Alleviating the inhibitory effect of salinity stress on nod gene expression in Rhizobium tibeticum – fenugreek (Trigonella foenum graecum) symbiosis by isoflavonoids treatment

References

• Abd-Alla MH. 1992. Nodulation and nitrogen fixation in faba bean (Vicia fab L.) plants under salt stress. Symbiosis. 12:311–319.
   Web of Science ®Google Scholar
• Abd-Alla MH. 1999. Nodulation and nitrogen fixation of lupinus species with Bradyrhizobium (lupin) strains in iron deficient soil. Biol Fertil Soils. 28:407–441. 10.1007/s003740050513
   Web of Science ®Google Scholar
• Abd-Alla MH. 2011. Nodulation and nitrogen fixation in interspecies grafts of soybean and common bean is controlled by isoflavonoid signal molecules translocated from shoot. Plant Soil Environ. 57:453–458.
   Web of Science ®Google Scholar
• Abd-Alla MH, Abdel Wahab AM. 1995. Survival of Rhizobium leguminosarum biovar viceae subjected to heat, drought and salinity in soil. Biol Plant. 37:131–137. 10.1007/BF02913008
   Web of Science ®Google Scholar
• Abd-Alla MH, Omar SA. 1998. Wheat-straw and cellulolytic fungi application increases nodulation, nodule efficiency and growth of fenugreek (Trigonella foenum graceum L.) grown in saline soil. Biol Fertil Soils. 26:58–65. 10.1007/s003740050343
   Web of Science ®Google Scholar
• Abd-Alla MH, Vuong TD, Harper JE. 1998. Genotypic differences in dinitrogen fixation response to NaCl stress in intact and grafted soybean. Crop Sci. 38:72–77. 10.2135/cropsci1998.0011183X003800010013x
   Web of Science ®Google Scholar
• Ali B, Hayat S, Hayat Q, Ahmad A. 2010. Cobalt stress affects nitrogen metabolism, photosynthesis and antioxidant system in chickpea (Cicer arietinum L.). J Plant Interact. 5:223–231. 10.1080/17429140903370584
   Web of Science ®Google Scholar
• Ausubel FM, Brent R, Kingston RE, Moore DD, Smith JA, Struhl K. 1987. Current protocols in molecular biology. New York, NY: Greene Publishing Associates and Wiley-Interscience, Wiley.
   Google Scholar
• Bandyopadhyay AK, Jain V, Nainawate HS. 1996. Nitrate alters the flavonoid profile and nodulation in pea (Pisum sativum L.). Biol Fert Soil. 21:189–192. 10.1007/BF00335933
   Web of Science ®Google Scholar
• Begum AA, Leibovitch S, Migner P, Zhang F. 2001. Specific flavonoids induced nod gene expression and pre-activated nod genes of Rhizobium leguminosarum increased pea (Pisum sativum L.) and lentil (Lens culinaris L.) nodulation in controlled growth chamber environments. J Exp Bot. 52:1537–1543. 10.1093/jexbot/52.360.1537
   PubMed Web of Science ®Google Scholar
• Bimboim HC, Doly J. 1979. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucl Acids Res. 7:1513–1523. 10.1093/nar/7.6.1513
   PubMed Web of Science ®Google Scholar
• Bukhari SB, Bhanger MI, Memon S. 2008. Antioxidative activity of extracts from fenugreek seeds (Trigonella foenum graecum). Pak J Anal Environ Chem. 9:78–83.
   Google Scholar
• Cooper JE. 2004. Multiple responses of rhizobia to flavonoids during legume root infection. Adv Bot Res. 41:1–62.
   Web of Science ®Google Scholar
• Cooper JE. 2007. Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J Appl Microbiol. 103:1355–1365. 10.1111/j.1365-2672.2007.03366.x
   PubMed Web of Science ®Google Scholar
• Cordovilla MP, Ligero F, Lluch C. 1994. The effect of salinity on N fixation and assimilation in Vicia faba. J Exp Bot. 45:1483–1488. 10.1093/jxb/45.10.1483
   Web of Science ®Google Scholar
• Coventry DR, Evans J. 1989. Symbiotic nitrogen fixation and soil acidity. In: Robson AD, editor. Soil acidity and plant growth. New York, NY: Academic Press; p. 103–137.
