doi: 10.15389/agrobiology.2018.1.3eng
UDC 631.461.52:581.557.2:577.175.19
Acknowledgements:
Supported financially by Russian Science Foundation (project ¹ 14-24-00135)
NEGATIVE HORMONAL REGULATION OF SYMBIOTIC NODULE
DEVELOPMENT. II. SALICILIC, JASMONIC AND ABSCISIC ACIDS
(review)
A.V. Tsyganova, V.E. Tsyganov
All-Russian Research Institute for Agricultural Microbiology, Federal Agency for Scientific Organizations, 3, sh. Podbel’skogo, St. Petersburg, 196608 Russia, e-mail tsyganov@arriam.spb.ru (✉ corresponding author)
ORCID:
Tsyganova A.V. orcid.org/0000-0003-3505-4298
Tsyganov V.E. orcid.org/0000-0003-3105-8689
Received September 5, 2016
As a result of interaction with rhizobia, legume plants are able to fix atmospheric nitrogen in symbiotic nodules. Development and functioning of symbiotic nodules are under strong host plant control, including phytohormonal regulation (B.J. Ferguson et al., 2014). Due to the fact that nodule formation is a highly energy-consuming process, nodule number is restricted by plant. The negative regulation of nodulation involves, along with ethylene (A.V. Tsyganova et al., 2015), also salicylic (P.C. Van Spronsen et al., 2003; G. Stacey et al., 2006), jasmonic (Sun et al., 2006) and abscisic (Ding et al., 2008) acids. It is important to note that all listed phytohormones act at the different stages of development and functioning of symbiotic nodules. The first negative effects of jasmonic and abscisic acids are related to the blocking of calcium oscillations (J. Sun et al., 2006; Y. Ding et al., 2008), induced by Nod factors (lipochitooligosaccharides synthesized by rhizobia and activating a program for the development of infection and nodule organogenesis). Calcium oscillations are also blocked by ethylene (G.E. Oldroyd et al., 2001). Salicylic, jasmonic and abscisic acids influence the further development of symbiosis, blocking both the growth of infection threads (through which the rhizobia penetrate into the root), and the formation of nodule primordia (T. Nakagawa et al., 2006; J. Sun et al., 2006; Y. Ding et al. 2008). For abscisic acid it was shown that its negative effect on the development of nodule primordia is mediated by the influence on cytokinin signal transduction pathway (Y. Ding et al., 2008). Salicylic, jasmonic and abscisic acids also negatively affect the nitrogen-fixing activity of the nodules, and for abscisic acid it has been shown that the negative effect is associated with the activation of the production of nitrogen monoxide NO (A. Tominaga ñ ñîàâò., 2010). Nevertheless, all these phytohormones can have a positive effect on the formation and functioning of nodules. For example, jasmonic acid activates the expression of rhizobial nod genes that control the synthesis of Nod factors (F. Mabood et al., 2006). It is interesting to note that for salicylic and abscisic acids a positive role in activating the defense mechanisms in plants under the action of stress factors has been shown, which leads to a decrease in their negative effect on the functioning of the nodules (F. Palma et al., 2013, 2014). Future studies of the interaction of ethylene, salicylic, jasmonic and abscisic acids in the negative regulation of the formation of nitrogen-fixing nodules are of great interest. Such studies should shed light on why several phytohormones are involved in negative regulation and what the specificity of each of them is. It is important to study the possibility of practical use of mutants with a lower level of any of the phytohormones (ethylene, salicylic, jasmonic and abscisic acids). Therefore, it seems promising to study the mutant enf1 (enhanced nitrogen fixation1), obtained on the model legume Lotus japonicus and characterized by an increased level of nitrogen fixation (A. Tominaga et al., 2009). At the same time, it should be considered that a change in the level of a certain phytohormone can have a negative impact both on the development of the plant and its response to abiotic and biotic stresses.
Keywords: plant-microbe interactions, legume-rhizobial symbiosis, symbiotic nodule, phytohormones.
REFERENCES
- Tsyganova V.A., Tsyganov V.E. Uspekhi sovremennoi biologii, 2012, 132(2): 211-222 (in Russ.).
- Tsyganova A.V., Kitaeva A.B., Brevin N.Dzh., Tsyganov V.E. [Cellular mechanisms of nodule development in legume plants. Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2011, 3: 34-40 (in Russ.).
