Approaches for enhancement of N2 fixation efficiency of chickpea (Cicer arietinum L.) under limiting nitrogen conditions

Plant Biotechnology Journal

Volumn 12, Issue 3, 2014, Pages 387-397

  Nasr Esfahani, Maryam ^a   Sulieman, Saad ^b,c   Schulze, Joachim ^d   Yamaguchi Shinozaki, Kazuko ^e   Shinozaki, Kazuo ^b   Tran, Lam Son ^b  

^a LORESTAN UNIVERSITY   (Iran)

^b Elements Chemistry Laboratory   (Japan)

^c UNIVERSITY OF KHARTOUM   (Sudan)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

^e UNIVERSITY OF TOKYO   (Japan)

Author keywords

C metabolism; Cicer arietinum; Gene expression; Mesorhizobium ciceri; N metabolism; Symbiotic efficiency

Indexed keywords

CICER ARIETINUM; EMBRYOPHYTA; MESORHIZOBIUM; MESORHIZOBIUM CICERI; TRACHEOPHYTA;

CARBON; MALIC ACID; MALIC ACID DERIVATIVE; NITROGEN; NITROGENASE; SUCROSE;

ARTICLE; BIOLOGICAL MODEL; BIOMASS; C-METABOLISM; CHICKPEA; CICER; ENZYMOLOGY; GENE EXPRESSION; MESORHIZOBIUM; MESORHIZOBIUM CICERI; METABOLISM; MICROBIOLOGY; N-METABOLISM; NITROGEN FIXATION; NODULATION; PHYSIOLOGY; PLANT; PLANT ROOT; SPECIES DIFFERENCE; SYMBIOSIS; SYMBIOTIC EFFICIENCY;

C-METABOLISM; CICER ARIETINUM; GENE EXPRESSION; MESORHIZOBIUM CICERI; N-METABOLISM; SYMBIOTIC EFFICIENCY;

BIOMASS; CARBON; CICER; MALATES; MESORHIZOBIUM; MODELS, BIOLOGICAL; NITROGEN; NITROGEN FIXATION; NITROGENASE; PLANT ROOTS; PLANT SHOOTS; ROOT NODULES, PLANT; SPECIES SPECIFICITY; SUCROSE; SYMBIOSIS;

EID: 84896390231     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12146     Document Type: Article

References (61)

