The Role of the external mycelial network of arbuscular mycorrhizal fungi: III. a study of nitrogen transfer between plants interconnected by a common mycelium

Significância do micélio externo dos fungos micorrízicos arbusculares: III. estudo da transferência de nitrogênio entre plantas inter-conectadas por um mesmo micélio

THE ROLE OF THE EXTERNAL MYCELIAL NETWORK OF ARBUSCULAR MYCORRHIZAL FUNGI: III. A STUDY OF NITROGEN TRANSFER BETWEEN PLANTS INTERCONNECTED BY A COMMON MYCELIUM

Marco A. Martins^* , Andre F. Cruz

Universidade Estadual do Norte Fluminense, Centro de Ciências e Tecnologias Agropecuárias, Setor de Microbiologia do Solo, Campos, RJ, Brasil

Approved: July 23, 1998

ABSTRACT

An experiment under greenhouse conditions was carried out to evaluate the relative contribuition of arbuscular mycorrhizal fungi (AMF) in the process of nitrogen transfer from cowpea to maize plants, using the isotope ¹⁵N. Special pots divided in three sections (A, B and C), were constructed and a nylon mesh screen of two diameters: 40µm (which allowed the AMF hyphae to pass but not the plant roots) or 1µm (which acted as a barrier to AM hyphae and plant roots) was inserted between the sections B and C. Section A had 25.5 mg of N/kg using (¹⁵NH₄)2SO₄ as N source. Two cowpea seedlings inoculated with Rhizobium sp. were transplanted with their root systems divided between the sections A and B. Ten days later, 2 seeds of maize were sown into the section C which was inoculated with Glomus etunicatum. Thirty-five days after transplanting, the maize plants were harvested. AMF inoculation increased dry weight and ¹⁵N and P content of maize plant shoots. Direct transfer of ¹⁵N via AMF hyphae was 21.2%; indirect transfer of ¹⁵N mediated by AMF mycelium network, was 9.6%, and indirect transfer not mediated by AM mycelium network , was 69.2%.

Key words: mycorrhizae, cowpea, maize, nitrogen transfer

In intercropping systems with grass and legume plants it is possible that the nitrogen derived from the biological fixation of nitrogen (BFN) by the legume can be transferred to the grass. Brophy et al. (3) detected a transfer of 40 kg of N from a legume to a grass, and Rao and Giller (27) observed a high content of N in grass intercropped with a legume. The flow of N between plants may happen through several pathways. The legume may release N to the soil through exsudates from the roots, leaves, nodule debris and roots tissues (5, 7, 14). Some works with ¹⁵N dilution (4) and subdivided roots (15) have shown increases of N transfer between plants associated with AMF. The AMF may promote a high uptake of N in grass intercropped with a legume, even though there may be no significant differences in the shoot dry weight (10). The N transferred may be enough to improve the growth of the receiver plants (9). The nitrogen transfer between plants mediated by the AMF may occur by the following pathways: 1) direct transfer (DT) of nitrogen through mycelium which interconnects the roots of two plants; 2) indirect transfer (IT_M), involving leakage of nitrogen from one root, its absorption by AMF hyphae scavenging in the rhizosphere, and transfer to neighbouring plants. In addition to these two pathways, there is a third mechanism which is not mediated by AMF, which involves the leakage of nitrogen from roots of one plant and its subsequent absorption by the roots of neighbouring plants. To evaluate the relative contribution of each pathway to the total N transferred from one plant to another is very important because the direct transfer of N by AMF mycelium reduces the loss of N in the soil (leaching and immobilization) and also could improve the N cycling. Our purpose was to examine the contribution of the three possible pathways to the N transfer process between cowpea (donor plant) and maize (receiver plant), using the isotope ¹⁵N.

³Fig. 1

Figure 1.

Each pot section was filled with a soil: sand substrate (1:2, v/v) previously sterilized with CH₃Br. The substrate properties were: pH 5.3; organic C, 0.41%; total N, 0.041%; P and K content 8 and 19 mg/kg, respectively. The substrate in each pot section was amended with: 50 mg P/kg, 50mg K/kg and 0.6 ton/ha of Ca and Mg in the proportions of 4:1. At planting, 25 mg/kg of N was added into the section A, using as source (¹⁵NH₄)₂SO₄ with 10% of ¹⁵N. Fifteen days later, 0.5 mg/kg of N was once again added into the section A, using the same source, but with 99% of ¹⁵N.