   Google Scholar
• Dakora FD, Joseph CM, Phillips DA. 1993. Common bean root exudates contain elevated levels of daidzein and coumestrol in response to Rhizobium inoculation. Mol Plant Microbe Interact. 6:665–668. 10.1094/MPMI-6-665
   Web of Science ®Google Scholar
• Echeverria M, Sannazzaro AI, Ruiz OA, Menéndez AB. 2013. Modulatory effects of Mesorhizobium tianshanense and Glomus intraradices on plant proline and polyamine levels during early plant response of Lotus tenuis to salinity. Plant Soil. 364:69–79. 10.1007/s11104-012-1312-6
   Web of Science ®Google Scholar
• Elsheikh EAE, Wood M. 1990. Salts effects on survival and multiplication of chickpea and soybean rhizobia. Soil Biol Biochem. 22:343–347. 10.1016/0038-0717(90)90111-C
   Web of Science ®Google Scholar
• González JE, Marketon MM. 2003. Quorum sensing in nitrogen-fixing Rhizobia. Microbiol Mol Biol Rev. 67:574–592. 10.1128/MMBR.67.4.574-592.2003
   PubMed Web of Science ®Google Scholar
• Guasch-Vidal B, Estévez J, Dardanelli MS, Soria-Díaz ME, Fernández de Córdoba F, Balog CIA, Manyani H, Gil-Serrano A, Thomas-Oates J, Hensbergen PJ, et al. 2013. High NaCl concentrations induce the nod genes of Rhizobium tropici CIAT899 in the absence of flavonoid inducers. Mol Plant Microbe Interact. 26:451–460. 10.1094/MPMI-09-12-0213-R
   PubMed Web of Science ®Google Scholar
• Hafeez FY, Aslam Z, Malik KA. 1988. Effect of salinity and inoculation on growth, nitrogen fixation and nutrient uptake of Vigna radiata L. Wilczek. Plant Soil. 106:3–8. 10.1007/BF02371188
   Web of Science ®Google Scholar
• Hardy RWF, Holsten RD, Jackson EK, Burns RC. 1968. The acetylene–ethylene assay for measurement of nitrogen fixation: laboratory and field evaluation. Plant Physiol. 48:1185–1207. 10.1104/pp.43.8.1185
   Web of Science ®Google Scholar
• Hassan S, Mathesius U. 2012. The role of flavonoids in root–rhizosphere signalling: opportunities and challenges for improving plant–microbe interactions. J Exp Bot. 63:3429–3444. 10.1093/jxb/err430
   PubMed Web of Science ®Google Scholar
• Hayat S, Hayat Q, Alyemeni MN, Ahmad A. 2012. Salicylic acid enhances the efficiency of nitrogen fixation and assimilation in Cicer arietinum plants grown under cadmium stress. J Plant Interact.
   Web of Science ®Google Scholar
• Hong GF, Burn JE, Johnston AWB. 1987. Evidence that DNA involved in the expression of nodulation (nod) genes in Rhizobium binds to the product of the regulatory gene nodD. Nucl Acids Res. 15:9677–9690. 10.1093/nar/15.23.9677
   PubMed Web of Science ®Google Scholar
• Hooykaas PJJ, Klapwijk PM, Nuti MP, Schilperoort RA, Rorsch A. 1977. Transfer of the Agrobacterium tumefaciens Ti plasmid to a virulant agrobacteria and to Rhizobium. J Gen Microbiol. 98:477–484. 10.1099/00221287-98-2-477
   Google Scholar
• Hungria M, Joseph CM, Phillips DA. 1991. Rhizobium nod-gene inducers exuded naturally from roots of common bean (Phaseolus vulgaris L.). Plant Physiol. 97:759–764.
   PubMed Web of Science ®Google Scholar
• Hungria M, Johnston AWB, Phillips DA. 1992. Effects of flavonoids released naturally from bean (Phaseolus vulgaris) on nodD-regulated gene transcription in Rhizobium leguminosarum bv. phaseoli. Mol Plant Microbe Interact. 5:199–203. 10.1094/MPMI-5-199
   PubMed Web of Science ®Google Scholar
• Lauter DJ, Munns DN, Clarkin KL. 1981. Salt response of chickpeas influenced by N supply. Agron J. 73:961–966. 10.2134/agronj1981.00021962007300060013x
   Web of Science ®Google Scholar
• Li B, Krumbein A, Neugart S, Li L, Schreiner M. 2012. Mixed cropping with maize combined with moderate UV-B radiations lead to enhanced flavonoid production and root growth in faba bean. J Plant Interact. 7:333–340. 10.1080/17429145.2012.714407
   Web of Science ®Google Scholar
• Lin M-H, Gresshoff PM, Ferguson BJ. 2012. Systemic regulation of soybean nodulation by acidic growth conditions. Plant Physiol. 160:2028–2039. 10.1104/pp.112.204149
   PubMed Web of Science ®Google Scholar
• Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar, Buchner A, Lai T, Steppi S, Jobb G et al. 2004. ARB: a software environment for sequence data. Nucleic Acids Res, 32:1363–1371.
   PubMed Web of Science ®Google Scholar
• Maj D, Wielboa J, Marek-Kozaczuka M, Skorupska A. 2010. Response to flavonoids as a factor influencing competitiveness and symbiotic activity of Rhizobium leguminosarum. Microbiol Res. 165:50–60. 10.1016/j.micres.2008.06.002
   PubMed Web of Science ®Google Scholar
• Miller J. 1992. A short course in bacterial genetics and handbook of E. coli and related bacteria. New York, NY: Cold Spring Harbor: Cold Spring Harbor Laboratory Press; p. 72–74.