1. Arrese-Igor, C., Gonzalez, E.M., Gordon, A.J., Minchin, F.R., Galvez, L., Royuela, M., Cabrerizo, P.M. and Aparicio-Tejo, P.M. (1999) Sucrose synthase and nodule nitrogen fixation under drought and other environmental stresses. Symbiosis, 27, 189-212.
2. Baier, M.C., Barsch, A., Kuster, H. and Hohnjec, N. (2007) Antisense repression of the Medicago truncatula nodule-enhanced sucrose synthase leads to a handicapped nitrogen fixation mirrored by specific alterations in the symbiotic transcriptome and metabolome. Plant Physiol. 145, 1600-1618.
3. Bargaz, A., Ghoulam, C., Amenc, L., Lazali, M., Faghire, M., Abadie, J. and Drevon, J. (2012) A phosphoenol pyruvate phosphatase transcript is induced in the root nodule cortex of Phaseolus vulgaris under conditions of phosphorus deficiency. J. Exp. Bot. 63, 4723-4730.
4. Barsch, A., Tellstrom, V., Patschkowski, T., Kuster, H. and Niehaus, K. (2006) Metabolite profiles of nodulated alfalfa plants indicate that distinct stages of nodule organogenesis are accompanied by global physiological adaptations. Mol. Plant Microbe Interact. 19, 998-1013.
5. Ben Romdhane, S., Tajini, F., Trabelsi, M., Aouani, M.E. and Mhamdi, R. (2007) Competition for nodule formation between introduced strains of Mesorhizobium ciceri and the native populations of rhizobia nodulating chickpea (Cicer arietinum) in Tunisia. World J. Microbiol. Biotechnol. 23, 1195-1201.
6. Ben Salah, I., Slatni, T., Albacete, A., Gandour, M., Andujar, C.M., Houmani, H., Ben Hamed, K., Martinez, V., Perez-Alfocea, F. and Abdelly, C. (2010) Salt tolerance of nitrogen fixation in Medicago ciliaris is related to nodule sucrose metabolism performance rather than antioxidant system. Symbiosis, 51, 187-195.
7. Bhattacharyya, P.N. and Jha, D.K. (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J. Microbiol. Biotechnol. 28, 1327-1350.
8. Bradford, M.M. (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 72, 248-254.
9. Burbano, C.S., Liu, Y., Rosner, K.L., Reis, V.M., Caballero-Mellado, J., Reinhold-Hurek, B. and Hurek, T. (2011) Predominant nifH transcript phylotypes related to Rhizobium rosettiformans in field-grown sugarcane plants and in Norway spruce. Env. Microbiol. Rep. 3, 383-389.
10. Chen, R.F., Scott, C. and Trepman, E. (1979) Fluorescence properties of Ortho-Phthaldialdehyde derivatives of amino-acids. Biochim. Biophys. Acta 576, 440-455.
11. Craig, J., Barratt, P., Tatge, H., Dejardin, A., Handley, L., Gardner, C.D., Barber, L., Wang, T., Hedley, C., Martin, C. and Smith, A.M. (1999) Mutations at the rug4 locus alter the carbon and nitrogen metabolism of pea plants through an effect on sucrose synthase. Plant J. 17, 353-362.
12. 2 fixation rate of drought-stressed soybeans. Plant Physiol. 136, 3313-3318.
13. Deslippe, J.R. and Egger, K.N. (2006) Molecular diversity of nifH genes from bacteria associated with high arctic dwarf shrubs. Microb. Ecol. 51, 516-525.
14. Drevon, J., Abdelly, C., Amarger, N., Aouani, M., Aurag, J., Gherbi, H., Jebara, M., Lluch, C., Payre, H., Schump, O., Soussi, M., Sifi, B. and Trabelsi, M. (2001) An interdisciplinary research strategy to improve symbiotic nitrogen fixation and yield of common bean (Phaseolus vulgaris) in salinised areas of the Mediterranean basin. J. Biotechnol. 91, 257-268.
15. Egli, M.A., Griffith, S.M., Miller, S.S., Anderson, M.P. and Vance, C.P. (1989) Nitrogen assimilating enzyme-activities and enzyme protein during development and senescence of effective and plant gene-controlled ineffective alfalfa nodules. Plant Physiol. 91, 898-904.
16. Fedorova, M., Tikhonovich, I.A. and Vance, C.P. (1999) Expression of C-assimilating enzymes in pea (Pisum sativum L.) root nodules. In situ localization in effective nodules. Plant, Cell Environ. 22, 1249-1262.
17. 2 fixation for the efficiency of symbiotic nitrogen fixation in pea at vegetative growth and during pod formation. J. Exp. Bot. 61, 2281-2291.
18. 2 fixation. J. Exp. Bot. 61, 121-130.
19. Flowers, T.J., Gaur, P.M., Gowda, C.L.L., Krishnamurthy, L., Samineni, S., Siddique, K.H.M., Turner, N.C., Vadez, V., Varshney, R.K. and Colmer, T.D. (2010) Salt sensitivity in chickpea. Plant, Cell and Environ. 33, 490-509.