- Oldroyd G.E. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol., 2013, 11(4): 252-263 CrossRef
- Hause B., Schaarschmidt S. The role of jasmonates in mutualistic symbioses between plants and soil-born microorganisms. Phytochemistry, 2009, 70(13): 1589-1599 CrossRef
- Desbrosses G.J., Stougaard J. Root nodulation: a paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host Microbe, 2011, 10(4): 348-358 CrossRef
- Suzaki T., Ito M., Kawaguchi M. Genetic basis of cytokinin and auxin functions during root nodule development. Front. Plant Sci., 2013, 4: 42 CrossRef
- Hayashi S., Gresshoff P.M., Ferguson B.J. Mechanistic action of gibberellins in legume nodulation. J. Integr. Plant Biol., 2014, 56(10): 971-978 CrossRef
- Guinel F.C. Ethylene, a hormone at the center-stage of nodulation. Front. Plant Sci., 2015, 6: 1121 CrossRef
- Tsyganova A.V., Tsyganov V.E. Negative hormonal regulation of symbiotic nodule development. I. Ethylene (review). Agricultural Biology, 2015, 50(3): 267-277 CrossRef
- Stec N., Banasiak J., Jasinski M. Abscisic acid-an overlooked player in plant-microbe symbioses formation Acta Biochim. Pol., 2016, 63(1): 53-58 CrossRef
- Rivas-San Vicente M., Plasencia J. Salicylic acid beyond defense: its role in plant growth and development. J. Exp. Bot., 2011, 62(10): 3321-3338 CrossRef
- Ryu H., Cho H., Choi D., Hwang I. Plant hormonal regulation of nitrogen-fixing nodule organogenesis. Mol. Cells, 2012, 34(2): 117-126 CrossRef
- Nagata M., Suzuki A. Effects of phytohormones on nodulation and nitrogen fixation in leguminous plants. In: Advances in biology and ecology of nitrogen fixation. T. Ohyama (ed.). InTech, Rijeka, Croatia,2014: 111-128 CrossRef
- Ferguson B.J., Mathesius U. Phytohormone regulation of legume-rhizobia interactions J. Chem. Ecol., 2014, 40(7): 770-790 CrossRef
- Vlot A.C., Dempsey D.M.A., Klessig D.F. Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol., 2009, 47: 177-206 CrossRef
- Ramanujam M.P., Jaleel V.A., Kumaravelu G. Effect of salicylic acid on nodulation, nitrogenous compounds and related enzymes of Vigna mungo. Biologia Plantarum, 1998, 41(2): 307-311 CrossRef
- Martinez-Abarca F., Herrera-Cervera J.A., Bueno P., Sanjuan J., Bisseling T., Olivares J. Involvement of salicylic acid in the establishment of the Rhizobium meliloti-alfalfa symbiosis. Mol. Plant Microbe In., 1998, 11(2): 153-155 CrossRef
- Blilou I., Ocampo J.A., García-Garrido J.M. Resistance of pea roots to endomycorrhizal fungus or Rhizobium correlates with enhanced levels of endogenous salicylic acid. J. Exp. Bot., 1999, 50(340): 1663-1668 CrossRef
- Lian B., Zhou X., Miransari M., Smith D.L. Effects of salicylic acid on the development and root nodulation of soybean seedlings. J. Agron. Crop Sci., 2000, 185(3): 187-192 CrossRef
- Sato T., Fujikake H., Ohtake N., Sueyoshi K., Takahashi T., Sato A., Ohyama T. Effect of exogenous salicylic acid supply on nodule formation of hypernodulating mutant and wild type of soybean. Soil Sci. Plant Nutr., 2002, 48(3): 413-420 CrossRef
- van Spronsen P.C., Tak T., Rood A.M., van Brussel A.A., Kijne J.W., Boot K.J. Salicylic acid inhibits indeterminate-type nodulation but not determinate-type nodulation. Mol. Plant Microbe In., 2003, 16(1): 83-91 CrossRef
