Legume-rhizobial symbiosis: progress and prospects

Автор: Glyanko A.K.

Журнал: Журнал стресс-физиологии и биохимии @jspb

Статья в выпуске: 2 т.14, 2018 года.

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Data on the role of the legume-rhizobial symbiosis (LRS) in national economic and a brief history of the fundamental study of this unique biological phenomenon are summarized. The features of the formation of root nodules of determinant and indeterminant types are described. The physiological role of the rhizobial Nod factor in suppressing the defense system of a legume plant and the role of the plant's immune systems (MTI and ETI) in the rhizobial infection and the formation of LRS are discussed. Signal systems of a legume plant (Ca2+, NO-synthase, NADPH oxidase) and their components (ROS, RNS) and other signaling molecules involved and interacting in LRS onset are described. The necessity of studying the local and systemic resistsnce of the legume plant to the rhizobial infection is emphasized.

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Rhizobiaceae family, legume plants (fabaceae), legume-rhizobial symbiosis, root nodules, nod factor, plant immune systems (mti, eti), ros, rns, ca2+, h2o2, no, salicylic acid, local and systemic resistance, biotic stress

Короткий адрес: https://sciup.org/143165190

IDR: 143165190

Список литературы Legume-rhizobial symbiosis: progress and prospects

  • Akimova G.P., Sokolova M.G. (2012) Cytokinin content during early stages of legume-rhizobium symbiosis and effect of hypothermia. Russ. J. Plant Physiol. 59, 656-661
  • Appleby C.A. (1992) The origin and functions of haemoglobin in plants. Science Progress. 76, 365-398
  • Baron C., Zambryski P.C. (1995) The plant response in pathogenesis, symbiosis, and wounding: variations on a common theme? Annu. Rev. Genet. 29, 107-129
  • Barraso J.B., Valderrama R., Corpas F.J. (2013) Immmunolocalization of S-nitrosoglutathione, S-nitrosoglutathione reductase and tyrosine nitration in pea leaf organelles. Acta Physiol. Plant. 35, 2635-2640
  • Baudouin E., Pieuchot L., Engler G., Pauly N., Puppo A.(2006) Nitric oxide is formed in Medicago truncutula -Sinorhizobium meliloti functional nodules. Mol. Plant-Microbe Interac. 19, 970-975
  • Baxter A., Mittler R., Suzuki N. (2014) ROS as key players in plant stress signaling. J. Exp. Bot. 65, 1229-1240
  • Beatly P.H., Good A.G. (2011) Future prospects for cereals that fix nitrogen. Science. 333, 416-417
  • Bellin D., Asai S., Delledonne M., Yoshioka H. (2013) Nitric oxide as mediator for defense responses. Mol. Plant-Microbe Interac. 26, 271-277
  • Blilou I., Ocampo J., Garcia-Garrido J. (1999) Resistance of pea root to endomycorrhizal fungus or Rhizobium correlates with enhanced levels of endogenous salicylic acid. J. Exp. Bot. 50, 1663-1668
  • Brewin N.J. (1991) Development of the legume root nodules. Annu. Rev. Cell Biol. 7, 191-226
  • Boscari A., Del Giudice J., Ferrarini A., Venturini L., Zaffini A.L., Delledonne M., Puppo A. (2013) Expression dynamics of the Medicago truncatula transcriptome during the symbiotic interaction with Sinorhizobium meliloti: which role for nitric oxide? Plant Physiol. 161, 425-439
  • Bueno P., Soto M.J., Rodriguez-Rosales M.P., Sanjuan J., Olivares J., Donaire J.P. (2001) Time-course of lipoxygenase, antioxidant enzyme activities and H2O2 accumulation during the early stages of Rhizobium-legume symbiosis. New Phytol. 152, 91-96
  • Buffard D., Esnault R., Kondorosi A. (1996) Role of plant defense in alfalfa during symbiosis. Word J. Microbiol. Biotechnol. 12, 175-188
  • Corpas F.J., Barroso J.B. (2014). Peroxynitrite (ONOO-) is endogenously produced in Arabidopsis peroxisomes and is over producer under cadmium stress. Annals Bot. 113, 87-96
  • Cardenas L., Quinto C. (2008) Reactive oxygen species (ROS) as early signals in root hair cells responding to rhizobial nodulation factors. Plant Signal. Behav. 3, 1101-1102
  • Corpas F.J., del Rio L.A., Barroso J.B. (2013) Protein tyrosine nitration in higher plants under natural and stress conditions. Front. Plant Sci. 4, 29 DOI: 10.3389/fpls.2013.00029
