RESEARCH PAPER
Nod factors improve the nitrogen content and rhizobial diversity of faba bean and alter soil dehydrogenase, protease, and acid phosphomonoesterase activities
 
More details
Hide details
1
Institute of Agrophysics, Polish Academy of Sciences, Doświadczalna 4, 20-290 Lublin, Poland
 
2
Department of Genetics and Microbiology, M. Curie-Skłodowska University, Akademicka 19, 20-033 Lublin, Poland
 
3
Siedlce University of Natural Sciences and Humanities, Konarskiego 2, 08-110 Siedlce, Poland
 
4
„SHIM-POL A.M. Borzymowski”, Lubomirskiego 5, 05-080 Izabelin, Poland
 
 
Acceptance date: 2019-07-08
 
 
Publication date: 2019-12-13
 
 
Int. Agrophys. 2020, 34(1): 9-15
 
KEYWORDS
TOPICS
ABSTRACT
Abstract. Nod factors produced by rhizobia are one of the most important signals involved in symbiotic associations involving legumes. A field trial was performed to assess the symbiotic activity, rhizosphere biological parameters, and plant biomass of faba bean (Vicia faba L.) treated with Nod factors. The soil was a Haplic Luvisol derived from loess. The faba bean seeds (cv. Granit) were soaked with an Nod factors solution (260 nM) or water (control) and sown. At the flowering stage, the genetic diversity of rhizobia (based on PCR-RFLP profiles and the sequencing of the 16-23S rDNA and nodD gene), nitrogenase activity (acetylene reduction assay), and nodule biomass were evaluated. Nitrogen yield and plant biomass were determined at the flowering and maturity stages. Rhizosphere soil was examined during plant growth in relation to the activities of dehydrogenase, protease, urease, and acid phosphomonoesterase. The results indicated that the application of the Nod factors improved nitrogenase activity (by 74-80%, depending on the parameter analysed) and increased the genetic diversity of rhizobia inhabiting root nodules, plant nitrogen content (by 16.8%, at maturity), and seed protein yield (by 14.6%). The rhizobial population became more heterogeneous under the influence of the Nod factors than it was for the control (12 and 7 specific genotypes, respectively). At the flowering stage, Nod factors enhanced dehydrogenase, protease, and acid phosphomonoesterase activities by 46, 36 and 9%, respectively. The results revealed the positive effect of Nod factors at reducing water deficiency effects during a growing season with a short-term rainfall deficit.
REFERENCES (46)
1.
Alef K., 1995. Dehydrogenase activity. In: Methods in applied soil microbiology and biochemistry (Eds K. Alef, P. Nannipieri). 228-231, London, Academic Press.
 
2.
Alef K., Nannipieri P., and Trazar-Cepeda C., 1995. Phosphatase activity. In: Methods in applied soil microbiology and biochemistry (Eds K. Alef, P. Nannipieri). 335-344. London, Academic Press.
 
3.
Alef K. and Nannipieri P., 1995. Protease activity. In: Methods in applied soil microbiology and biochemistry (Eds K. Alef, P. Nannipieri). 313-315, London, Academic Press.
 
4.
Anglade J., Billen G., and Garnier J., 2015. Relationships for estimating N2 fixation in legumes: incidence for N balance of legume-based cropping systems in Europe. Ecosphere, 6(3), 37, http://dx.doi.org/10.1890/ES14....
 
5.
Aschi A., Aubert M., Riah-Anglet W., Nélieu S., Dubois C., Akpa-Vinceslas M., and Trinsoutrot-Gattin I., 2017. Introduction of Faba bean in crop rotation: Impacts on soil chemical and biological characteristics. Appl. Soil Ecol., 120, 219-228, https://doi.org/10.1016/j.apso....
 
6.
Baddeley J.A., Jones S., Topp C.F.E., Watson C.A., Helming J., and Stoddard F.L., 2013. Biological nitrogen fixation (BNF) in Europe. Legume Futures Report 1.5. Available from www.legumefutures.de.
 
7.
Denisow B. and Malinowski D.P., 2016. Climate change and the future of our world - implications for plant phenology, physiology, plant communities, and crop management. Acta Agrobot., 69(2), 1683. http://dx.doi.org/10.5586/aa.1....
 
8.
D’Haeze W. and Holsters M., 2002. Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology, 12, 79-105, https://doi.org/10.1093/glycob....
 
9.
Duzan H.M., Zhou X., Souleimanov A., and Smith, D.L., 2004. Perception of Bradyrhizobium japonicum Nod factor by soybean (Glycine max L. Merr.) root hairs under abiotic stress conditions. J. Exp. Bot., 55, 2641-2646, https://doi.org/10.1093/jxb/er....
 
10.
FAO, 1998. World Reference Base for Soil Resources. World Soil Resources Report 84. FAO, Rome. 88pp.
 
11.
Gamas P., Brault M., Jardinaud M.F., and Frugier F., 2017. Cytokinins in Symbiotic Nodulation: When, Where, What For? Trends Plant Sci., 22, 792-802, https://doi.org/10.1016 /j.tplants.2017.06.012.
 