- Stacey G., McAlvin C.B., Kim S.Y., Olivares J., Soto M.J. Effects of endogenous salicylic acid on nodulation in the model legumes Lotus japonicus and Medicago truncatula. Plant Physiol., 2006, 141(4): 1473-1481 CrossRef
- Riely B.K., Lougnon G., Ané J.-M., Cook D.R. The symbiotic ion channel homolog DMI1 is localized in the nuclear membrane of Medicago truncatula roots. Plant J., 2007, 49(2): 208-216 CrossRef
- Bonfante P., Genre A., Faccio A., Martini I., Schauser L., Stougaard J., Webb J., Parniske M. The Lotus japonicus LjSym4 gene is required for the successful symbiotic infection of root epidermal cells. Mol. Plant Microbe In., 2000 13(10): 1109-1120 CrossRef
- Bastianelli F., Costa A., Vescovi M., D’Apuzzo E., Zottini M., Chiurazzi M., Schiavo F.L. Salicylic acid differentially affects suspension cell cultures of Lotus japonicus and one of its non-symbiotic mutants. Plant Mol. Biol., 2010, 72(4-5): 469-483 CrossRef
- Levine A., Tenhaken R., Dixon R., Lamb C. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell, 1994, 94(4): 491-501 CrossRef
- Palma F., López-Gómez M., Tejera N.A., Lluch, C. Salicylic acid improves the salinity tolerance of Medicago sativa in symbiosis with Sinorhizobium meliloti by preventing nitrogen fixation inhibition. Plant Sci., 2013, 208: 75-82 CrossRef
- Hayat S., Hayat Q., Alyemeni M.N., Ahmad A. Salicylic acid enhances the efficiency of nitrogen fixation and assimilation in Cicer arietinum plants grown under cadmium stress. J. Plant Interact., 2014, 9(1): 35-42 CrossRef
- Tett A.J., Karunakaran R., Poole P.S. Characterisation of SalRAB a salicylic acid inducible positively regulated efflux system of Rhizobium leguminosarum bv viciae 3841. PloS ONE, 2014, 9(8): e103647 CrossRef
- Wasternack C., Hause B. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Annals of Botany, 2013, 111(6): 1021-1058 CrossRef
- Rosas S., Soria R., Correa N., Abdala G. Jasmonic acid stimulates the expression of nod genes in Rhizobium. Plant Mol. Biol., 1998, 38(6): 1161-1168 CrossRef
- Mabood F., Souleimanov A., Khan W., Smith D.L. Jasmonates induce Nod factor production by Bradyrhizobium japonicum. Plant Physiol. Bioch., 2006, 44(11): 759-765 CrossRef
- Creelman R.A., Mullet J.E. Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. PNAS USA, 1995, 92(10): 4114-4119 CrossRef
- Zhang J., Subramanian S., Zhang Y., Yu O. Flavone synthases from Medicago truncatula are flavanone-2-hydroxylases and are important for nodulation. Plant Physiol., 2007, 144(2): 741-751 CrossRef
- Sun J., Cardoza V., Mitchell D.M., Bright L., Oldroyd G., Harris J.M. Crosstalk between jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation. Plant J., 2006, 46(6): 961-970 CrossRef
- Oldroyd G.E.D., Engstrom E.M., Long S.R. Ethylene inhibits the Nod factor signal transduction pathway of Medicago truncatula. Plant Cell, 2001, 13(8): 1835-1849 CrossRef
- Nakagawa T., Kawaguchi M. Shoot-applied MeJA suppresses root nodulation in Lotus japonicus. Plant Cell Physiol., 2006, 47(1): 176-180 CrossRef
- Seo H.S., Li J., Lee S.-Y., Yu J.-W., Kim K.-H., Lee S.-H., Lee I.-J., Paek N.-C. The hypernodulating nts mutation induces jasmonate synthetic pathway in soybean leaves. Mol. Cells, 2007, 24(2): 185.