20. Gaur, P.M., Jukantil, A.K. and Varshney, R.K. (2012) Impact of genomic technologies on chickpea breeding strategies. Agronomy 2, 199-221.
21. Geurts, R., Lillo, A. and Bisseling, T. (2012) Exploiting an ancient signalling machinery to enjoy a nitrogen fixing symbiosis. Curr. Opin. Plant Biol. 15, 438-443.
22. Gonzalez, E.M., Gordon, A.J., James, C.L. and Arreseigor, C. (1995) The role of sucrose synthase in the response of soybean nodules to drought. J. Exp. Bot. 46, 1515-1523.
23. Gonzalez, E.M., Galvez, L., Royuela, M., Aparicio-Tejo, P.M. and Arrese-Igor, C. (2001) Insights into the regulation of nitrogen fixation in pea nodules: lessons from drought, abscisic acid and increased photoassimilate availability. Agronomie, 21, 607-613.
24. Gordon, A.J. (1991) Enzyme distribution between the cortex and the infected region of soybean nodules. J. Exp. Bot. 42, 961-967.
25. Gordon, A.J. and James, C.L. (1997) Enzymes of carbohydrate and amino acid metabolism in developing and mature nodules of white clover. J. Exp. Bot. 48, 895-903.
26. Gordon, A.J., Minchin, F.R., James, C.L. and Komina, O. (1999) Sucrose synthase in legume nodules is essential for nitrogen fixation. Plant Physiol. 120, 867-877.
27. Graham, P.H. and Vance, C.P. (2003) Legumes: Importance and constraints to greater use. Plant Physiol. 131, 872-877.
28. Groat, R.G. and Vance, C.P. (1981) Root nodule enzymes of ammonia assimilation in alfalfa (Medicago Sativa L) - developmental patterns and response to applied nitrogen. Plant Physiol. 67, 1198-1203.
29. Hoagland, D.R. and Arnon, D.I. (1950) A water culture method for growing plants without soil. Circular 347, pp. 25-32. Berkley: University of California Agricultural Experiment Station.
30. Horst, I., Welham, T., Kelly, S., Kaneko, T., Sato, S., Tabata, S., Parniske, M. and Wang, T.L. (2007) TILLING mutants of Lotus japonicus reveal that nitrogen assimilation and fixation can occur in the absence of nodule-enhanced sucrose synthase. Plant Physiol. 144, 806-820.
31. Icgen, B., Ozcengiz, G. and Alaeddinoglu, N.G. (2002) Evaluation of symbiotic effectiveness of various Rhizobium cicer strains. Res. Microbiol. 153, 369-372.
32. Keutgen, A.J. and Pawelzik, E. (2008) Contribution of amino acids to strawberry fruit quality and their relevance as stress indicators under NaCl salinity. Food Chem. 111, 642-647.
33. Kyei-Boahen, S., Slinkard, A.E. and Walley, F.L. (2002) Evaluation of rhizobial inoculation methods for chickpea. Agron J. 94, 851-859.
34. Laranjo, M., Branco, C., Soares, R., Alho, L., Carvalho, M.D.E. and Oliveira, S. (2002) Comparison of chickpea rhizobia isolates from diverse Portuguese natural populations based on symbiotic effectiveness and DNA fingerprint. J. Appl. Microbiol. 92, 1043-1050.
35. Lea, P.J., Sodek, L., Parry, M.A.J., Shewry, R. and Halford, N.G. (2007) Asparagine in plants. Ann. Appl. Biol. 150, 1-26.
36. Lopez, M., Herrera-Cervera, J.A., Iribarne, C., Tejera, N.A. and Lluch, C. (2008) Growth and nitrogen fixation in Lotus japonicus and Medicago truncatula under NaCl stress: nodule carbon metabolism. J. Plant Physiol. 165, 641-650.
37. Mafongoya, P.L., Mpepereki, S. and Mudyazhezha, S. (2009) The importance of biological nitrogen fixation in cropping systems in nonindustrialized nations. In Nitrogen Fixation in Crop Production (Emerich, D.W. and Krishnan, H.B., eds), pp. 329-348. Madison, WI, USA: American Society of Agronomy, Crop Science Society of America, Soil Science Society of America.
38. Mhadhbi, H., Jebara, M., Limam, F. and Aouani, M.E. (2004) Rhizobial strain involvement in plant growth, nodule protein composition and antioxidant enzyme activities of chickpea-rhizobia symbioses: modulation by salt stress. Plant Physiol. Biochem. 42, 717-722.
39. Mhadhbi, H., Jebara, M., Zitoun, A., Limam, F. and Aouani, M.E. (2008) Symbiotic effectiveness and response to mannitol-mediated osmotic stress of various chickpea-rhizobia associations. World J. Microb. Biot. 24, 1027-1035.
