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Current IssueEditorial BoardOnline First ArticlesArchive

volume 28 issue 2 (june 2007) : 127-134

RELATIONSHIP BETWEEN NITROGEN FIXATION AND CARBON METABOUSM IN LEGUMES: A REVIEW

J
JASLEEN AND NEERA GARG*
1Department of Botany, Panjab University, Chandigarh-160014, India.

  • Submitted|

  • First Online |

  • doi

Cite article:- GARG* NEERA AND JASLEEN (2025). RELATIONSHIP BETWEEN NITROGEN FIXATION AND CARBON METABOUSM IN LEGUMES: A REVIEW. Agricultural Reviews. 28(2): 127-134. doi: .

ABSTRACT

The process of nitrogen fixation by the legumes imposes carbon (C) energy burden on the plant. The photosynthate translocated from the leaves provides carbon skeleton, reducing power and energy required for the symbiotic nitrogen fixation. Sucrose from the shoot is converted to organic acids, principally dicarboxylates that are supplied to bacteroids to provide reductant for the support of key enzyme nitrogenase. It has been established during the last two decades that an anaplerotic carbon dioxide fixation takes place in nodules, via phosphoenol pyruvate carboxylase (PEPC), a key enzyme for carbon dioxide fixation in plants, algae, cyanobaderia and bacteria, located in the cytoplasm of host cells. Although, it has been shown that nitrogen fixation is fuelled by recently synthesized sucrose translocated to the root nodule, neither sucrose nor hexoses are readily metabolised by isolated bacteroids at rates capable of supporting nitrogenase. In contrast, there is evidence to prove that dicarboxylates play a major and essential role in supporting nitrogen fixation. This review throws light on the relationship between nitrogen fixation and PEPC activity in legume nodules.