  • Charpentier M., Oldroyd G. (2010) How close are we to nitrogen-fixing cereals? Curr. Opin. Plant Biol. 13, 556-564
  • Downie J.A. (2014) Calcium signals in plant immunity: a spiky issue. New Phytol. 204, 733-735
  • Deakin W.J., Broughton W.J. (2009) Simbiotic use of phatogenic strategies: rhizobial protein secretion systems. Nature Rev. Microbiol. 7, 312-320
  • Denarie J., Debelle F. (1996) Rhizobium lipochitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 65, 503-535
  • Djordjevic M.A., Gabriel D.W., Rolfe B.J. (1987) Rhizobium -the refined parasite avoid the host response? Annu.Rev. Phytopathol. 25, 145-168
  • Ehrhard D.W., Atkinson E.M., Long S.R. (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell. 85(5), 673-681
  • Ferguson B.J., Mathesius U. (2003) Signaling interactions during nodule development. J. Plant Growth Regul. 22, 47-72
  • Ferguson B.J., Indrasumunar A., Hayashi S., Lin M-H., Lin Y-H., Reid D.E., Gresshoff P.M. (2010) Molecular analysis of legume nodule development and autoregulation. J. Integr. Plant Biol. 52, 61-76
  • Ferguson B.J., Mathesius U. (2014) Phytohormone regulation of legume-rhizobia interactions. J. Chemical Ecology. 40, 770-790
  • Franssen H.J., Vijn I., Yang W.C., Bisseling T. (1992) Developmental aspects of the Rhizobium-legume symbiosis. Plant Mol. Biol. 19, 89-107
  • Fred E.B., Graul J. (1916) The effect of soluble nitrogenous salts on nodule formation. J. Amer. Soc. Agron. 8, 316-328
  • Gough C., Cullimore J. (2011) Lipochitooligosaccharide signaling in endosymbiotic plant-microbe interactions. Mol. Plant-Microbe Interac. 24, 867-878
  • Granqvist E., Sun J., den Camp R.O., Pujic P., Hill L., Normand P., Morris R.J., Downie J.A., Geurts R., Oldroyd G.E.D. (2015) Bacterial-induced calcium oscillations are common to nitrogen-fixing associations of nodulating legumes and non-legumes. New Phytol. 207, 551-558
  • Graham P.H, Vance C.P. (2003) Legumes: importance and constraints to greater use. Plant Physiol. 131, 872-877
  • Glyan’ko A.K., Makarova LE., Vasil’eva G.G., Mironova N.V. (2005) Possible involvement of hydrogen peroxide and salicylic acid in the legume-Rhizobium symbiosis. Biology Bulletin. 32, 245-249
  • Glyan’ko A.K., Mitanova N.B., Stepanov A.A. (2012) Influence of environmental factors on the generation of nitric oxide in the roots of etiolated pea seedlings. Appl. Biochem. Microbiol. 48, 83-89
  • Glyan’ko A.K. (2013) Initiation of synthesis of nitrogen oxide (NO) in the roots of etiolated pea seedlings under the influence of N-compounds//Biochemistry (Moskow), 78, 471-476
  • Glyan’ko A.K., Ischenko A.A., Stepanov A.V. (2014) Influence of calcium and rhizobial infection (Rhizobium leguminosarum) on the dynamics of the content of nitrogen oxide in the roots of etiolated pea seedlings (Pisum sativum L.) Appl. Biochem. Microbiol. 50, 652-657
  • Glyan’ko A.K. (Review) (2014a). N.A. Provorov, N.I. Vorob’ev Genetic foundations of the evolution of plant-microbial symbiosis/Ed. I.A. Tikhonovich/Bulletin of the Society of Physiologists of Russia. 29, 63-70
  • Glyan’ko A.K. (2014) The role of Nod factor Rhizobium in the induction of plant signal systems during the formation of legume-rhizobial symbiosis. Bulletin of Kharkiv. nat. agrarian un-ty. Ser. Biology. 3 (33), 6-14 (in Ukrainian)
  • Glyan’ko A.K. (2015) Phytohormones and nodule formation in legume plants. Bulletin of Kharkiv. nat. agrarian un-ty. Ser. Biology. 3 (36), 6-19 (in Ukrainian)
  • Glyan’ko A.K., Ischenko A.A. (2015) The role of cytokinin and auxin in the regulation of the nodulation process in legume plants. Journal of Stress Physiology and Biochemistry. 11(2), 16-27
  • Glyan’ko A.K. (2016) Defense systems of a legume plant in case of infection with rhizobia. Bulletin of Kharkiv. nat. agrarian un-ty. Ser. Biology. 1(37), 63-77 (in Ukrainian)
  • Glyan’ko A.K., Isсhenko A.A. (2017) Immunity of a leguminous plant infected by nodular bacteria Rhizobium spp. F. (Review). Appl. Biochem. Microbiol. 53, 140-148
  • Glyan’ko A.K., Ischenko A.A. (2017a) Reactive species of oxygen and nitrogen -possible mediators of systemic resistance in legumes under the influence of the rhizobial infection. Bulletin of Kharkiv. nat. agrarian un-ty. Ser. Biology. 1(40), 9-20 (in Ukrainian)