Two seedlings of cowpea inoculated with Rhizobium sp. strain BR-2001, from the National Centre of Agrobiology Research - EMBRAPA - RJ - Brazil, were carefully planted with their roots divided so that half of their root systems were growing in each of sections A and B. The pots were then placed in a green house.

Ten days later, two seeds of maize (receiver plant) were sown into the section C. The inoculation with AMF was made in half of the pots by adding into the substrate of section C, approximately 20 g of soil containing spores and hyphae of Glomus etunicatum (Becker and Gerdemann). In the case of non-mycorrhizal plant pots, approximately 25 ml of filtrate solution (filter paper Whatman n° 1) derived from infected soil, was added into section C to ensure that control plants received a bacterial population comparable with that present in the mycorrhizal medium, but lacking AM propagules.

Thirty-five days after maize planting, the plants were harvested. A sub-sample of cowpea and maize roots was taken to determine the root colonization by AMF (11). The shoot of maize plants was oven-dried (48h at 80°C), weighed and ground. The ¹⁵N content was determined by mass spectrometer and P content colorimetrically by spectrophotometer.

The relative contribution of each of the three processes of N transfer to the total amount ¹⁵N transferred to maize was obtained using the procedures of Martins (22) for ¹⁴C, as follows:

a) Direct transfer pathway via AMF hyphae (DT):

Where:

N_M40 = ¹⁵N content in maize shoots grown in pots with a nylon mesh screen of 40µm and inoculated with AMF;

N_M1 = ¹⁵N content in maize shoots grown in pots with a nylon mesh screen of 1µm and inoculated with AMF.

b) Indirect transfer pathway mediated by AMF mycelium network (IT_M)

Where:

N_M1 = ¹⁵N content in maize shoots grown in pots with a nylon mesh screen of 1 µm and inoculated with AMF;

NN_M40= ¹⁵N content in maize shoots grown in pots with a nylon mesh screen of 40 µm and not inoculated with AMF;

N_M40 = ¹⁵N content in maize shoots grown in pots with a nylon mesh screen of 40 µm and inoculated with AMF.

c) Indirect transfer pathway not mediated by AMF (ITNM)

Where:

NN_M40= ¹⁵N content in maize shoots grown in pots with a nylon mesh screen of 40 µm and not inoculated with AMF;

N_M40 = ¹⁵N content in maize shoots grown in pots with a nylon mesh screen of 40 µm and inoculated with AMF.

Data were subjected to an analysis of variance (ANOVA test); least significant differences were calculated by an F test.

Fig. 2

Figure 2.Glomus etunicatum

The mycorrhizal infection led to a significant increase of both dry weight (Fig. 3) and P content (Fig. 4) of maize shoots. There was no effect due to the barrier between the sections B and C on dry weight of maize shoots. However, P content in the pots inoculated with AMF (+AMF) was significantly lower in the pots with a nylon mesh screen of 1 µm.

Figure 3.

Figure 4.

The ¹⁵N content in maize shoots was not significantly affected by the presence of the imposed barrier (Fig. 5). Mycorrhizal infection led to a significant increase of ¹⁵N content in maize shoots.

Figure 5. ¹⁵

The relative contribution of each pathway to the total amount of ¹⁵N transferred to maize shoots mediated by AMF, including the direct (DT) and indirect process (ITM), was lower (21.2 + 9.6 = 30.8%) than the contribution not mediated by the fungi (ITNM = 69.2%) (Table 1). Thus the main route by which ¹⁵N was transferred from cowpea to maize was via the indirect transfer not involving the AMF, where the ¹⁵N may have been exudated from the cowpea root into soil solution being subsequently uptaken by the roots of maize plants.

Fig 2et al.et al.