KEYWORDS

    REFERENCES

    1. Anthon, G.E. and Emerich, OW. (1990). Plant Physio/' 92: 346-351.
    2. Appleby, CA (1984). Annu. Rev. Plant Physio/' 35: 443-478.
    3. Arwas, R., etal (1985). J. Gen. Microbial. 131: 2059-2066.
    4. Bandurski, etal R.S. and Grenier, C.M. (1953). J. BioI. Chern. 204: 781-786.
    5. Bolton, E., Higgisson, B., Harrington, A and O'Gara, E (1986). Arch. Microbia/. 144: 142-146.
    6. Brewin, N.J. (1991). Annu. Rev. Cell Bio/. 7: 191-226
    7. Bryce, J.H. and Day, DA (1990). J. Expt. Bot. 41: 961-967.
    8. Christel1ar, J.T., Laing, WA and Sutton, W.O. (1977). Plant Physio/. 60: 47-50.
    9. Coker, G.T. and Schubert, KR. (1981). Plant Physio/. 691: 696.
    10. Copeland, L. and Turner, J.E (1987). In: The Biochemistry of plants. 11 (eds.), Stumpf, P.K, Conn, E.E., Academic Press, San Diego, pp.I07-128.
    11. Copeland, L., Vel1a, J. and Hong, Z.Q. (1989). Phytochem. 28: 57-61.
    12. Cral1e, H.T. and Heichel, G.H. (1985). Plant Physio/. 79: 381-385.
    13. Day, DA (1990). In: Nitrogen Fixation: Achievements and objectives (005.) P. Gresshoff, etalChapman HaI1, pp.219-226.
    14. Day, DA and Copeland, L. (1991). Plant Physio/. Biochem. 29(2): 185-201
    15. Day, DA and Mannix, M. (1988). Plant Physiol. Biochem. 26: 567-573.
    16. Day, DA, Price, G.D. and Udvardi, MK (1989). Aust. J. Plant Physio/. 16: 69-~.
    17. Dennis, D.T. and Greyson, M.E (1987). Physio/' Plant. 69: 395-404.
    18. Deroche, M.E. and Carrayol, E. (1988). Physiol. Plant. 74: 775-782.
    19. Dilworth, M. and Glenn, A (1984). Trends Biochem. Sci. 9: 519-523.
    20. Driscol1, B.T. and Finan, T.M. (1993). Mo/. Microbiol. 7: 865-873.
    21. Driscol1, B.T. and Finan, T.M. (1996). J. Bacteria/. 178: 2224-2231.
    22. Engelke, T., Jagadish, M.N. and Puhler, A (1987). J. Gen. Microbiol. 133: 3019-3029.
    23. Finan, T.M., Wood, J.M. and Jordan, D.C. (1983). J. Bacteriol. 154: 1403-1413.
    24. Garg, N., Singla, R. and Geetanjali. (2004). Ind. J. Exp. BioI. 42: 138-142.
    25. Giblin, L., Archdeacon, J. and O'Gara, E (1996). FEMS Microbial. Lett. 139: 19-25.
    26. Glenn, AR. and Dilworth, M.J. (1981). Arch. Microbia/. 129: 233-239.
    27. Glenn, AR., Poole, P.S. and Hudman, J.E (1980). J. Gen. Microbiol. 119: 267-271.
    28. Gordon, AJ., Ryle, G.JA, Mitchel1, D.E and Powel1, C.E. (1985). J. Exp. Bot. 36: 756-759.
    29. Hostak, M.S., Henson, CA, Duke, SH and Vanderbosch, KA (1987). Can. J. Bot. 65: 1108-1115.
    30. Humbeck, C. and Werner, D. (1987). Endocytobiosis Cell Res. 4: 185-186.
    31. Israel, OW. and Jackson, W.A. (1982). Plant Physiol. 69: 171-178.
    32. Jiang, J., Gu, B., Albright, L.M. and Nixon, B.T. (1989). J. Bacterial. 171: 5244-5253.
    33. Jording, D. and Puhler, A (1993). Mol. Gen. Genet. 241: 106-114.
    34. Jording, D., Sharma, P.K, Schmidt, R., Engelke, T., Unde, C. and Puhler, A (1992). J. Plant Physiol. 141: 18-27.
    35. Kimura, I. And Tajima, S. (1989). Soil Sci. Plant Nutr. 35: 271-279. .
    36. King, B.J., Layzel1, D.B. and Canvin, D.T. (1986). Plant Physiol. 81: 200-205.
    37. Kouchi, H. and Nakaji, K (1985). Soil Sci. Plant Nub: 31: 323-334.
    38. Kouchi, H. and Yoneyama, T. (1986). Physio/. Plant. 68: 2338-2344  134 AGRICULTURAL REVIEWS
    39. Kouchi, H., Fukai, K, Katagiri, H., Minamisawa, K and Tajima, S. (1988). Physio/. Plant. 73: 327-334.
    40. Kouchi, H., Nakaji, K, Yoneyama, T. and Ishizuka, J. (1985). Ann. Bot. 56: 333-346.
    41. Lawrie, AC. and Wheeler, C.T. (1975). New Phytol. 74: 429-436.
    42. Layzell, D.B., eta! (1990). In: Nitrogen Fixation: Achievements and Objectives P. Gresshoff, etaK::hapman and Hall, New York - London: pp.21-33.
    43. Leegood, R.C. and Osmond, C.B.(1990). In: Plant Physiology, Biochemistry and Molecular Biology (eds) D.T. Dennis, D.H. Turpin. Essex: Longman Sci. Tech, pp.274-298.
    44. Lepiniec, L., Vidal, J., Chollet, R., Gadal, P. and Cretin, C. (1994). Plant Sci. 99: 111-124.
    45. McDermott, T.R., Griffith, S.M., Vance, C.P. and Graham, P.H. (1989). FEMS Microbiol. Rev. 63: 327-340.