  • Gage D.J. (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol. Mol. Biol. Rev. 68, 280-300
  • Gamas P., de Billy F., Truchet G. (1998) Symbiosis-specific expression of two Medicago truncatula nodulin genes, MtN1 and Mt13, incoding products gomologous to plant defense proteins. Mol. Plant-Microbe Interac. 11, 393-403
  • Glyan’ko A.К., Ischenko A.A., Stepanov A.V. (2014) Influence of calcium and rhizobial infections (Rhizobium leguminosarum) on the dynamics of nitric oxide (NO) content in roots of etiolated pea (Pisum sativum L.) seedlings. Applied Biochem. Microbiol. 50, 652-657
  • Gourion B., Berrabah F., Ratet P., Stacey G. (2015) Rhizobium-legume symbioses: the crucial role of plant immunity. Trends Plant Sci. 20, 186-194
  • Hayashi T., Banda M., Kouchi H., Hayashi M., Imaizumi-Anraku H. (2010) A dominant function of CCaMK in intracellular accommodation of bacterial and fungal endosymbionts. Plant J. 63, 141-154
  • Heidstra R., Bisseling T. (1996) Nod factor-induced host responses and mechanisms of Nod factor perception. New Phytol. 133, 25-43
  • Herouart D., Baudouin E., Frendo P., Harrison J., Santos R., Jamet A., Van de Sype G., Touati D., Puppo A. (2002) Reactive oxygen species, nitric oxide and glutathione: key role in the establishment of the legume-Rhizobium symbiosis//Plant Physiol. Biochem. 40, 619-624
  • Hichri I., Bosscari A., Castella C., Rovere M., Puppo A., Brouquisse R. (2015). Nitric oxide: a multifaceted regulator of the nitrogen-fixing symbiosis. J. Exp. Bot. 66, 2877-2887
  • Hirsch A.M. (1992) Developmental biology of legume nodulation. New Phytol. 122, 211-237
  • Klatt P., Lamas S. (2000) Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur. J. Biochem. 267, 4928-4944
  • Kubienova L., Ticha T., Jahnova J., Luhova L., Mieslerova B., Pettrivalsky M. -(2014) Effect of abiotic stress stimuli on S-nitrosoglutathione reductase in plants. Planta. 239, 139-146
  • Kretovich V.L. (1997). Biochemistry of air nitrogen assimilation by plants. Moscow: Nauka, 486 p
  • Karpets Yu.V., Kolupaev Yu.E. (2007) Functional interaction of nitrogen oxide with reactive oxygen species and calcium ions in the formation of adaptive plant reactions. Bulletin of Kharkiv. nat. agrarian un-ty. Ser. Biology. 2 (41), 6-31 (in Ukrainian)
  • Kolupaev Yu.E. (2007) Calcium and stress reactions of plants. Bulletin of Kharkiv. nat. agrarian un-ty. Ser. Biology. 1(10), 24-41 (in Ukrainian)
  • Kolupaev Yu.E., Karpets Yu.V., Yastreb T.O., Lugovaya A.A. (2016) Signal mediators in the realization of the physiological effects of stressful phytohormones. Bulletin of Kharkiv. nat. agrarian un-ty. Ser. Biology. 1(37), 42-62 (in Ukrainian)
  • Kots S.Ya., Morgun V.V., Patyka V.F. et al. (2010, 2011) Legume-rhizobial symbiosis, Vol. 1, 508 p.;Vol. 2, 524 p.; Kiev: Logos (in Ukrainian)
  • Krugova E.D. (2009) Specific strategies of nodule and phytopathogenic bacteria in plant infection. Physiology and biochemistry of cult. plants. 41, 3-15 (in Ukrainian)
  • Kuznetsova I.G., Sazonova A.L., Safronova V.I., Pinaev A.G., Verkhozina A.V., Tikhomirova N.Yu., Osledkin Yu.S., Belimov A.A. (2015) Genetic diversity of microsymbionts of Baikal species of vetchling (Lathyrus), pea (Vicia), oxytrope (Oxytropis) and loco (Astragalus). Agricultural Biology (Sel’skohozyastvennaya Biologiya). 50(3), 345-352
  • Long S.R. (2001) Genes and signals in the rhizobium-legume symbiosis. Plant Physiol. 125, 69-72
  • Leon J., Lawton M.A., Raskin I. (1995). Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol. 105, 1673-1678
  • Lohar D.P., Haridas S., Gantt J.S., VandenBosch K. A. (2007) A transient decrease in reactive oxygen species in roots leads to root hair deformation in the legume-rhizobia symbiosis. New Phytol. 173, 39-49
  • Liang Y., Cao Y., Tanaka K., Thibivilliers S., Wan J., Choi J., ho Kang C., Qiu J., Stacey G. (2013) Non legumes respond to rhizobial Nod factors by suppressing the innate immune response. Science. 341, 1384-1387
  • Long S.R. (1996) Rhizobium symbiosis: Nod factors in perspective. Plant Cell. 8, 1885-1898.