12.
Janczarek M., Rachwał K., Marzec A., Grządziel J., and Palusińska-Szysz M., 2015. Signal molecules and cell-surface components involved in early stages of the legume-rhizobium interactions. Appl. Soil Ecol., 85, 94-113, https://doi.org/10.1016/j.apso....
 
13.
Kelly S., Sullivan J.T., Kawaharada Y., Radutoiu S., Ronson S.C., and Stougaar J., 2018. Regulation of Nod factor biosynthesis by alternative NodD proteins at distinct stages of symbiosis provides additional compatibility scrutiny. Environ. Microbiol., 20, 97-110, https://doi.org/10.1111/1462-2....
 
14.
Khan W., Prithiviraj B., and Smith D.L., 2008. Nod factor [Nod Bj V (C18:1, MeFuc)] and lumichrome enhance photosynthesis and growth of corn and soybean. J. Plant Physiol., 165, 1342-1351, https://doi.org/10.1016/j.jplp....
 
15.
Kiba T., Kudo T., Kojima M., and Sakakibara H., 2011. Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. J. Exp. Bot., 62, 1399-409, https://doi.org/10.1093/jxb/er....
 
16.
Kidaj D., Wielbo J., and Skorupska A., 2012. Nod factors stimulate seed germination and promote growth and nodulation of pea and vetch under competitive conditions. Microbiol. Res., 167, 144-150, https://doi.org/10.1016/j.micr....
 
17.
Kjeldahl J.G., 1883. Neue Methode zur Bestimmung des Stickstoffs in organischen Körpern (New method for the determination of nitrogen in organic substances). Zeitschrift für analytische Chemie, 22, 366-383, https://doi.org/10.1007/BF0133....
 
18.
Köpke U. and Nemecek T., 2010. Ecological services of faba bean. Field Crops Res., 115, 217-233, https://doi.org/10.1016 /j.fcr.2009.10.012.
 
19.
Ladd J.N. and Butler J.H.A., 1972. Short-term assays of soil proteolytic enzyme activities using proteins and dipeptide derivatives as substrates. Soil Biol. Biochem., 4, 19-30, https://doi.org/10.1016/0038-0....
 
20.
Laguerre G., Mavingui P., Allard M.R., Charnay M.P., Louvrier P., Mazurier S.I., Rigottier-Gois L., and Amarger N., 1996. Typing of rhizobia by PCR DNA fingerprinting and PCR-restriction fragment length polymorphism analysis of chromosomal and symbiotic gene regions: application to Rhizobium leguminosarum and its different biovars. Appl. Environ. Microbiol., 62, 2029-2036.
 
21.
Li H., Zhang F., Rengel Z., and Shen J., 2013. Rhizosphere properties in monocropping and intercropping systems between faba bean (Vicia faba L.) and maize (Zea mays L.) grown in a calcareous soil. Crop Pasture Sci., 64, 976-984, https://doi.org/10.1071/CP1326....
 
22.
Lupwayi N.Z., and Kennedy A.C., 2007. Grain legumes in Northern Great Plains: impacts on selected biological soil Processes. Agron. J., 99, 1700-1709, https://doi.org/10.2134/agronj....
 
23.
Maj D., Wielbo J., Marek-Kozaczuk M., and Skorupska A., 2010. Response to flavonoids as a factor influencing competitiveness and symbiotic activity of Rhizobium leguminosarum. Microbiol. Res., 165, 50-60, https://doi.org/10.1016/j.micr....
 
24.
Marks B.B., Megías M., Ollero F.J., Nogueira M.A., Araujo R.S., and Hungria M., 2015. Maize growth promotion by inoculation with Azospirillum brasilense and metabolites of Rhizobium tropici enriched on lipo-chitooligosaccharides (LCOs). AMB Express, 5, 71, https://doi.org/10.1186/s13568....
 
25.
Miransari M. and Smith D., 2009. Rhizobial lipo-chitooligosaccharides and gibberellins enhance barley (Hordeum vulgare L.) seed germination. Biotechnology, 8, 270-275, https://doi.org/10.3923/biotec....
 
26.
Nandhini D.U., Somasundaram E., and Amanullah M.M., 2017. Effect of rhizobial nod factors (lipochitooligosaccharide) on seedling growth of blackgram under salt stress. Legume Res., 41, 159-162, https://doi.org/10.18805/LR-35....
 
27.
Paul E.A., and Clark F.E., 1996. Soil Biology and Biochemistry, Academic Press: San Diego, CA, USA.
 
28.
Podleśny J., Wielbo J., Podleśna A., and Kidaj D., 2014. The pleiotropic effects of extract containing rhizobial Nod factors on pea growth and yield. Cent. Eur. J. Biol., 9, 396-409, https://doi.org/10.2478/s11535....
 
29.
Prithiviraj B., Zhou X., Souleimanov A., Kahn W.M., and Smith D.L., 2003. A host-specific bacteria-to-plant signal molecule (Nod factor) enhances germination and early growth of diverse crop plants. Planta, 216, 437-445.
 