    46. McKay, I.A., Dilworth, M.J. and Glenn, A.R. (1988). MNF 3481. J. Gen. Microbiol. 134: 1433-1440.
    47. Menegus, E, et al Physiol. Plant. 74: 444-449.
    48. Merczewski, W. (1989). Physio/' Plant. 76: 539-543.
    49. Miller, S.S., Boylan, KL.M. and Vance, C.P. (1987). Plant Physiol. 84: 501-508.
    50. Mitsch, M.J., Voegele, R.T., Cowie, A eta!. (1998). J. BioI. Chern. 273: 9330-9336.
    51. Miziorko, H.M., Nowak, T. and Mildvan, AS. (1974). 163: 378-389.
    52. Morell, H. and Copeland, L. (1985). Plant Physiol. 78: 149-154.
    53. Morell, M. and Copeland, L. (1984). Plant Physio/. 74: 1030-1034.
    54. O'Leary, M.H. (1982). Phosphoenol pyruvate carboxylase: Annu. Rev. Plant P1}ysiol. 33: 297-315.
    55. Pathirana, SM., Samac, DA, Roeven, R, Yoshioka, H., Vance, C.P. and Gantt, J.S. (1997). Plant J. 12(2): 293-304.
    56. Pathirana, S.M., Vance, C.P., Miller, S.S. and Gantt, J.S. (1992). Plant Mol. BioI. 20: 437-450.
    57. Peterson; J.B. and Evans, H.J. (1979). Biochem. Biophys. Acta. 567: 445-452
    58. Poole, P. and Allaway, D. (2000). Adv. Microb. Physiol. 43: 117-163.
    59. Rawsthorne, S. and La Rue, T.A (1986). Plant Physiol. 81: 1097-1102.
    60. Reibach, P.H. and Streeter, J.G. (1983). Plant Physiol. 72: 634-640.
    61. Reibach, P.H. and Streeter, J.G. (1984). J. Bacteriol. 159: 47-52.
    62. Reid, C.J. and Poole, P.S. 1998. J. Bacteriol. 2660-2669.
    63. Robertson, J.G. and Taylor, M.P. (1973). Planta. 112: 1-6.
    64. Robinson, D.L., Pathirana, S.M., Gantt, J.S. and Vance, C.P. (1996). Plant Cell Environ. 19: 602-608.
    65. Romanov, v.1., et al Phytochern. 24: 2157-2160.
    66. Ronson, C., Astwood, P., Nixon, T. and Ausubel, F. (1987). Nud. Acids Res. 15: 7923-7934.
    67. Ronson, C.w. (1988). In: Nitrogen fIXation: hundred years after etalH. Bothe, Gustav Fischer, NewYork, N.Y, pp.5470fJ51.
    68. Romon, C.W. and Astwood, P.M. (1985). In: Nitrogen fixation research progress H.J. Evans, et a! Martinus Nijhoff, Dordrecht, The Netherlands, pp.201-207.
    69. Ronson, C.w., (1981). Proc. Nail. Acad. Sci. (USA). 78: 4284-4288.
    70. Rosendahl, L. et al (1990). Plant Physiol. 12-19.
    71. Salminen, S.o. and Streeter, J.G. (1986). Plant Physiol. 81: 538-541.
    72. Salminen, S.O. and Streeter. J.G. (1987). Plant Physiol. 83: 535-540.
    73. San Francisco, M.J.D. and Jacobson, G.R. (1986). FEMS Microbiol. Lett. 35: 71-74.
    74. Schubert, KR. (1986). Ann. Rev. Plant Physiol. 37: 539-574.
    75. Streeter, J.G. (1981). Ann. Bot. 48: 441-450.
    76. Streeter, J.G. (1982). Planta. 155: 112-115
    77. Streeter, J.G. (1987). Plant Physiol. 85: 768-773.
    78. Streeter, J.G. and Salminen, 5.0. (1985). In: Nitrogen fIXation research progress Evans H.J., et a! Marlinus Nijhoff, Dordrecht, pp.277-283.
    79. Stumpf, DK and Burris, R.H. (1979). Anal. Biochern. 95: 311-315.
    80. Thummler, E and Verma, D.P.S. (1987). J. BioI. Chern. 262:.14730-14736.
    81. TIng, I.P. and Osmond, C.P. (1973). Plant Physiol. 51: 439-447.
    82. Toh, H., Kawamura, T. and Izui, K (1994). Plant Cell Environ. 17: 31-43.
    83. Udvardi, MK, Ou Yang, L.J., Young, S. and Day, DA (1990). Mol. Plant Microbe Interact. 3: 334-340.
    84. Udvardi, M,K., Salom, C.L. and Day, DA (1988). Mol. Plant Microbe Interact. 1: 250-254.
    85. Utter, MF. and Kolenbrander, HM. (1972). In: The enzymes (ed.) P.O. Boyer (Dordrecht, K1uwer Academic). 6: 117-136.
    86. Vance, C.P. and Heichel, G.H. (1991). Annu. Rev. Plant Physio/. Plant Mol. BioI. 42: 373-392.
    87. Vance, C.P. and Stade, S. (1984). Plant Physiol. 75: 261-264.
    88. Vance, c.P., Boylan, KL.M., Maxwell, CA, Heichel, GHand Hardman, L.L. (1985). Plant Pllysiol. 78: 774-778.
    89. Verma, D.P.S. and Hong, Z.L. (1996). Trends Microbiol. 4: 364-368.
    90. Walsh, K.B., Vessey, JK and Layzell, D.B. (1987). Plant Physiol. 85: 137-144.
    91. Watson, R.J. (1990). Mol. Plant Microbe Interact. 3: 174-181.
    92. Yarosh, O.K., Charles, T.C. and Finan, T.H. (1989). Mol. Microbiol. 3: 813: 823.
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      volume 28 issue 2 (june 2007) : 127-134