  • Martinez-Abarka F., Herrera-Cervera J.A., Bueno P., Sanjuan J., Bisseling T., Olivares J. (1998) Involvement of salicylic acid in the establishment of the Rhizobium meliloti-alfalfa symbiosis. Mol. Plant Microbe Interac. 11, 153-155
  • Martinez-Hidalgo P., Hirsch A.M. (2017) The nodule microbiome: N2-fixing rhizobia do not live alone. Phytobiomes J. 1 (2), 70-82
  • Meyer C., Lea U.S., Provan F., Kaizer W.M., Lillo C. (2005). Is nitrate reductase a major player in the plant NO (nitric oxide) game? Photosynth. Res. 83, 181-189
  • Meilhoc E., Boscan A., Bruand C., Puppo A.,Brouquisse R. (2011) Nitric oxide in legume-rhizobium symbiosis. Plant Science. 181, 573-581
  • Maksimov I.V., Cherepanov E.A. (2006) Pro/antioxidant system and plant resistance to pathogens. Biology Bulletin Reviews. 126, 250-261
  • Mishustin E.N., Shilnikova V.K. (1968) Biological fixation of atmospheric nitrogen. Moscow: Nauka, 531 p.
  • Mishustin E.N. (1972) Microorganisms and productivity of agriculture. Moskow: Nauka, 343 p.
  • Mishustin E.N., Shilnikova V.K. (1973) Nodule bacteria and inoculation process. Moscow: Nauka, 288 p.
  • Mitanova N.B., Glyan’ko A.K., Vasilieva G.G. (2006) Influence of nitrogen compounds on the adhesion and penetration of nodule bacteria into root tissues and the growth of etiolated pea seedlings. Agrochemistry (Agrokhimiya). 10, 52-55
  • Molodchenkova O.O. (2001) Assumed functions of salicylic acid in plants. Physiology and biochemistry cult. plants. 33, 463-473 (in Ukrainian)
  • Mostofa M.G., Fujita M., Tran L.S.P. (2015). Nitric oxide mediates hydrogen peroxide-and salicylic acid-induced salt tolerance in rice (Oriza sativa) seedlings. Plant Growth Regul. 77, 265-277
  • Murray J.D. (2011) Invasion by invitation rhizobial infection in legumes//Mol. Plant-Microbe Interac. 24, 631-639
  • Ortega-Galisteo A.P., Rodriguez-Serrano M., Pazmino D.M., Gupta D.K., Sandalio L.M., Romero-Puertas M.S. (2012) S-Nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. J. Exp. Bot. 63, 2089-2103
  • Oldroyd G.E.D., Murray J.D., Poole P.S., Downie A. (2011) The rules of engagement in the legume-rhizobial symbiosis. Annu. Rev. Genet. 45, 119-144
  • Oldroyd G.E.D., Downie J.A (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59, 519-546
  • Park S.W., Kaimoyo E., Kumar D., Mosher S., Klessing D.F. (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science. 318, 113-116
  • Pallas J.A., Paiva N.L., Lamb C., Dixon R.A. (1996) Tobacco plants epigenetically suppressed in phenylalanine ammonia-lyase expression do not develop systemic acquired resistance in response to infection by tobacco mosaic virus. Plant J. 10, 281-293
  • Puppo A., Pauly N., Boscari A., Mandon K., Brouquisse R. (2013) Hydrogen peroxide and nitric oxide: key regulators of the legume -Rhizobium and mycorrhizal symbioses. Antioxidant Redox Signal. 18, 2202-2219
  • Provorov N.A., Vorob’ev N.I. (2012) Genetic foundations of the evolution of plant-microbial symbiosis. S. -Petersburg: Informnavigator, 400 p.
