vavilovВавиловский журнал генетики и селекцииVavilov Journal of Genetics and Breeding2500-3259Institute of Cytology and Genetics of Siberian Branch of the RAS10.18699/VJGB-22-58vavilov-3440Research ArticleМАТЕРИАЛЫ КОНФЕРЕНЦИИ «МЕХАНИЗМЫ АДАПТАЦИИ МИКРООРГАНИЗМОВ», ИРКУТСКВлияние ионов меди на ассоциации бактерий рода Azospirillum с проростками пшеницы (Triticum aestivum L.)Effect of copper ions on the associations of Azospirillum bacteria with wheat seedlings (Triticum aestivum L.)https://orcid.org/0000-0003-1927-918XМуратоваА. Ю.MuratovaA. Yu.

Саратов

Saratov

muratova_a@ibppm.ruhttps://orcid.org/0000-0002-8814-6949ЛюбуньЕ. В.LyubunE. V.

Саратов

Saratov

https://orcid.org/0000-0002-0021-4936ГолубевС. Н.GolubevS. N.

Саратов

Saratov

https://orcid.org/0000-0003-4501-4046ТурковскаяО. В.TurkovskayaO. V.

Саратов

Saratov

Институт биохимии и физиологии растений и микроорганизмов – обособленное структурное подразделение Федерального исследовательского центра «Саратовский научный центр Российской академии наук»РоссияInstitute of Biochemistry and Physiology of Plants and Microorganisms – Subdivision of the Saratov Federal Scientific Centre of the Russian Academy of SciencesRussian Federation202203092022265477485Copyright © Муратова А.Ю., Любунь Е.В., Голубев С.Н., Турковская О.В., 20222022Муратова А.Ю., Любунь Е.В., Голубев С.Н., Турковская О.В.Muratova A.Y., Lyubun E.V., Golubev S.N., Turkovskaya O.V.This work is licensed under a Creative Commons Attribution 4.0 License.https://vavilov.elpub.ru/jour/article/view/3440

Растительно-микробные ассоциации в результате своей физиолого-биохимической активности способны определять подвижность, биодоступность и накопление в растительных тканях тяжелых металлов. Указанные способности являются основой для использования растений и ассоциированных с ними микроорганизмов в разработке подходов, обеспечивающих как предотвращение попадания токсичных металлов в пищевые культуры, так и извлечение поллютантов из загрязненных земель с помощью технологий фиторемедиации. Успешное применение растительно-микробных комплексов в той или иной области зависит от изученности механизмов взаимодействий в системе конкретных организмов с тяжелыми металлами. Целью представленных исследований была оценка влияния ионов меди на эффекты бактеризации растений пшеницы мягкой (Triticum aestivum L.) тремя штаммами Azospirillum, обладающими свойствами стимуляции роста растений (PGPR). В ходе эксперимента анализировали ростовые параметры 14-суточных проростков пшеницы, содержание пигментов фотосинтеза, активность растительных оксидоредуктаз и аккумуляцию металла растительными тканями. Все штаммы в той или иной степени компенсировали фитотоксическое воздействие меди на развитие проростков и увеличивали ее аккумуляцию в корнях и побегах. Показано отчетливое усиление воздействия меди на фотосинтетический аппарат бактеризованных растений, выражающееся в изменении содержания основных пигментов, в первую очередь уменьшении хлорофилла b. Анализ активности растительных оксидоредуктаз (пероксидаз и фенолоксидаз) как участников физиологических ответов растений на стрессовые воздействия выявил их штаммоспецифичный характер и существенное влияние меди на бактеризованные растения. В целом полученные результаты показали отчетливое разноплановое влияние исследованных штаммов азоспирилл на физиологобиохимический статус растений пшеницы. Выявленный компенсаторный эффект бактерий на фитотоксическое воздействие меди и одновременно повышение ее накопления в растительных тканях могут рассматриваться как взаимоисключающие аспекты растениеводства, связанные с выращиванием пищевых растений на загрязненных тяжелыми металлами площадях.