The external mycelial network of AMF growing from the section C into the section B can promote links between the two plant species. Read et al. (30) observed that most plants in seminatural grassland become heavily infected very soon after seed germination. They suggested that infection of the developing root system must arise from contact with mycelium spreading from plants with established infection, and that as a consequence of this pattern of infection, many plants within the community must be inter-linked by mycorrhizal hyphae. This has since been confirmed by studies of the development of infection of seedlings in the field (29).

This work showed that the maize shoot dry weights were higher in mycorrhizal plants than those of their non-mycorrhizal counterparts (Fig. 3). However there is no evidence that this fact is attributable to the N transferred from legume to grass. It is more probable that this plant growth is due to a higher P content observed in mycorrhizal plants (Fig. 4). Hamel and Smith (12) concluded that the higher growth of maize plants intercropped with soybean under mycorrhizal condition was due mainly to a better P uptake by mycorrhizal plants and the N-transfer to maize plants had low significance to that growth. In practice the N content transferred between plants may not be enough to improve the growth or mineral nutrition of the receiver plant, because perhaps the maize plants need a higher quantity of N than that available from the cowpea plants.

The results revealed that AMF was enable to promote direct transfer of N from donor to receiver plants, because there was an increase of ¹⁵N transferred to receiver when they were separated from the donor plants by a nylon mesh screen of 40µm, which allowed only the AMF mycelium to pass. The involvement of AMF in the process of N transfer between plants remains controversial. Some researches have shown a positive effect (17, 19). On the other hand, others have not observed any influence of mycorrhizae in this process (16). Hamel and Smith (13) showed that even though the AMF had established links between plants, they did not increase N transfer. According to Johansen et al. (18), the transfer of N from one plant to another mediated by arbuscular mycelium depends on the demand of plants. Tomm et al. (32) have also pointed out that this process can be bi-directional depending of the demand of receiver plants.

The transfer of substances between plants mediated by AMF have been also shown for other elements, such as carbon and phosphorus, by using radioisotope techniques. Francis and Read (8) and Martins (22) have demonstrated that the ¹⁴C transfer between plants occurred directly via AMF mycelium. Whittingham and Read (35) and Martins and Read (23) showed that direct transfer of 32P between living source and sink plants occurs mainly by hyphae connecting the two plants.

The present study revealed that the AMF can provide channels for transfer of N between plants cultivated under intercropped systems. However, the most significant route by which ¹⁵N was transferred from cowpea to maize was by the indirect process not involving the fungus. Further studies are now required to determine if the transferred N is enough to stimulate the growth of the receiver and it is also necessary to evaluate the behaviour of this fungus under other environmental circunstances.

ACKNOWLEDGMENTS

We are extremely grateful to CNPq (Brazil) for financial support.

RESUMO

Significância do micélio externo dos fungos micorrízicos arbusculares. III. Estudo da transferência de nitrogênio entre plantas inter-conectadas por um mesmo micélio.

Conduziu-se um experimento em casa de vegetação para avaliar a importância dos fungos micorrízicos arbusculares (FMA) sobre o processo de transferência de nitrogênio de plantas de caupi para o milho, utilizando-se o isótopo ¹⁵N. Foram construídos vasos compartimentalizados, compostos de 3 seções (A, B e C) de 2 dm³ de capacidade. Entre as seções B e C inseriu-se uma tela de nylon com 2 diâmetros de abertura de malha: 1 µm (que atuou como barreira para o micélio fúngico e para as raízes das plantas), ou 40 µm (que atuou como barreira somente para as raízes das plantas). Adicionou-se 25,5 mg/kg de N na forma de (¹⁵ NH₄)₂SO₄ na seção A dos vasos. A seguir, 2 plântulas de caupi previamente inoculadas com Rhizobium sp. foram plantadas com seus sistemas radiculares divididos entre as seções A e B. Após 10 dias, duas sementes de milho foram semeadas na seção C, onde se efetuou a inoculação com o fungo Glomus etunicatum no orifício de plantio. O experimento foi coletado 35 dias após, e os resultados demonstraram que a presença do FMA aumentou a matéria seca e o conteúdo de ¹⁵ N e P da parte aérea das plantas de milho. A transferência direta de ¹⁵ N via hifa fúngica, foi de 21,2%; a transferência indireta mediada pelos FMA, foi de 9,6%; e a indireta não mediada pelos FMA, foi de 69,2%.