40. Miller, S.S., Driscoll, B.T., Gregerson, R.G., Gantt, J.S. and Vance, C.P. (1998) Alfalfa malate dehydrogenase (MDH): molecular cloning and characterization of five different forms reveals a unique nodule-enhanced MDH. Plant J. 15, 173-184.
41. Minchin, F.R., James, E.K. and Becana, M. (2008) Oxygen diffusion, production of reactive oxygen and nitrogen species, and antioxidants in legume nodules. In Nitrogen-fixing Leguminous Symbioses (Dilworth, M.J., James, E.K., Sprent, J.I. and Newton, W.E., eds), pp. 321-362. Dordrecht, The Netherlands: Springer.
42. Mwanamwenge, J., Loss, S.P., Siddique, K.H.M. and Cocks, P.S. (1998) Growth, seed yield and water use of faba bean (Vicia faba L) in a short-season Mediterranean-type environment. Aust. J. Exp. Agr. 38, 171-180.
43. Nasr Esfahani, M. (2011) The effect of drought stress on the nitrogenase activity in sensitive and tolerance symbioses of chickpea (Cicer arietinum L.)-Mesorhizobium ciceri. PhD thesis, University of Isfahan, Iran.
44. Nasr Esfahani, M. and Mostajeran, A. (2011) Rhizobial strain involvement in symbiosis efficiency of chickpea-rhizobia under drought stress: plant growth, nitrogen fixation and antioxidant enzyme activities. Acta Physiol. Plant 33, 1075-1083.
45. Nomura, M., Mai, H.T., Fujii, M., Hata, S., Izui, K. and Tajima, S. (2006) Phosphoenolpyruvate carboxylase plays a crucial role in limiting nitrogen fixation in Lotus japonicus nodules. Plant Cell Physiol. 47, 613-621.
46. Peoples, M.B. (2009) The potential environmental benefits and risks derived from legumes in rotations. In Nitrogen Fixation in Crop Production (Emerich, D.W. and Krishnan, H.B., eds), pp. 349-385. Madison, WI, USA: American Society of Agronomy, Crop Science Society of America, Soil Science Society of America.
47. 2 fixation. In Nitrogen Fixation in Crop Production (Emerich, D.W. and Krishnan, H.B., eds), pp. 211-238. Madison, WI, USA: American Society of Agronomy, Crop Science Society of America, Soil Science Society of America.
48. Rubio, L.M. and Ludden, P.W. (2008) Biosynthesis of the iron-molybdenum cofactor of nitrogenase. Annu. Rev. Microbiol. 62, 93-111.
49. Schulze, J. (2004) How are nitrogen fixation rates regulated in legumes? J. Plant Nutr. Soil Sci. 167, 125-137.
50. Schulze, J., Shi, L.F., Blumenthal, J., Samac, D.A., Gantt, J.S. and Vance, C.P. (1998) Inhibition of alfalfa root nodule phosphoenolpyruvate carboxylase through an antisense strategy impacts nitrogen fixation and plant growth. Phytochemistry, 49, 341-346.
51. Schulze, J., Tesfaye, M., Litjens, R.H.M.G., Bucciarelli, B., Trepp, G., Miller, S., Samac, D., Allan, D. and Vance, C.P. (2002) Malate plays a central role in plant nutrition. Plant Soil, 247, 133-139.
52. Sulieman, S. and Schulze, J. (2010a) The efficiency of nitrogen fixation of the model legume Medicago truncatula (Jemalong A17) is low compared to Medicago sativa. J. Plant Physiol. 167, 683-692.
53. 2 fixation efficiency in the model legume Medicago truncatula. Plant, Cell Environ. 33, 2162-2172.
54. Sulieman, S. and Tran, L.S. (2013) Asparagine: an amide of particular distinction in the regulation of symbiotic nitrogen fixation of legumes. Crit. Rev. Biotechnol. 33, 309-327.
55. 2 fixation in Medicago truncatula. Physiol. Plant. 140, 21-31.
56. Sulieman, S., Schulze, J. and Tran, L.S. (2013) Comparative Analysis of the Symbiotic Efficiency of Medicago truncatula and Medicago sativa under Phosphorus Deficiency. Int. J. Mol. Sci. 14, 5198-5213.
57. Tran, L.S. and Nguyen, H.T. (2009) Future biotechnology of legumes. In Nitrogen Fixation in Crop Production (Emerich, D.W. and Krishnan, H.B., eds), pp. 265-308. Madison, WI, USA: American Society of Agronomy, Crop Science Society of America, Soil Science Society of America.
58. 2 fixation in soybean. Physiol. Plant. 110, 215-223.
59. Vance, C.P. (2001) Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol. 127, 390-397.
60. Vance, C.P. (2008) Carbon and nitrogen metabolism in legume nodules. In Nitrogen-fixing Leguminous Symbioses (Dilworth, M.J., James, E.K., Sprent, J.I. and Newton, W.E., eds), pp. 293-320. Dordrecht, The Netherlands: Springer.
61. White, J., Prell, J., James, E.K. and Poole, P. (2007) Nutrient sharing between symbionts. Plant Physiol. 144, 604-614.