      RELATIONSHIP BETWEEN NITROGEN FIXATION AND CARBON METABOUSM IN LEGUMES: A REVIEW

      J
      JASLEEN AND NEERA GARG*
      1Department of Botany, Panjab University, Chandigarh-160014, India.

      • Submitted|

      • First Online |

      • doi

      Cite article:- GARG* NEERA AND JASLEEN (2025). RELATIONSHIP BETWEEN NITROGEN FIXATION AND CARBON METABOUSM IN LEGUMES: A REVIEW. Agricultural Reviews. 28(2): 127-134. doi: .

      ABSTRACT

      The process of nitrogen fixation by the legumes imposes carbon (C) energy burden on the plant. The photosynthate translocated from the leaves provides carbon skeleton, reducing power and energy required for the symbiotic nitrogen fixation. Sucrose from the shoot is converted to organic acids, principally dicarboxylates that are supplied to bacteroids to provide reductant for the support of key enzyme nitrogenase. It has been established during the last two decades that an anaplerotic carbon dioxide fixation takes place in nodules, via phosphoenol pyruvate carboxylase (PEPC), a key enzyme for carbon dioxide fixation in plants, algae, cyanobaderia and bacteria, located in the cytoplasm of host cells. Although, it has been shown that nitrogen fixation is fuelled by recently synthesized sucrose translocated to the root nodule, neither sucrose nor hexoses are readily metabolised by isolated bacteroids at rates capable of supporting nitrogenase. In contrast, there is evidence to prove that dicarboxylates play a major and essential role in supporting nitrogen fixation. This review throws light on the relationship between nitrogen fixation and PEPC activity in legume nodules.