Palavras-chave: micorrizas, caupi, milho, transferência de nitrogênio.

Glomus mosseae New Phytol.,

2. Bethlenfalvay, G.J.; Reyes-Solis, M.G.; Camel, S.B.; Ferrera-Cerrato, R. Nutrient transfer between the root zones of soybean and maize plants connected by a common mycorrhizal mycelium. Physiol Plantarum, 82:423-432, 1991

3. Brophy, L.S.; Heichel, G.H.; Russelle, M.P. Nitrogen transfer from forage legumes to grass in a systematic planting design. Crop Sci, 27:753-758, 1987.

4. Barea, J.M.; Azcón-Aguilar, C.; Azcón, R. Vesicular-Arbuscular mycorrhiza improve both symbiotic N₂-fixation and N uptake from soil as assessed with a ¹⁵N technique under field conditions. New Phytol., 106: 717-725, 1987.

5. Burton, J.W.; Brim, C..A.; Rawlings, J.O. Performance of non-nodulating and nodulating soybean isolines in mixed culture with nodulating cultivars. Crop Sci., 23:469-473, 1983.

6. Camel, S.B.; Reyes-Solis, M.G.; Ferrera-Cerrato, R.; Franson, R.L.; Brown, M.S.; Bethlenfalvay, G.J. Growth of VA mycorrhizal mycelium through bulk soil. Soil Sci. Am. J., 55: 389-393, 1991.

7. Dubach, M.; Russelle, M.P. Forage legumes roots and nodules and their role in the nitrogen transfer. Agron. J., 86: 259-66, 1994.

8. Francis, R.; Read, D.J. Direct transfer of carbon between plants connected by VA mycorrhizal mycelium. Nature, 307:53-56, 1984.

9. Francis, R.; Finlay, R.D.; Read, D.J. Transfer of nutrients in inter and intra-specific combination of host plants. In:Vesicular-Arbuscular mycorrhiza in natural vegetation systems. New Phytol., 102: 103-111, 1986.

10. Frey B.; Shuepp, H. Transfer of symbiotically fixed nitrogen from berseen (Trifolium alexandrinum L) to maize via VA mycorrhizal hyphae. New Phytol., 122: 447-454, 1992.

11. Giovannetti, M.; Mosse, B. An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol., 84: 489-500, 1980.

12. Hamel, C.; Smith, D.L Interspecific N-transfer and plant development in a mycorrhizal field-grown mixture. Soil Biol. Biochem., 23: 661-665, 1991.

13. Hamel, C.; Smith, D.L. Mycorrhizae-mediated ¹⁵N transfer from soybean to corn in field-grown intercrops. Effect of component crop spatial relationships. Soil Biol. Biochem., 24:499-501, 1992.

14. Haynes, R. J. Competitive aspects of the grass-legume association. Adv. in Agron., 33:227-261, 1980.

15. Haystead, A.; Malajczuk, N.; Grove, T.S. Underground transfer of nitrogen between pasture plants infected with VA mycorrhizal fungi. New Phytol., 108: 417-423, 1988.

16. Ikram A., Jensen E.S.; Jakobsen I. No significant transfer of N and P from Pueraria phaseoloides to Hevea brasiliensis via hyphal links of arbuscular mycorrhiza. Soil Biol. Biochem., 26: 1541-1547, 1994.

17. Johansen, A.; Jensen, E.S. Transfer of N and P from intact or decompositing roots of pea to barley interconnected by an arbuscular mycorrhizal fungus. Soil Biol. Biochem., 28: 73-81, 1996.

18. Johansen, A.; Jakobsen, I.; Jensen, E.S.; Hyphal, N. transport by a vesicular-arbuscular mycorrhizal fungus associated with cucumber grown at 3 nitrogen levels. Plant Soil 160: 1-9, 1994.

19. Kessel, C.V.; Singleton, P.W.; Hoben, H.J. Enhaced N-transfer from a soybean to maize by Vesicular Arbuscular Mycorrhizal (VAM) fungi. Plant Physiol, 79 562-563, 1985

20. Martins, M.A. The role of the external mycelial network of VA mycorrhizal fungi. A study of carbon transfer between plants interconnected by a common mycelium. Mycorrhiza, 2: 69-73, 1992a.