  • Rolfe B.G., Gresshoff P.M. (1988). Genetic analysis of legume nodule initiation. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39, 297-319
  • Rao M.V., Paliyath G., Ormrod D.P., Murr D.P., Watkins C.B. (1997) Influence of salicylic acid on H2O2 production, oxidative stress, and H2O2-metabolizing enzymes. Salicylic acid-mediated oxidative damage requires H2O2. Plant Physiol. 115, 137-149
  • Romero-Puertas M.S., Roddriguez-Serrano M., Sandalio L.M. (2013) Protein S-nytrosylation in plants under abiotic stress: an overview. Front. Plant Sci. 4: 373 DOI: 10.3389/fpls.2013.00373
  • Ryals J.A., Neuenschwander U.H., Willits M.G., Molina A., Steiner H.Y., Hunt M.D. (1996) Systemic acquired resistance. Plant Cell. 8, 1809-1819
  • Rhizobiaceae (2002) Molecular biology of bacteria interacting with plants. S.-Petersburg: Biont, 567 p.
  • Shaw S.L., Long S.R. (2003) Nod factor elicits two separable calcium responses in Medicago truncatula root hair cells. Plant Physiol. 131, 976-984
  • Spaink H.P. (1995) The molecular basis of infection and nodulation by rhizobia: the ins and outs of sympathogenesis. Annu. Rev. Phytopathol. 33, 345-368
  • Skorpil P., Broughton W.J. (2005) Molecular interaction between Rhizobium and legumes. In: Molecular Basis of Symbiosis. Ed. J. Overmann. Berlin-Heidelberg: Springer-Verlag, P. 143-165
  • Stacey G., McAlvin C.B., Sung-Yong Kim, Olivares J., Sato M.J. (2006) Effect of endogenous salicylic acid on nodulation in the model legumes Lotus japonicus and Medicago tranculata. Plant Physiol. 141, 1473-1481
  • Santos R., Herouart D., Sigaud S., Touati D., Puppo A. (2001) Oxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction. Mol. Plant-Microbe Interac. 14, 86-89
  • Sidorova K.K. (1981) Genetics of peas mutants. Novosibirsk: Nauka, 169 p.
  • Sidorova K.K., Shumnyj V.K. (1999) Genetics of symbiotic nitrogen fixation and selection bases for self-pollinating legumes (as in the case of Pisum sativum L.). Genetics (Genetika). 35, 1550-1557
  • Sidorova K.K., Shumnyj V.K., Nazarov V.M. (2006). Symbiotic nitrogen fixation: genetic, selection and ecology-agrochemical aspects. Novosibirsk: Akad. publishing house "Geo", 134 p.
  • Sidorova K.K., Shumnyj V.K. (2003) Creation and genetic study of the collection of symbiotic mutants of peas (Pisum sativum L.). Genetics (Genetika). 39, 501-509
  • Sidorova K.K., Shumny V.K., Vlasova E.Yu., Glyanenko M.N., Mishchenko T.M., Maystrenko G.G. (2010) Symbiogenetics and selection of macrosymbiont for increasing nitrogen fixation as in the case of peas (Pisum sativum L.)//VOGiS Herald. (Vestnik Vserossijskogo Obschestva Genetikov i Selektsionerov) 14, 357-374
  • Shevchuk V.Ye. (1979). Legumes and soil fertility. Irkutsk: East Siberian Book Publishing House, 98 p.
  • Shumnyj V.K., Sidorova K.K., Klevenskaya I.L. (1991) Biological fixation of nitrogen. Novosibirsk: Nauka, 270 p.