The physiological and biochemical activity of plant–microbial associations enables them to determine the mobility, bioavailability, and accumulation of heavy metals in plant tissues. These abilities are the basis for the use of plants and their associated microorganisms in the development of approaches that ensure both the prevention of the ingress of toxic metals into food crops and the extraction of pollutants from polluted soils by using phytoremediation technologies. Whether plant–microbial complexes are used successfully depends on the knowledge of how specific organisms interact with heavy metals. We evaluated the effect of copper ions on common wheat (Triticum aestivum L.) inoculated with three plant-growth-promoting rhizobacteria (PGPR) of the genus Azospirillum. We analyzed the growth variables of 14-day-old wheat seedlings, the content of photosynthesis pigments, the activity of plant oxidoreductases, and the accumulation of copper by plant tissues. All strains more or less compensated for copper toxicity to seedling development and increased metal accumulation in roots and shoots. Copper affected the photosynthetic apparatus of the inoculated plants, primarily by decreasing the content of chlorophyll b. An analysis of the activity of plant oxidoreductases (peroxidases and phenoloxidases), which are involved in the physiological responses of plants to pollutant stress, showed strain-specific dependence and a significant effect of copper on the inoculated plants. Overall, the obtained results clearly show that the effect of Azospirillum on the physiological and biochemical status of wheat is diverse. The compensatory effect of bacteria on copper toxicity and the simultaneous increase in metal accumulation in plant tissues can be considered as mutually exclusive crop-production aspects associated with the growing of food plants in heavy-metal-polluted areas.

