarova@sifibr.irk.ru

I. G. Petrova

Siberian Institute of Plant Physiology and Biochemistry SB RAS

Email: hplc_04@mail.ru

N. A. Sokolova

Siberian Institute of Plant Physiology and Biochemistry SB RAS

Email: fhma_lab@mail.ru

S. S. Makarov

Irkutsk National Research Technical University

Email: makarov@mail.ru

V. A. Pionkevich

Irkutsk National Research Technical University

Email: pionkevichva@mail.ru

References

  1. Султанходжаев М. Н., Таджибаев М. М. Фенил-β-нафтиламин из трех видов растений // Химия природных соединений. 1976. Т. 12. N 3. С. 406.
  2. Евстратова Р. И., Запесочная Г. Г. N-фенил-2-нафтиламин из Centaurea salonitana // Химия природных соединений. 1977. N 4. С. 582.
  3. Жанаева T. A., Кривощекова О. Е., Семенов А. А., Минаева В. Г. N-фенил-2-нафтиламин из цветов Burleurum aureum // Химия природных соединений. 1989. Т. 25. N 3. С. 377.
  4. Makarova L. E., Smirnov V. I., Klyba L. V., Petrova I. G., Dudareva L. V. Role of allelopathic compounds in the regulation and development of legume-rhizobial symbiosis // Applied Biochemistry and Microbiology. 2012. Vol. 48, no. 4. P. 355-362. https://doi.org/10.1134/S0003683812030064.
  5. Enikeev A. G., Semenov A. A., Permyakov A. V., Sokolova N. A., Gamburg K. Z., Dudareva L. V. Biosynsesis of ortho-phthalic acid esters in plant and cell cultures // Applied Biochemistry and Microbiology. 2019. Vol. 55, no. 3. P. 282-285. https://doi.org/10.1134/S0003683819020066.
  6. Makarova L. E., Moritz А. S., Sokolova N. А., Petrova I. G., Semenov А. А., Dudareva L. V., et al. Degradation of N-phenyl-2-naphthylamine by Rhizobium leguminosarum bv. viciae, Pseudomonas syringae pv. pisi, and Clavibacter michiganensis sps. sepedonicus bacteria // Applied Biochemistry and Microbiology. 2020. Vol. 56, no. 2. P. 202-210. https://doi.org/10.1134/S0003683820010123.
  7. Макарова Л. Е., Мориц А. С., Соколова Н. А. Образование фталатов при деградации N-фенил-2-нафтиламина почвенными бактериями // Известия вузов. Прикладная химия и биотехнология. 2021. Т. 11. N 1. С. 107-115. https://doi.org/10.21285/2227-2925-2021-11-1-107-115.
  8. Novak K. Induction of phytoalexin in pea roots by Rhizobia // Development in Soil Science. 1989. Vol. 18. P. 63-66. https://doi.org/10.1016/S0166-2481(08)70197-1.
  9. Шафикова Т. Н., Омеличкина Ю. В., Еникеев А. Г., Бояркина С. В., Гвильдис Д. Э., Семенов А. А. Эфиры ортофталевой кислоты подавляют способность фитопатогенов образовывать биопленки // Доклады Академии наук. 2018. Т. 480. N 3. С. 381-383. https://doi.org/10.7868/S0869565218150264.
  10. Makarova L. E., Dudareva L. V., Petrova I. G., Vasil’eva G. G. Secretion of phenolic compounds into root exudates of pea seedlings upon inoculation with Rhizobium leguminosarum bv. vicea or Pseudomonas siringae pv. pisi. // Applied Biochemistry and Microbiology. 2016. Vol. 52, no. 2. P. 205-209. https://doi.org/10.1134/S0003683816020095.
  11. Проворов Н. А., Воробьев Н. И. Генетические основы эволюции растительно-микробного симбиоза: монография. СПб.: Информ-Навигатор, 2012. 400 с.
  12. Melnykova N. M., Mykhalkiv L. M., Omelchuk S. V., Beregovenko S. K. Rhizosphere microorganisms as a factor influencing the rhizobia-legume symbiosis // Plant Physiology and Genetics. 2018. Vol. 50, no. 4. P. 299-321. https://doi.org/10.15407/frg2018.04.299.
  13. Акимова Г. П., Верхотуров В. В., Соколова М. Г., Белопухов С. Л. Модуляция про/антиоксидантной активности пероксидазы в корнях проростов гороха, инокулированных Rhizobium и Azotobacter // Известия Тимирязевской сельскохозяйственной академии. 2019. N 1. С. 138-145. https://doi.org/10.34677/0021-342X-2019-1-138-145.
  14. Makoi J. H. R., Ndakidemi P. A. Biological, ecological and agronomic significance of plant phenolic compounds in rhizosphere of the symbiotic legumes (review) // African Journal of Biotechnology. 2007. Vol. 6, no. 12. P. 1358-1368.
  15. Sweigard J. A., Matthews D. E., Vanetten H. D. Synthesis of the phytoalexin pisatin by a methyltransferase from pea // Plant Physiology. 1986. Vol. 80, no. 1. P. 277-279. https://doi.org/10.1104/pp.80.1.277.