      KEYWORDS

        REFERENCES

        1. Anthon, G.E. and Emerich, OW. (1990). Plant Physio/' 92: 346-351.
        2. Appleby, CA (1984). Annu. Rev. Plant Physio/' 35: 443-478.
        3. Arwas, R., etal (1985). J. Gen. Microbial. 131: 2059-2066.
        4. Bandurski, etal R.S. and Grenier, C.M. (1953). J. BioI. Chern. 204: 781-786.
        5. Bolton, E., Higgisson, B., Harrington, A and O'Gara, E (1986). Arch. Microbia/. 144: 142-146.
        6. Brewin, N.J. (1991). Annu. Rev. Cell Bio/. 7: 191-226
        7. Bryce, J.H. and Day, DA (1990). J. Expt. Bot. 41: 961-967.
        8. Christel1ar, J.T., Laing, WA and Sutton, W.O. (1977). Plant Physio/. 60: 47-50.
        9. Coker, G.T. and Schubert, KR. (1981). Plant Physio/. 691: 696.
        10. Copeland, L. and Turner, J.E (1987). In: The Biochemistry of plants. 11 (eds.), Stumpf, P.K, Conn, E.E., Academic Press, San Diego, pp.I07-128.
        11. Copeland, L., Vel1a, J. and Hong, Z.Q. (1989). Phytochem. 28: 57-61.
        12. Cral1e, H.T. and Heichel, G.H. (1985). Plant Physio/. 79: 381-385.
        13. Day, DA (1990). In: Nitrogen Fixation: Achievements and objectives (005.) P. Gresshoff, etalChapman HaI1, pp.219-226.
        14. Day, DA and Copeland, L. (1991). Plant Physio/. Biochem. 29(2): 185-201
        15. Day, DA and Mannix, M. (1988). Plant Physiol. Biochem. 26: 567-573.
        16. Day, DA, Price, G.D. and Udvardi, MK (1989). Aust. J. Plant Physio/. 16: 69-~.
        17. Dennis, D.T. and Greyson, M.E (1987). Physio/' Plant. 69: 395-404.
        18. Deroche, M.E. and Carrayol, E. (1988). Physiol. Plant. 74: 775-782.
        19. Dilworth, M. and Glenn, A (1984). Trends Biochem. Sci. 9: 519-523.
        20. Driscol1, B.T. and Finan, T.M. (1993). Mo/. Microbiol. 7: 865-873.
        21. Driscol1, B.T. and Finan, T.M. (1996). J. Bacteria/. 178: 2224-2231.
        22. Engelke, T., Jagadish, M.N. and Puhler, A (1987). J. Gen. Microbiol. 133: 3019-3029.
        23. Finan, T.M., Wood, J.M. and Jordan, D.C. (1983). J. Bacteriol. 154: 1403-1413.
        24. Garg, N., Singla, R. and Geetanjali. (2004). Ind. J. Exp. BioI. 42: 138-142.
        25. Giblin, L., Archdeacon, J. and O'Gara, E (1996). FEMS Microbial. Lett. 139: 19-25.
        26. Glenn, AR. and Dilworth, M.J. (1981). Arch. Microbia/. 129: 233-239.
        27. Glenn, AR., Poole, P.S. and Hudman, J.E (1980). J. Gen. Microbiol. 119: 267-271.
        28. Gordon, AJ., Ryle, G.JA, Mitchel1, D.E and Powel1, C.E. (1985). J. Exp. Bot. 36: 756-759.
        29. Hostak, M.S., Henson, CA, Duke, SH and Vanderbosch, KA (1987). Can. J. Bot. 65: 1108-1115.
        30. Humbeck, C. and Werner, D. (1987). Endocytobiosis Cell Res. 4: 185-186.
        31. Israel, OW. and Jackson, W.A. (1982). Plant Physiol. 69: 171-178.
        32. Jiang, J., Gu, B., Albright, L.M. and Nixon, B.T. (1989). J. Bacterial. 171: 5244-5253.
        33. Jording, D. and Puhler, A (1993). Mol. Gen. Genet. 241: 106-114.
        34. Jording, D., Sharma, P.K, Schmidt, R., Engelke, T., Unde, C. and Puhler, A (1992). J. Plant Physiol. 141: 18-27.
        35. Kimura, I. And Tajima, S. (1989). Soil Sci. Plant Nutr. 35: 271-279. .
        36. King, B.J., Layzel1, D.B. and Canvin, D.T. (1986). Plant Physiol. 81: 200-205.
        37. Kouchi, H. and Nakaji, K (1985). Soil Sci. Plant Nub: 31: 323-334.
        38. Kouchi, H. and Yoneyama, T. (1986). Physio/. Plant. 68: 2338-2344  134 AGRICULTURAL REVIEWS
        39. Kouchi, H., Fukai, K, Katagiri, H., Minamisawa, K and Tajima, S. (1988). Physio/. Plant. 73: 327-334.
        40. Kouchi, H., Nakaji, K, Yoneyama, T. and Ishizuka, J. (1985). Ann. Bot. 56: 333-346.
        41. Lawrie, AC. and Wheeler, C.T. (1975). New Phytol. 74: 429-436.
        42. Layzell, D.B., eta! (1990). In: Nitrogen Fixation: Achievements and Objectives P. Gresshoff, etaK::hapman and Hall, New York - London: pp.21-33.
        43. Leegood, R.C. and Osmond, C.B.(1990). In: Plant Physiology, Biochemistry and Molecular Biology (eds) D.T. Dennis, D.H. Turpin. Essex: Longman Sci. Tech, pp.274-298.
        44. Lepiniec, L., Vidal, J., Chollet, R., Gadal, P. and Cretin, C. (1994). Plant Sci. 99: 111-124.
        45. McDermott, T.R., Griffith, S.M., Vance, C.P. and Graham, P.H. (1989). FEMS Microbiol. Rev. 63: 327-340.