AzospirillumTriticum aestivumмедьпроросткифотосинтетические пигментыпероксидазалакказатирозиназаAzospirillumTriticum aestivumcopperseedlingsphotosynthetic pigmentsperoxidaselaccasetyrosinaseThis work was carried out under research theme No. 121031700141-7ReferencesBashan Y., de-Bashan L.E. How the plant growth-promoting bacterium Azospirillum promotes plant growth – a critical assessment. Adv. Agron. 2010;108:77-136. DOI 10.1016/S0065-2113(10)08002-8.Bashan Y., de-Bashan L.E. How the plant growth-promoting bacterium Azospirillum promotes plant growth – a critical assessment. Adv. Agron. 2010;108:77-136. DOI 10.1016/S0065-2113(10)08002-8.Boleta E.H.M., Shitate Galindo F., Jalal A., Santini J.M.K., Rodrigues W.L., Lima B.H.D., Arf O., da Silva M.R., Buzetti S., Teixeira Filho M.C.M. Inoculation with growth-promoting bacteria Azospirillum brasilense and its effects on productivity and nutritional accumulation of wheat cultivars. Front. Sustain. Food Syst. 2020;4:607262. DOI 10.3389/fsufs.2020.607262.Boleta E.H.M., Shitate Galindo F., Jalal A., Santini J.M.K., Rodrigues W.L., Lima B.H.D., Arf O., da Silva M.R., Buzetti S., Teixeira Filho M.C.M. Inoculation with growth-promoting bacteria Azospirillum brasilense and its effects on productivity and nutritional accumulation of wheat cultivars. Front. Sustain. Food Syst. 2020;4:607262. DOI 10.3389/fsufs.2020.607262.Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal. Biochem. 1976;72(1-2):248-254. DOI 10.1006/abio.1976.9999.Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal. Biochem. 1976;72(1-2):248-254. DOI 10.1006/abio.1976.9999.Breckle S.W. Growth under stress: heavy metals. In: Waisel Y., Kafkafi U. (Eds.) Plant Roots: The Hidden Half. N.Y.: Marsel Dekker Inc., 1991;351-373.Breckle S.W. Growth under stress: heavy metals. In: Waisel Y., Kafkafi U. (Eds.) Plant Roots: The Hidden Half. N.Y.: Marsel Dekker Inc., 1991;351-373.Caiola M.G., Canini A., Botta A.L., Del Gallo M. Localization of Azospirillum brasilense Cd in inoculated tomato (Lycopersicon esculentum Mill.) roots. Ann. Microbiol. 2004;54(4):365-380.Caiola M.G., Canini A., Botta A.L., Del Gallo M. Localization of Azospirillum brasilense Cd in inoculated tomato (Lycopersicon esculentum Mill.) roots. Ann. Microbiol. 2004;54(4):365-380.Caverzan A., Casassola A., Brammer S.P. Antioxidant responses of wheat plants under stress. Genet. Mol. Biol. 2016;39(1):1-6. DOI 10.1590/1678-4685-GMB-2015-0109.Caverzan A., Casassola A., Brammer S.P. Antioxidant responses of wheat plants under stress. Genet. Mol. Biol. 2016;39(1):1-6. DOI 10.1590/1678-4685-GMB-2015-0109.Criquet S., Joner E., Leglize P., Leyval C. Anthracene and mycorrhiza affect the activity of oxidoreductases in the roots and the rhizosphere of lucerne (Medicago sativa L.). Biotechnol. Lett. 2000;22:1733-1737. DOI 10.1023/A:1005604719909.Criquet S., Joner E., Leglize P., Leyval C. Anthracene and mycorrhiza affect the activity of oxidoreductases in the roots and the rhizosphere of lucerne (Medicago sativa L.). Biotechnol. Lett. 2000;22:1733-1737. DOI 10.1023/A:1005604719909.Dang V.B.H., Doan H.D., Dang-Vu T., Lohi A. Equilibrium and kinetics of biosorption of cadmium (II) and copper (II) ions by wheat straw. Biores. Technol. 2009;100(1):211-219. DOI 10.1080/19443994.2012.691745.Dang V.B.H., Doan H.D., Dang-Vu T., Lohi A. Equilibrium and kinetics of biosorption of cadmium (II) and copper (II) ions by wheat straw. Biores. Technol. 