- Zdyb A., Demchenko K., Heumann J., Mrosk C., Grzeganek P., Göbel C., Feussner I., Pawlowski K., Hause B. Jasmonate biosynthesis in legume and actinorhizal nodules. New Phytol., 2011, 189(2): 568-579 CrossRef
- Suzuki A., Suriyagoda L., Shigeyama T., Tominaga A., Sasaki M., Hiratsuka Y., Yoshinaga A., Arima S., Agarie S., Sakai T., Inada S., Jikumaru Y., Kamiya Y., Uchiumi T., Abe M., Hashiguchi M., Akashi R., Sato S., Kaneko T., Tabata S., Hirsch A.M. Lotus japonicus nodulation is photomorphogenetically controlled by sensing the red/far red (R/FR) ratio through jasmonic acid (JA) signaling. PNAS USA, 2011, 108(40): 16837-16842 CrossRef
- Costanzo M.E., Andrade A., del Carmen Tordable M., Cassán F., Abdala G. Production and function of jasmonates in nodulated roots of soybean plants inoculated with Bradyrhizobium japonicum. Arch. Microbiol., 2012, 194(10): 837-845 CrossRef
- Umezawa T., Nakashima K., Miyakawa T., Kuromori T., Tanokura M., Shinozaki K., Yamaguchi-Shinozaki K. Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol., 2010, 51(11): 1821-1839 CrossRef
- Phillips D.A. Abscisic acid inhibition of root nodule initiation in Pisum sativum. Planta, 1971, 100(3): 181-190 CrossRef
- Cho M.J., Harper J.E. Effect of abscisic acid application on root isoflavonoid concentration and nodulation of wild-type and nodulation-mutant soybean plants. Plant Soil, 1993, 153(1): 145-149 CrossRef
- Bano A., Harper J.E., Auge R.M., Neuman D.S. Changes in phytohormone levels following inoculation of two soybean lines differing in nodulation. Funct. Plant Biol., 2002, 29(8): 965-974 CrossRef
- Suzuki A., Akune M., Kogiso M., Imagama Y., Osuki K., Uchiumi T., Higashi S., Han S.Y., Yoshida S., Asami T., Abe M. Control of nodule number by the phytohormone abscisic acid in the roots of two leguminous species. Plant Cell Physiol., 2004, 45(7): 914-922 CrossRef
- González E.M., Gálvez L., Arrese-Igor C. Abscisic acid induces a decline in nitrogen fixation that involves leghaemoglobin, but is independent of sucrose synthase activity. J. Exp. Bot., 2001, 52(355): 285-293 CrossRef
- Khadri M., Tejera N.A., Lluch C. Alleviation of salt stress in common bean (Phaseolus vulgaris) by exogenous abscisic acid supply. J. Plant Growth Regul., 2006, 25(2): 110-119 CrossRef
- Palma F., López-Gómez M., Tejera N.A., Lluch C. Involvement of abscisic acid in the response of Medicago sativa plants in symbiosis with Sinorhizobium meliloti to salinity. Plant Sci., 2014, 223: 16-24 CrossRef
- Ding Y., Kalo P., Yendrek C., Sun J., Liang Y., Marsh J.F., Harris J.M., Oldroyd G.E. Abscisic acid coordinates nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula. Plant Cell, 2008, 20(10): 2681-2695 CrossRef
- Caba J.M., Centeno M.L., Fernández B., Gresshoff P.M., Ligero F. Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a supernodulating mutant and the wild type. Planta, 2000, 211(1): 98-104 CrossRef
- Tominaga A., Nagata M., Futsuki K., Abe H., Uchiumi T., Abe M., Kucho K., Hashiguchi M., Akashi R., Hirsch A.M., Arima S., Suzuki A. Enhanced nodulation and nitrogen fixation in the abscisic acid low-sensitive mutant enhanced nitrogen fixation1 of Lotus japonicus. Plant Physiol., 2009, 151(4): 1965-1976 CrossRef
- Tominaga A., Nagata M., Futsuki K., Abe H., Uchiumi T., Abe M., Kucho K., Hashiguchi M., Akashi R., Hirsch A., Arima S., Suzuki A. Effect of abscisic acid on symbiotic nitrogen fixation activity in the root nodules of Lotus japonicus. Plant Signaling & Behavior, 2010, 5(4): 440-443 CrossRef
- Shimoda Y., Shimoda-Sasakura F., Kucho K., Kanamori N., Nagata M., Suzuki A., Abe M., Higashi S., Uchiumi T. Overexpression of class 1 plant hemoglobin genes enhances symbiotic nitrogen fixation activity between Mesorhizobium loti and Lotus japonicus. Plant J., 2009, 57(2): 254-263 CrossRef