  16. Vanetten H. D., Temporini E., Wassman C. Phytoalexin (and phytoanticipin) tolerance as a virulence trait: why is it not required by all pathogens? // Physiological and Molecular Plant Pathology. 2001. Vol. 68, no. 2. P. 1276-1283. https://doi.org/10.1006/pmpp.2001.0350.
  17. Carlson R. E., Dolphin D. H. Pisum sativum stress metabolites: two cinnamylphenols and 2’-methoxychalcone // Phytochemistry. 1982. Vol. 21, no. 7. P. 1733-1736. https://doi.org/10.1016/S0031-9422(82)85049-8.
  18. Altenburger R., Brack W., Greco W. R., Groot M., Jung K., Ovari A., et al. On the mode of action of N-phenyl-2-naphthylamine in plants // Environmental Science & Technology. 2006. Vol. 40, no. 19. P. 6163-6169. https://doi.org/10.1021/es060338e.
  19. Hauser R., Calafat A. M. Phthalates and human health // Occupational and Environmental Medicine. 2005. Vol. 62, no. 11. P. 806-818. https://doi.org/10.1136/oem.2004.017590.
  20. Kato-Noguchi H. Isolation and identification of an allelopathic substance in Pisum sativum // Phytochemistry. 2003. Vol. 62, no. 7. P. 1141-1144. https://doi.org/10.1016/S0031-9422(02)00673-8.
  21. Hartwig U. A., Josef C. M., Phillips D. A. Flavonoid released naturally from alfalfa seeds enhance growth rate of Rhizobium meliloti // Journal of Plant Physiology. 1991. Vol. 95, no. 3. P. 797-803. https://doi.org/10.1104/pp.95.3.797.
  22. Cruickshank I. A. M. Studies of phytoalexins. IY. The antimicrobial spectrum of pisatin // Australian Journal of Biological Sciences. 1962. Vol. 15, no. 5. P. 141-159. https://doi.org/10.1071/BI9620147.
  23. Parke D., Ornston L. N. Enzymes of the β-ketoadipate pathway are inducible in Rhizobium and Agrobacterium spp. and constitutive in Bradyrhizobium spp. // Journal of Bacteriology. 1986. Vol. 165, no. 1. P. 288-292. https://doi.org/10.1128/jb.165.1.288-292.1986.
  24. Пат. № 2231546, Российская Федерация, C12 N1/20//(C12 N1/20, C12 R1:065). Штамм бактерий AZ D10 VKM B-2272 Д, обладающий ростостимулирующими свойствами и устойчивый к дельтаметрину / О. Б. Вайшля, А. А. Бондаренко; заявитель и патентообладатель Томский государственный университет. Заявл. 28.08.2002; опубл. 27.06.2004.
  25. Marek E. V., Koslitz S., Weiss T., Fartasch M., Schlüter G., Käfferlein H. U., et al. Quantification of N-phenyl-2-naphthylamine by gas chromatography and isotope-dilution mass spectrometry and its percutaneous absorption ex vivo under workplace conditions // Archives of Toxicology. 2017. Vol. 91, no. 11. P. 3587-3596. https://doi.org/10.1007/s00204-017-2046-2.
  26. Alim Al-Bari M. A., Sayeed M. A., Rahman M. S., Mossadik M. A. Characterization and antimicrobial activities of a phenolic acid derivative produced by Streptomyces bangladeshiensis, a novel species collected in Bangladesh // Research Journal of Medical Sciences. 2006. Vol. 1, no. 2. P. 77-81.
  27. Пастухова Е. С., Егорова В. О., Соколова Н. А., Плотникова Е. Г. Бактерии-деструкторы ортофталевой кислоты, выделенные из отходов калийного производства // Вестник Пермского университета. Серия: Биология. 2010. N 3. С. 227-232.
  28. Kim S. M., Yoo J. A., Baek J. M., Cho K. H. Diethyl phthalate exposure is associated with embryonic toxicity, fatty liver changes, and hypolipidemia via impairment of lipoprotein functions // Toxicology in Vitro. 2015. Vol. 30, no. 1. P. 383-393. https://doi.org/10.1016/j.tiv.2015.09.026.
  29. Mathesius U., Bayliss C., Weinman J. J., Schlaman H. R. M., Spaink H. P., Rolfe B. G., et al. Flavonoids synthezed in cortical cells during nodule initiation are early developmental markers in white clover // Molecular Plant-Microbe Interactions. 1998. Vol. 11, no. 12. P. 1223-1232. http://dx.doi.org/10.1094/MPMI.1998.11.12.1223.

Supplementary files

Supplementary Files
Action
1. JATS XML


Согласие на обработку персональных данных

 

Используя сайт https://journals.rcsi.science, я (далее – «Пользователь» или «Субъект персональных данных») даю согласие на обработку персональных данных на этом сайте (текст Согласия) и на обработку персональных данных с помощью сервиса «Яндекс.Метрика» (текст Согласия).