2009;100(1):211-219. DOI 10.1080/19443994.2012.691745.de Oliveira Pinheiro R., Boddey L.H., James E.K., Sprent J., Boddey R. Adsorption and anchoring of Azospirillum strains to roots of wheat seedlings. Plant Soil. 2002;246(2):151-166. DOI 10.1023/A:1020645203084.de Oliveira Pinheiro R., Boddey L.H., James E.K., Sprent J., Boddey R. Adsorption and anchoring of Azospirillum strains to roots of wheat seedlings. Plant Soil. 2002;246(2):151-166. DOI 10.1023/A:1020645203084.Dos Santos F.N., Hayashi Sant’ A.F., Massena R.V., Ambrosini A., Gazolla V.C., Rothballer M., Schwab S., Baura V.A., Balsanelli E., Pedrosa F.O., Pereira P.L.M., de Souza E.M., Hartmann A., Cassan F., Zilli J.E. Genome-based reclassification of Azospirillum brasilense Sp245 as the type strain of Azospirillum baldaniorum sp. nov. Int. J. Syst. Evol. Microbiol. 2020;70:6203-6212. DOI 10.1099/ijsem.0.004517.Dos Santos F.N., Hayashi Sant’ A.F., Massena R.V., Ambrosini A., Gazolla V.C., Rothballer M., Schwab S., Baura V.A., Balsanelli E., Pedrosa F.O., Pereira P.L.M., de Souza E.M., Hartmann A., Cassan F., Zilli J.E. Genome-based reclassification of Azospirillum brasilense Sp245 as the type strain of Azospirillum baldaniorum sp. nov. Int. J. Syst. Evol. Microbiol. 2020;70:6203-6212. DOI 10.1099/ijsem.0.004517.El-Samad A.H.M. The biphasic role of cupper and counteraction with Azospirillum brasilense application on growth, metabolities, osmotic pressure and mineral of wheat plant. Am. J. Plant Sci. 2017;8: 1182-1195. DOI 10.4236/AJPS.2017.85078.El-Samad A.H.M. The biphasic role of cupper and counteraction with Azospirillum brasilense application on growth, metabolities, osmotic pressure and mineral of wheat plant. Am. J. Plant Sci. 2017;8: 1182-1195. DOI 10.4236/AJPS.2017.85078.Fukami J., Cerezini P., Hungria M. Azospirillum: benefits that go far beyond biological nitrogen fixation. AMB Express. 2018;8(1):73. DOI 10.1186/s13568-018-0608-1.Fukami J., Cerezini P., Hungria M. Azospirillum: benefits that go far beyond biological nitrogen fixation. AMB Express. 2018;8(1):73. DOI 10.1186/s13568-018-0608-1.Galindo F.S., Rodrigues W.L., Biagini A.L.C., Fernandes G.C., Baratella E.B., da Silva C.A., Jr, Buzetti S., Teixeira Filho M.C.M. Assessing forms of application of Azospirillum brasilense associated with silicon use on wheat. Agronomy. 2019;9(11):678. DOI 10.3390/agronomy9110678.Galindo F.S., Rodrigues W.L., Biagini A.L.C., Fernandes G.C., Baratella E.B., da Silva C.A., Jr, Buzetti S., Teixeira Filho M.C.M. Assessing forms of application of Azospirillum brasilense associated with silicon use on wheat. Agronomy. 2019;9(11):678. DOI 10.3390/agronomy9110678.Hoagland D.R., Arnon D.I. The Water-Culture Method for Growing Plants without Soil. Berkeley: Univ. of California, 1950;347:8.Hoagland D.R., Arnon D.I. The Water-Culture Method for Growing Plants without Soil. Berkeley: Univ. of California, 1950;347:8.Huang X.D., El-Alawi Y., Penrose D.M., Glick B.R., Greenberg B.M. Responses of three grass species to creosote during phytoremediation. Environ. Pollut. 2004;130(3):453-463. DOI 10.1016/j.envpol.2003.12.018.Huang X.D., El-Alawi Y., Penrose D.M., Glick B.R., Greenberg B.M. Responses of three grass species to creosote during phytoremediation. Environ. Pollut. 2004;130(3):453-463. DOI 10.1016/j.envpol.2003.12.018.Kamnev A.A., Tugarova A.V., Antonyuk L.P. Endophytic and epiphytic strains of Azospirillum brasilense respond differently to heavy metal stress. Microbiology. 2007;76(6):809-811. DOI 10.1134/S0026261707060239.Kamnev A.A., Tugarova A.V., Antonyuk L.P. Endophytic and epiphytic strains of Azospirillum brasilense respond differently to heavy metal stress. Microbiology. 2007;76(6):809-811. DOI 10.1134/S0026261707060239.Kamnev A.A., Tugarova A.V., Antonyuk L.P., Tarantilis P.A., Polissiou M.G., Gardiner P.H.E. Effects of heavy metals on plant-associated rhizobacteria: comparison of endophytic and non-endophytic strains of Azospirillum brasilense. J. Trace Elem. Med. Biol. 2005; 19(1):91-95. DOI 10.1016/j.jtemb.2005.03.002.Kamnev A.A., Tugarova A.V., Antonyuk L.P., Tarantilis P.A., Polissiou M.G., Gardiner P.H.E. Effects of heavy metals on plant-associated rhizobacteria: comparison of endophytic and non-endophytic strains of Azospirillum brasilense. J. Trace Elem. Med. Biol. 2005; 19(1):91-95. DOI 10.1016/j.jtemb.2005.03.002.Larionov М.V., Larionov N.V. Characteristics of accumulation of heavy metals in soil ecosystems of Saratov Volga river region. Vestnik Orenburgskogo Gosudarstvennogo Universiteta = Vestnik of the Orenburg State University. 