   Google Scholar
• Miransari M, Smith DL. 2007. Overcoming the stressful effects of salinity and acidity on soybean [Glycine max (L.) Merr.] nodulation and yields using signal molecule genistein under field conditions. J Plant Nutr. 30:1967–1992. 10.1080/01904160701700384
   Web of Science ®Google Scholar
• Miransari M, Smith DL. 2008. Using signal molecule genistein to alleviate the stress of suboptimal root zone temperature on soybean-Bradyrhizobium symbiosis under different soil textures. J Plant Interact. 3:287–295. 10.1080/17429140802160136
   Web of Science ®Google Scholar
• Nandasena KG, O'Hara GW, Tiwari RP, Howieson JG. 2009. A basis for the development of an inferior N2 fixation phenotype in root nodule bacteria following lateral transfer of symbiotic genes. In: The 16th International Congress of Nitrogen Fixation; June 14–19; Big Sky, Montana.
   Google Scholar
• Oke V, Long RS. 1999. Bacterial genes induced within the nodule during the Rhizobium-legume symbiosis. Mol Microbiol. 32:837–849.
   PubMed Web of Science ®Google Scholar
• Peck MC, Fisher RF, Long SR. 2006. Diverse flavonoids stimulate NodD1 binding to nod gene promoters in Sinorhizobium meliloti. J Bacteriol. 188:5417–5427. 10.1128/JB.00376-06
   PubMed Web of Science ®Google Scholar
• Rao M, Blane U, Zonnenberg, M. 1985. PC-state version I A. Athens, Georgia, USA: The University of Georgia.
   Google Scholar
• Serraj R, Vasquez-Diaz H, Drevon JJ. 1998. Effects of salt stress on nitrogen fixation, oxygen diffusion, and ion distribution in soybean, common bean, and alfalfa. J Plant Nutr. 21:475–488. 10.1080/01904169809365418
   Web of Science ®Google Scholar
• Singleton PW, Bohlool B. 1984. Effect of salinity on nodule formation by soybean. Plant Physiol. 74:72–76. 10.1104/pp.74.1.72
   PubMed Web of Science ®Google Scholar
• Spaink HP, Wijffelman CA, Pees E, Okker RJH, Lugtenberg BJJ. 1987. Rhizobium nodulation gene nodD as a determinant of host specificity. Nature. 328:337–340. 10.1038/328337a0
   Web of Science ®Google Scholar
• Tu JC. 1981. Effect of salinity on rhizobium–root-hair interaction, nodulation and growth of soybean. Can J Plant Sci. 61:231–239.
   Web of Science ®Google Scholar
• Vincze E, Bowra S. 2006. Transformation of rhizobia with broad-host-range plasmids by using a freeze–thaw method. Appl Environ Microbiol. 72:2290–2293. 10.1128/AEM.72.3.2290-2293.2006
   PubMed Web of Science ®Google Scholar
• Wang SP, Stacey G. 1990. Ammonia regulation of nod genes in Bradyrhizobium japonicum. Mol Gen Genet. 223:329–331. 10.1007/BF00265071
   PubMedGoogle Scholar
• Yanagi K, Koichi Sugimoto K, Matsui K. 2011. Oxylipin-specific cytochrome P450s (CYP74s) in Lotus japonicus: their implications in response to mechanical wounding and nodule formation. J Plant Interact. 6:255–264. 10.1080/17429145.2011.562985
   Web of Science ®Google Scholar
• Yousef AN, Sprent JI. 1983. Effect of NaCl on growth, nitrogen incorporation and chemical composition of inoculated and NH4NO3 fertilized Vicia faba L. plants. J Exp Bot. 143:941–950. 10.1093/jxb/34.8.941
   Web of Science ®Google Scholar
• Zaat SA, Wijffelman CA, Spaink HP, van Brussel AAN, Okker RJ, Lugtenberg BJJ. 1987. Induction of the nodA promoter of Rhizobium leguminosarum Sym plasmid pRL1JI by plant flavanones and flavones. J Bacteriol. 169:198–204.
   PubMed Web of Science ®Google Scholar
• Zahran HH, Sprent JI. 1986. Effect of sodium chloride and polyethylene glycol on root hair infection and nodulation of Vicia faba L. plants by Rhizobium leguminosarum. Planta. 167:303–309. 10.1007/BF00391332
   PubMed Web of Science ®Google Scholar
• Zhang F, Smith DL. 1995. Preincubation of Bradyrhizobium japonicum with genistein accelerates nodule development of soybean at suboptimal root zone temperatures. Plant Physiol. 103:961–968.
   Google Scholar
• Zhang F, Smith DL. 1996. Inoculation of soybean (Glycine max (L.) Merr.) with genistein-preincubated Bradyrhizobium japonicum or genistein directly applied into soil increases soybean protein and dry matter yield under short season conditions. Plant Soil. 179:233–241.
   Web of Science ®Google Scholar
• Zhang F, Smith DL. 2002. Interorganismal signalling in suboptimum environments: the legume-rhizobia symbiosis. Adv Agron 76:125–161.
   Web of Science ®Google Scholar
• Zhang X-S, Cheng H-P. 2006. Identification of Sinorhizobium meliloti early symbiotic genes by use of a positive functional screen. Appl Environ Microbiol. 72:2738–2748.
   PubMed Web of Science ®Google Scholar