21. Martins, M.A. Interactions between plants with special reference to the role of the external mycelium of VA mycorrhizal fungi. The University of Sheffield, England, (PhD Thesis), 1992b, 171 p.

22. Martins, M.A. The role of the external mycelial network of arbuscular mycorrhizal fungi in the carbon transfer process between plants. Mycol Res., 97:807-810, 1993

23. Martins, M.A.; Read, D.J. The role of the external mycelial network of VA mycorrhizal fungi. II A study of phosphorus transfer between plants interconnected by a common mycelium. Rev. de Microb., 27: 30-35, 1996.

24. Mosse, B. Specificit in VA mycorrhizas. In: Sanders, F.E.; Mosse, B.; Tinker, P.B. Endomycorrhizas. Academic Press, London, 1975, 469-484 pp.

25. Newman, E.I. Mycorrhizal links between plants: their functioning and ecological significance. Adv. in Ecol. Res., 18:243-270, 1988.

26. Newman, E.I.; Eason, W.R. Rates of phosphorus transfer within and between ryegrass (Lolium perenne) plants. Funct. Ecol., 7: 242-248, 1993.

27. Rao, A.V.; Giller, K.E. Nitrogen fixation and its transfer from Leucaena to Grass using N¹⁵ . Ecol. Manag., 61: 221-227, 1994.

28. Read, D.J. The structure and function of the vegetative mycelium of mycorrhizal roots. In: Jennings, D.H.; Rayner, A.D.M. The Ecology and Physiology of the Fungal Mycelium, Cambridge: Cambridge University Press. 1984, 215-240 pp.

29. Read, D.J.; Birch, C.P.D. The effects and implications of disturbance of mycorrhizal mycelial systems. Proc. Royal Soc. Edinb., 94: 13-24, 1986.

30. Read, D.J.; Kouchecki, H.K.; Hodgson , J. VA mycorrhiza in natural vegetation systems. I The occurrence of infection. New Phytol., 77: 641-53, 1976.

31. Ritz, K.; Newman, E.I. Evidence for rapid cycling of phosphorus from dying roots to living plants. Oikos, 45: 174-180, 1985.

32. Tomm, G.O.; Kessel, G.V.; Slinkard, A.E. Bidirectional transfer of nitrogen between alfafa and bromegrass: Short and long term evidence. Plant and Soil 164: 77-86, 1994.

33. Tommerup, I.C. Spore dormancy in VA mycorrhizal fungi. Trans. Br. Mycol. Soc., 81: 37-45, 1983.

34. Van Kessel, C.; Singleton, P.W.; Hoben, H. Enhanced N-transfer from a soybean to maize by VA mycorrhizal fungi. Plant Physiol., 79:562-563, 1985.

35. Whittingham, J.; Read, D.J. Nutrient transfer between plants with mycorrhizal interconnections: Vesicular-arbuscular mycorrhiza in natural vegetation systems. New Phytol., 90: 277-284, 1981.