2010;1(107):110-114. (in Russian) Leonowicz A., Grzywnowicz K. Quantitative estimation of laccase forms in somewhite-rot fungi using syringaldazine as a substrate. Enzyme Microb. Technol. 1981;3:55-58. DOI 10.1016/0141-0229(81)90036-3.Larionov М.V., Larionov N.V. Characteristics of accumulation of heavy metals in soil ecosystems of Saratov Volga river region. Vestnik Orenburgskogo Gosudarstvennogo Universiteta = Vestnik of the Orenburg State University. 2010;1(107):110-114. (in Russian) Leonowicz A., Grzywnowicz K. Quantitative estimation of laccase forms in somewhite-rot fungi using syringaldazine as a substrate. Enzyme Microb. Technol. 1981;3:55-58. DOI 10.1016/0141-0229(81)90036-3.Liu Y., Chen Y., Yang Y., Zhang Q., Fu B., Cai J., Guo W., Shi L., Wu J., Chen Y. A thorough screening based on QTLs controlling zinc and copper accumulation in the grain of different wheat genotypes. Environ. Sci. Pollut. Res. 2021;28:15043-15054. DOI 10.1007/s11356-020-11690-3.Liu Y., Chen Y., Yang Y., Zhang Q., Fu B., Cai J., Guo W., Shi L., Wu J., Chen Y. A thorough screening based on QTLs controlling zinc and copper accumulation in the grain of different wheat genotypes. Environ. Sci. Pollut. Res. 2021;28:15043-15054. DOI 10.1007/s11356-020-11690-3.Lyubun Y., Muratova A., Dubrovskaya E., Sungurtseva I., Turkovskaya O. Combined effects of cadmium and oil sludge on sorghum: growth, physiology, and contaminant removal. Environ. Sci. Pollut. Res. 2020;27:22720-22734. DOI 10.1007/s11356-020-08789-y.Lyubun Y., Muratova A., Dubrovskaya E., Sungurtseva I., Turkovskaya O. Combined effects of cadmium and oil sludge on sorghum: growth, physiology, and contaminant removal. Environ. Sci. Pollut. Res. 2020;27:22720-22734. DOI 10.1007/s11356-020-08789-y.Medvedev I.F., Derevyagin S.S. Heavy Metals in Ecosystems. Saratov: Rakurs Publ., 2017. (in Russian)Medvedev I.F., Derevyagin S.S. Heavy Metals in Ecosystems. Saratov: Rakurs Publ., 2017. (in Russian)Michaud A.M., Bravin M.N., Galleguillos M., Hinsinger P. Copper uptake and phytotoxicity as assessed in situ for durum wheat (Triticum turgidum durum L.) cultivated in Cu-contaminated, former vineyard soils. Plant Soil. 2007;298(1-2):99-111. DOI 10.1007/s11104-007-9343-0.Michaud A.M., Bravin M.N., Galleguillos M., Hinsinger P. Copper uptake and phytotoxicity as assessed in situ for durum wheat (Triticum turgidum durum L.) cultivated in Cu-contaminated, former vineyard soils. Plant Soil. 2007;298(1-2):99-111. DOI 10.1007/s11104-007-9343-0.Nadeem S.M., Naveed M., Ahmad M., Zahir Z.A. Rhizosphere bacteria for crop production and improvement of stress tolerance: mechanisms of action, applications, and future prospects. In: Plant Microbes Symbiosis: Applied Facets. India: Springer, 2015;1-36. DOI 10.1007/978-81-322-2068-8_1.Nadeem S.M., Naveed M., Ahmad M., Zahir Z.A. Rhizosphere bacteria for crop production and improvement of stress tolerance: mechanisms of action, applications, and future prospects. In: Plant Microbes Symbiosis: Applied Facets. India: Springer, 2015;1-36. DOI 10.1007/978-81-322-2068-8_1.Pichhode M., Nikhil K. Effect of copper mining dust on the soil and vegetation in India: a critical review. Int. J. Mod. Sci. Eng. Technol. 2015;2(2):73-76.Pichhode M., Nikhil K. Effect of copper mining dust on the soil and vegetation in India: a critical review. Int. J. Mod. Sci. Eng. Technol. 2015;2(2):73-76.Prasad D.D.K., Prasad A.R.K. Altered 5-aminolevulinic acid metabolism by lead and mercury in germinating seedlings of Bajra (Pennisetum typhoideum). J. Plant Physiol. 