  • Sagi M., Fluhr R. (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol. 141, 336-340
  • Shah J., Zeier J. (2013) Long-distance communication and signal amplification in the systemic acquired resistance. Front. Plant Sci. 4: 30 DOI: 10.3389/fpls.2013.0003
  • Scheler C., Durner J., Astier J. (2013) Nitric oxide and reactive oxygen species in plant biotic interactions. Curr. Opin. Plant Biol. 16, 534-539
  • Scott P., Pregelj L., Chen N., Hadler J., Djordjevic M., Gresshoff P. (2008) Pongamia pinnata: an untapped resource for the biofuels industry of the future. BioEnergy Res. 1, 2-11
  • Shimoda Y., Nagata M., Suzuki A., Abe M., Sato S., Kato T., Tabata S., Higashi S., Uchiumi T. (2005) Symbiotic rhizobium and nitric oxide induce gene expression of non-symbiotic hemoglobin in Lotus japonicus. Plant Cell Physiol. 46, 99-107
  • Singh S., Parniske M. (2012) Activation of calcium -and calmodulin -dependent protein kinase (CCaMK), the central regulator of plant root endosymbiosis. Curr. Opin. Plant Biol. 15, 444-453
  • Timmers A.C., Soupene E., Auriac M.C., de Billy F., Vasse J., Boistard P., Truchet G. (2000) Saprophytic intracellular rhizobia in alfalfa nodules. Mol. Plant-Microbe Interac. 13, 1204-1213
  • Tarchevsky I.A. (2002) Signaling systems of plant cells. Moscow: Nauka, p.103-113. Tikhonovich I.A., Provorov N.A. (2009) Symbiosis of plants and microorganisms. Molecular genetics of agrosystems of the future. S.-Petersburg: Publishing House of S-Petersburg University, 210 p.
  • Tsyganova A.V., Kitaeva A.B., Brevin N.J., Tsyganov V.E. (2011) Cellular mechanisms of the development of symbiotic nodules in legumу plants. Agrocultural Biology (Sel’skohozyastvennaya Biologiya). 3, 34-41
  • Vasse J., de Billy F., Truchet J. (1993). Abortion of infection during the Rhizobium meliloti-alfalfa symbiotic interaction is accompanied by hypersensitive reaction. Plant J. 4, 555-566
  • Vernooij B., Friedrich L., Morse A., Reist R., Kolditz-Jawhar R., Ward E. (1994) Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance. Plant Cell. 6, 959-965
  • Vasil’eva G.G., Mironova N.V., Glyan’ko A.K., Shepot’ko L.N. (2001) Generation of superoxide radicals in pea seedlings during inoculation with nitrogen-fixing bacteria of different compatibility//Agricultural Biology (Sel’skohozyastvennaya Biologiya). 3, 79-83
  • Vorob’ev V.A. (1998) Symbiotic nitrogen fixation and temperature. Novosibirsk: Nauka, 126 p.
  • Vul'f E.V., Maleeva O.F. (1969) Directory. World resources of useful plants. Leningrad: Nauka, p. 221-222
  • Wang Y., Loake G.J., Chu C. (2013). Cross-talk of nitric oxide and reactive oxygen species in plant programmed cell death. Front. Plant Sci. 4: 314 DOI: 10.3389/fpls.2013.00314
  • Wang P., Du Y., Ren D., Song C.P. (2010) Hydrogen peroxide-mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. Plant Cell. 22, 2981-2998
  • Yakovleva Z.M. (1975) Bacteroides of nodule bacteria. Novosibirsk: Nauka, 171 p.
  • Yun B.W., Feechan A., Yin M., Saidi N.B., Le Bihan T., Yu M., Moore J.W., Kang J.G., Kwon E., Spoel S.H., Pallas J.A., Loake G.J. (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature. 478, 264-268
  • Yamamoto Y., Kanayama Y. (1990) Inhibition of nitrogen fixation in soybean plants supplied with nitrate. II. Accumulation and properties of nitrosyllehemoglobin in nodules. Plant Cell Physiol. 31, 207-214
  • Yamamoto Y., Watanabe I., Kanayama Y. (1990). Inhibition of nitrogen fixation in soybean plants supplied with nitrate. 1. Nitrite accumulation and formation of nitrosylleghemoglobin in nodules. Plant Cell Physiol. 31, 341-346
  • Yu M., Lamatina L., Spoel S.H., Loake G.J. (2014) Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytol. 202, 1142-1156
  • Zhao J., Fujita K., Sakai K. (2007) Reactive oxygen species, nitric oxide, and their interactions play different roles in Cupressus lusitanica cell death and phytoalexin biosynthesis. New Phytol. 175, 215-229
  • Zaninotto F., la Camera S., Polverari A., Delledonne M. (2006) Cross talk between reactive nitrogen and oxygen species during the hypersensitive disease resistance response. Plant Physiol. 141, 379-383
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