30.
Prudent M., Salon C., Smith D.L., and Emery R.J.N., 2016. Nod factor supply under water stress conditions modulates cytokinin biosynthesis and enhances nodule formation and N nutrition in soybean. Plant Signal Behav., 11, e1212799, https://doi.org/10.1080/155923....
 
31.
Schimel J.P. and Bennett J., 2004. Nitrogen mineralization: Challenges of a changing paradigm. Ecology, 85, 591-602, https://doi.org/10.1890/03-800....
 
32.
Schwinghamer T., Souleimanov A., Dutilleul P., and Smith D., 2016. Supplementation with solutions of lipo-chitooligosacharide Nod Bj V (C18:1, MeFuc) and thuricin 17 regulates leaf arrangement, biomass, and root development of canola (Brassica napus L.). Plant Growth Regul., 78, 31-41, https://doi.org/10.1007/s10725....
 
33.
Siczek A., Frąc M., Nawrocka A., Wielbo J., and Kidaj D., 2015. The response of rhizosphere microbial properties to flavonoids and Nod factors. Acta Agric. Scand., Soil Plant Sci., 65, 125-131, https://doi.org/10.1080/090647....
 
34.
Siczek A., Lipiec J., Wielbo J., Kidaj D., and Szarlip P., 2014. Symbiotic activity of pea (Pisum sativum) after application of nod factors under field conditions. Int. J. Mol. Sci., 15, 7344-7351, https://doi.org/10.3390/ijms15....
 
35.
Siczek A., Lipiec J., Wielbo J., Szarlip P., and Kidaj D., 2013. Pea growth and symbiotic activity response to Nod factors (lipo-chitooligosaccharides) and soil compaction. Appl. Soil Ecol., 72, 181-186, https://doi.org/10.1016/j.apso....
 
36.
Smith S., Habib A., Kang Y., Leggett M., and Diaz-Zorita M., 2015. LCO applications provide improved responses with legumes and nonlegumes. In: Biological Nitrogen Fixation (Ed. F.J. de Bruijn). pp. 1077-1085. 1st edn. John Wiley & Sons Inc, https://doi.org/10.1002/978111....
 
37.
Tabatabai M.A. and Bremner J.M., 1969. Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol. Biochem. 1, 301-307, https://doi.org/10.1016/0038-0... (69)90012-1.
 
38.
Thalmann A., 1968. Zur Methodik der Bestimmung der Dehydrogenase - Aktivität im Boden mittels Triphenyl-tetrazoliumchlorid (TTC). Landwirtsh Forsch, 21, 249-258.
 
39.
Wahbi S., Prin Y., Thioulouse J., Sanguin H., Baudoin E., Maghraoui T., Oufdou K., Le Roux C., Galiana A., Hafidi M., and Duponnois R., 2016. Impact of wheat/faba bean mixed cropping or rotation systems on soil microbial functionalities. Front. Plant Sci., 7, 1364, https://doi.org/10.3389/fpls.2....
 
40.
Wielbo J., Kidaj D., Koper P., Kubik-Komar A., and Skorupska A., 2012. The effect of biotic and physical factors on the competitive ability of Rhizobium eguminosarum. Cent. Eur. J. Biol., 7, 13-24, https://doi.org/10.2478/s11535....
 
41.
Wielbo J., Marek-Kozaczuk M., Kidaj D., and Skorupska A., 2011. Competitiveness of Rhizobium leguminosarum bv. trifolii strains in mixed inoculation of clover (Trifolium pratense). Pol. J. Microbiol., 60, 43-49.
 
42.
Wielbo J., Marek-Kozaczuk M., Kubik-Komar A., and Skorupska A., 2007. Increased metabolic potential of Rhizobium spp. is associated with bacterial competitiveness. Can. J. Microbiol., 53, 957-967, https://doi.org/10.1139/W07-05....
 
43.
Wielbo J., Marek-Kozaczuk M., Mazur A., Kubik-Komar A., and Skorupska A., 2010. Genetic and metabolic divergence within a Rhizobium leguminosarum bv. trifolii population recovered from clover nodules. Appl. Environ. Microb., 76, 4593-4600, https://doi.org/10.1128/AEM.00....
 
44.
Zahir Z.A., Zafar-ul-Hye M., Sajjad S., and Naveed M., 2011. Comparative effectiveness of Pseudomonas and Serratia sp. containing ACC-deaminase for coinoculation with Rhizobium leguminosarum to improve growth, nodulation, and yield of lentil. Biol. Fert. Soils, 47, 457-465, https://doi.org/10.1007/s00374....
 
45.
Zantua M.I. and Bremner J.M., 1977. Stability of urease in soils. Soil Biol. Biochem., 9, 135-140, https://doi.org/10.1016/0038-0....
 
46.
Zhang N., He X., Gao Y., Li Y., Wang H., Ma D., Zhang R., and Yang S., 2010. Pedogenic carbonate and soil dehydrogenase activity in response to soil organic matter in artemisia ordosica community. Pedosphere, 20, 229-235.
 
eISSN:2300-8725
ISSN:0236-8722
Journals System - logo
Scroll to top