1987;127:241-249. DOI 10.1007/BF02702668.Prasad D.D.K., Prasad A.R.K. Altered 5-aminolevulinic acid metabolism by lead and mercury in germinating seedlings of Bajra (Pennisetum typhoideum). J. Plant Physiol. 1987;127:241-249. DOI 10.1007/BF02702668.Prasad M.N.V., Strzalka K. Impact of heavy metals on photosynthesis. In: Prasad M.N.V., Hagemeyer J. (Eds.) Heavy Metal Stress in Plants: From Molecules to Ecosystems. Berlin: Springer, 1999;117-138. DOI 10.1007/978-3-662-07745-0_6.Prasad M.N.V., Strzalka K. Impact of heavy metals on photosynthesis. In: Prasad M.N.V., Hagemeyer J. (Eds.) Heavy Metal Stress in Plants: From Molecules to Ecosystems. Berlin: Springer, 1999;117-138. DOI 10.1007/978-3-662-07745-0_6.Quartacci M.F., Pinzino C., Sgherri C.L.M., Dalla Vecchia F., Navari-Izzo F. Growth in excess copper induces changes in the lipid composition and fluidity of PSII-enriched membranes in wheat. Physiol. Plantarum. 2000;108:87-93. DOI 10.1034/j.1399-3054.2000.108001087.x.Quartacci M.F., Pinzino C., Sgherri C.L.M., Dalla Vecchia F., Navari-Izzo F. Growth in excess copper induces changes in the lipid composition and fluidity of PSII-enriched membranes in wheat. Physiol. Plantarum. 2000;108:87-93. DOI 10.1034/j.1399-3054.2000.108001087.x.Rai R., Agrawal M., Agrawal S.B. Impact of heavy metals on physiological processes of plants: with special reference to photosynthetic system. Ch. 6. In: Singh A., Prasad S.M., Singh R.P. (Eds.) Plant Responses to Xenobiotics. Singapore: Springer Nature, 2016;127-140. DOI 10.1007/978-981-10-2860-1_6.Rai R., Agrawal M., Agrawal S.B. Impact of heavy metals on physiological processes of plants: with special reference to photosynthetic system. Ch. 6. In: Singh A., Prasad S.M., Singh R.P. (Eds.) Plant Responses to Xenobiotics. Singapore: Springer Nature, 2016;127-140. DOI 10.1007/978-981-10-2860-1_6.Rais A., Jabeen Z., Shair F., Hafeez F.Y., Hassan M.N. Bacillus spp., a bio-control agent enhances the activity of antioxidant defense enzymes in rice against Pyricularia oryzae. PLoS One. 2017;12(11): e0187412. DOI 10.1371/journal.pone.0187412.Rais A., Jabeen Z., Shair F., Hafeez F.Y., Hassan M.N. Bacillus spp., a bio-control agent enhances the activity of antioxidant defense enzymes in rice against Pyricularia oryzae. PLoS One. 2017;12(11): e0187412. DOI 10.1371/journal.pone.0187412.Reis V., Baldani V.L.D., Baldani J.I. Isolation, identification and biochemical characterization of Azospirillum spp. and other nitrogenfixing bacteria. In: Cassán F., Okon Y., Creus C. (Eds.) Handbook for Azospirillum. Basel: Springer, 2015;10:978-983. DOI 10.1007/978-3-319-06542-7_1.Reis V., Baldani V.L.D., Baldani J.I. Isolation, identification and biochemical characterization of Azospirillum spp. and other nitrogenfixing bacteria. In: Cassán F., Okon Y., Creus C. (Eds.) Handbook for Azospirillum. Basel: Springer, 2015;10:978-983. DOI 10.1007/978-3-319-06542-7_1.Rothballer M., Schmid M., Hartmann A. In situ localization and PGPReffect of Azospirillum brasilense strains colonizing roots of different wheat varieties. Symbiosis. 2003;34:261-279.Rothballer M., Schmid M., Hartmann A. In situ localization and PGPReffect of Azospirillum brasilense strains colonizing roots of different wheat varieties. Symbiosis. 2003;34:261-279.Sayyad G., Afyuni M., Mousavi S.-F., Abbaspour K.C., Hajabbasi M.A., Richards B.K., Schulin R. Effects of cadmium, copper, lead, and zinc contamination on metal accumulation by safflower and wheat. Soil Sediment Contam. Int. J. 2009;18(2):216-228. DOI 10.1080/15320380802660248.Sayyad G., Afyuni M., Mousavi S.