        46. McKay, I.A., Dilworth, M.J. and Glenn, A.R. (1988). MNF 3481. J. Gen. Microbiol. 134: 1433-1440.
        47. Menegus, E, et al Physiol. Plant. 74: 444-449.
        48. Merczewski, W. (1989). Physio/' Plant. 76: 539-543.
        49. Miller, S.S., Boylan, KL.M. and Vance, C.P. (1987). Plant Physiol. 84: 501-508.
        50. Mitsch, M.J., Voegele, R.T., Cowie, A eta!. (1998). J. BioI. Chern. 273: 9330-9336.
        51. Miziorko, H.M., Nowak, T. and Mildvan, AS. (1974). 163: 378-389.
        52. Morell, H. and Copeland, L. (1985). Plant Physiol. 78: 149-154.
        53. Morell, M. and Copeland, L. (1984). Plant Physio/. 74: 1030-1034.
        54. O'Leary, M.H. (1982). Phosphoenol pyruvate carboxylase: Annu. Rev. Plant P1}ysiol. 33: 297-315.
        55. Pathirana, SM., Samac, DA, Roeven, R, Yoshioka, H., Vance, C.P. and Gantt, J.S. (1997). Plant J. 12(2): 293-304.
        56. Pathirana, S.M., Vance, C.P., Miller, S.S. and Gantt, J.S. (1992). Plant Mol. BioI. 20: 437-450.
        57. Peterson; J.B. and Evans, H.J. (1979). Biochem. Biophys. Acta. 567: 445-452
        58. Poole, P. and Allaway, D. (2000). Adv. Microb. Physiol. 43: 117-163.
        59. Rawsthorne, S. and La Rue, T.A (1986). Plant Physiol. 81: 1097-1102.
        60. Reibach, P.H. and Streeter, J.G. (1983). Plant Physiol. 72: 634-640.
        61. Reibach, P.H. and Streeter, J.G. (1984). J. Bacteriol. 159: 47-52.
        62. Reid, C.J. and Poole, P.S. 1998. J. Bacteriol. 2660-2669.
        63. Robertson, J.G. and Taylor, M.P. (1973). Planta. 112: 1-6.
        64. Robinson, D.L., Pathirana, S.M., Gantt, J.S. and Vance, C.P. (1996). Plant Cell Environ. 19: 602-608.
        65. Romanov, v.1., et al Phytochern. 24: 2157-2160.
        66. Ronson, C., Astwood, P., Nixon, T. and Ausubel, F. (1987). Nud. Acids Res. 15: 7923-7934.
        67. Ronson, C.w. (1988). In: Nitrogen fIXation: hundred years after etalH. Bothe, Gustav Fischer, NewYork, N.Y, pp.5470fJ51.
        68. Romon, C.W. and Astwood, P.M. (1985). In: Nitrogen fixation research progress H.J. Evans, et a! Martinus Nijhoff, Dordrecht, The Netherlands, pp.201-207.
        69. Ronson, C.w., (1981). Proc. Nail. Acad. Sci. (USA). 78: 4284-4288.
        70. Rosendahl, L. et al (1990). Plant Physiol. 12-19.
        71. Salminen, S.o. and Streeter, J.G. (1986). Plant Physiol. 81: 538-541.
        72. Salminen, S.O. and Streeter. J.G. (1987). Plant Physiol. 83: 535-540.
        73. San Francisco, M.J.D. and Jacobson, G.R. (1986). FEMS Microbiol. Lett. 35: 71-74.
        74. Schubert, KR. (1986). Ann. Rev. Plant Physiol. 37: 539-574.
        75. Streeter, J.G. (1981). Ann. Bot. 48: 441-450.
        76. Streeter, J.G. (1982). Planta. 155: 112-115
        77. Streeter, J.G. (1987). Plant Physiol. 85: 768-773.
        78. Streeter, J.G. and Salminen, 5.0. (1985). In: Nitrogen fIXation research progress Evans H.J., et a! Marlinus Nijhoff, Dordrecht, pp.277-283.
        79. Stumpf, DK and Burris, R.H. (1979). Anal. Biochern. 95: 311-315.
        80. Thummler, E and Verma, D.P.S. (1987). J. BioI. Chern. 262:.14730-14736.
        81. TIng, I.P. and Osmond, C.P. (1973). Plant Physiol. 51: 439-447.
        82. Toh, H., Kawamura, T. and Izui, K (1994). Plant Cell Environ. 17: 31-43.
        83. Udvardi, MK, Ou Yang, L.J., Young, S. and Day, DA (1990). Mol. Plant Microbe Interact. 3: 334-340.
        84. Udvardi, M,K., Salom, C.L. and Day, DA (1988). Mol. Plant Microbe Interact. 1: 250-254.
        85. Utter, MF. and Kolenbrander, HM. (1972). In: The enzymes (ed.) P.O. Boyer (Dordrecht, K1uwer Academic). 6: 117-136.
        86. Vance, C.P. and Heichel, G.H. (1991). Annu. Rev. Plant Physio/. Plant Mol. BioI. 42: 373-392.
        87. Vance, C.P. and Stade, S. (1984). Plant Physiol. 75: 261-264.
        88. Vance, c.P., Boylan, KL.M., Maxwell, CA, Heichel, GHand Hardman, L.L. (1985). Plant Pllysiol. 78: 774-778.
        89. Verma, D.P.S. and Hong, Z.L. (1996). Trends Microbiol. 4: 364-368.
        90. Walsh, K.B., Vessey, JK and Layzell, D.B. (1987). Plant Physiol. 85: 137-144.
        91. Watson, R.J. (1990). Mol. Plant Microbe Interact. 3: 174-181.
        92. Yarosh, O.K., Charles, T.C. and Finan, T.H. (1989). Mol. Microbiol. 3: 813: 823.
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