-F., Abbaspour K.C., Hajabbasi M.A., Richards B.K., Schulin R. Effects of cadmium, copper, lead, and zinc contamination on metal accumulation by safflower and wheat. Soil Sediment Contam. Int. J. 2009;18(2):216-228. DOI 10.1080/15320380802660248.Statsenko A.P., Tuzhilova L.I., Vyugovsky A.A. Plant peroxidases – markers of chemical pollution of natural environments. Vestnik Orenburgskogo Gosudarstvennogo Universiteta = Vestnik of the Orenburg State University. 2008;10(92):188-191. (in Russian)Statsenko A.P., Tuzhilova L.I., Vyugovsky A.A. Plant peroxidases – markers of chemical pollution of natural environments. Vestnik Orenburgskogo Gosudarstvennogo Universiteta = Vestnik of the Orenburg State University. 2008;10(92):188-191. (in Russian)Sullivan M.L. Beyond brown: polyphenol oxidases as enzymes of plant specialized metabolism. Front. Plant Sci. 2015;5:783. DOI 10.3389/fpls.2014.00783.Sullivan M.L. Beyond brown: polyphenol oxidases as enzymes of plant specialized metabolism. Front. Plant Sci. 2015;5:783. DOI 10.3389/fpls.2014.00783.Teixeira Filho M.C.M.T., Galindo F.S., Buzetti S., Santini J.M.K. Inoculation with Azospirillum brasilense improves nutrition and increases wheat yield in association with nitrogen fertilization. Ch. 6. In: Wanyera R., Owuoche J. (Eds.) Wheat Improvement, Management and Utilization. IntechOpen, 2017;99-114. DOI 10.5772/67638.Teixeira Filho M.C.M.T., Galindo F.S., Buzetti S., Santini J.M.K. Inoculation with Azospirillum brasilense improves nutrition and increases wheat yield in association with nitrogen fertilization. Ch. 6. In: Wanyera R., Owuoche J. (Eds.) Wheat Improvement, Management and Utilization. IntechOpen, 2017;99-114. DOI 10.5772/67638.Titov A.F., Kaznina N.M., Talanova V.V. Heavy Metals and Plants. Petrozavodsk: Karelian Research Centre of RAS, 2014. (in Russian)Titov A.F., Kaznina N.M., Talanova V.V. Heavy Metals and Plants. Petrozavodsk: Karelian Research Centre of RAS, 2014. (in Russian)Wang H., Zhong G., Shi G., Pan F. Toxicity of Cu, Pb, and Zn on seed germination and young seedlings of wheat (Triticum aestivum L.). In: Li D., Liu Y., Chen Y. (Eds.) Computer and Computing Technologies in Agriculture IV. CCTA 2010. IFIP Advances in Information and Communication Technology. Vol. 346. Berlin; Heidelberg: Springer, 2011;231-240. DOI 10.1007/978-3-642-18354-6_29.Wang H., Zhong G., Shi G., Pan F. Toxicity of Cu, Pb, and Zn on seed germination and young seedlings of wheat (Triticum aestivum L.). In: Li D., Liu Y., Chen Y. (Eds.) Computer and Computing Technologies in Agriculture IV. CCTA 2010. IFIP Advances in Information and Communication Technology. Vol. 346. Berlin; Heidelberg: Springer, 2011;231-240. DOI 10.1007/978-3-642-18354-6_29.Wang S., Wu W., Liu F., Liao R., Hu Y. Accumulation of heavy metals in soil-crop systems: a review for wheat and corn. Environ. Sci. Pollut. Res. 2017;24(18):15209-15225. DOI 10.1007/s11356-017-8909-5.Wang S., Wu W., Liu F., Liao R., Hu Y. Accumulation of heavy metals in soil-crop systems: a review for wheat and corn. Environ. Sci. Pollut. Res. 2017;24(18):15209-15225. DOI 10.1007/s11356-017-8909-5.Yaneva O.D. Mechanisms of bacterial resistance to heavy metal ions. Mikrobiologichnyi Zhurnal = Microbiological Journal. 2009; 71(6):54-65. (in Ukrainian)Yaneva O.D. Mechanisms of bacterial resistance to heavy metal ions. Mikrobiologichnyi Zhurnal = Microbiological Journal. 2009; 71(6):54-65. (in Ukrainian)Yang Y.-J., Cheng L.-M., Liu Z.-H. Rapid effect of cadmium on lignin biosynthesis in soybean roots. Plant Sci. 2007;172:632-639. DOI 10.1016/j.plantsci.2006.11.018.Yang Y.-J., Cheng L.-M., Liu Z.-H. Rapid effect of cadmium on lignin biosynthesis in soybean roots. Plant Sci. 2007;172:632-639. DOI 10.1016/j.plantsci.2006.11.018.Yruela I. Cooper in plants. Braz. J. Plant Physiol. 2005;17(1):145-156. DOI 10.1590/S1677-04202005000100012.Yruela I. Cooper in plants. Braz. J. Plant Physiol. 2005;17(1):145-156. DOI 10.1590/S1677-04202005000100012.

The authors declare that there are no conflicts of interest present.