• ¹
  Ames, R.N.; Reid, C.P.P.; Parter, L.K.; Cambardella, C. Sources by Glomus mosseae, a vesicular-arbuscular mycorrhizal fungus. New Phytol., 95: 381-396, 1983
• ²
  Bethlenfalvay, G.J.; Reyes-Solis, M.G.; Camel, S.B.; Ferrera-Cerrato, R. Nutrient transfer between the root zones of soybean and maize plants connected by a common mycorrhizal mycelium. Physiol Plantarum, 82:423-432, 1991
• ³
  Brophy, L.S.; Heichel, G.H.; Russelle, M.P. Nitrogen transfer from forage legumes to grass in a systematic planting design. Crop Sci, 27:753-758, 1987.
• ⁴
  Barea, J.M.; Azcón-Aguilar, C.; Azcón, R. Vesicular-Arbuscular mycorrhiza improve both symbiotic N₂-fixation and N uptake from soil as assessed with a ¹⁵N technique under field conditions. New Phytol., 106: 717-725, 1987.
• ⁵
  Burton, J.W.; Brim, C..A.; Rawlings, J.O. Performance of non-nodulating and nodulating soybean isolines in mixed culture with nodulating cultivars. Crop Sci., 23:469-473, 1983.
• ⁶
  Camel, S.B.; Reyes-Solis, M.G.; Ferrera-Cerrato, R.; Franson, R.L.; Brown, M.S.; Bethlenfalvay, G.J. Growth of VA mycorrhizal mycelium through bulk soil. Soil Sci. Am. J., 55: 389-393, 1991.
• ⁷
  Dubach, M.; Russelle, M.P. Forage legumes roots and nodules and their role in the nitrogen transfer. Agron. J., 86: 259-66, 1994.
• ⁸
  Francis, R.; Read, D.J. Direct transfer of carbon between plants connected by VA mycorrhizal mycelium. Nature, 307:53-56, 1984.
• ⁹
  Francis, R.; Finlay, R.D.; Read, D.J. Transfer of nutrients in inter and intra-specific combination of host plants. In:Vesicular-Arbuscular mycorrhiza in natural vegetation systems. New Phytol., 102: 103-111, 1986.
• ¹⁰
  Frey B.; Shuepp, H. Transfer of symbiotically fixed nitrogen from berseen (Trifolium alexandrinum L) to maize via VA mycorrhizal hyphae. New Phytol., 122: 447-454, 1992.
• ¹¹
  Giovannetti, M.; Mosse, B. An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol., 84: 489-500, 1980.
• ¹²
  Hamel, C.; Smith, D.L Interspecific N-transfer and plant development in a mycorrhizal field-grown mixture. Soil Biol. Biochem., 23: 661-665, 1991.
• ¹³
  Hamel, C.; Smith, D.L. Mycorrhizae-mediated ¹⁵N transfer from soybean to corn in field-grown intercrops. Effect of component crop spatial relationships. Soil Biol. Biochem., 24:499-501, 1992.
• ¹⁴
  Haynes, R. J. Competitive aspects of the grass-legume association. Adv. in Agron., 33:227-261, 1980.
• ¹⁵
  Haystead, A.; Malajczuk, N.; Grove, T.S. Underground transfer of nitrogen between pasture plants infected with VA mycorrhizal fungi. New Phytol., 108: 417-423, 1988.
• ¹⁶
  Ikram A., Jensen E.S.; Jakobsen I. No significant transfer of N and P from Pueraria phaseoloides to Hevea brasiliensis via hyphal links of arbuscular mycorrhiza. Soil Biol. Biochem., 26: 1541-1547, 1994.
• ¹⁷
  Johansen, A.; Jensen, E.S. Transfer of N and P from intact or decompositing roots of pea to barley interconnected by an arbuscular mycorrhizal fungus. Soil Biol. Biochem., 28: 73-81, 1996.
• ¹⁸
  Johansen, A.; Jakobsen, I.; Jensen, E.S.; Hyphal, N. transport by a vesicular-arbuscular mycorrhizal fungus associated with cucumber grown at 3 nitrogen levels. Plant Soil 160: 1-9, 1994.
• ¹⁹
  Kessel, C.V.; Singleton, P.W.; Hoben, H.J. Enhaced N-transfer from a soybean to maize by Vesicular Arbuscular Mycorrhizal (VAM) fungi. Plant Physiol, 79 562-563, 1985
• ²⁰
  Martins, M.A. The role of the external mycelial network of VA mycorrhizal fungi. A study of carbon transfer between plants interconnected by a common mycelium. Mycorrhiza, 2: 69-73, 1992a.
• ²¹
  Martins, M.A. Interactions between plants with special reference to the role of the external mycelium of VA mycorrhizal fungi. The University of Sheffield, England, (PhD Thesis), 1992b, 171 p.
• ²²
  Martins, M.A. The role of the external mycelial network of arbuscular mycorrhizal fungi in the carbon transfer process between plants. Mycol Res., 97:807-810, 1993
• ²³
  Martins, M.A.; Read, D.J. The role of the external mycelial network of VA mycorrhizal fungi. II A study of phosphorus transfer between plants interconnected by a common mycelium. Rev. de Microb., 27: 30-35, 1996.
• ²⁴
  Mosse, B. Specificit in VA mycorrhizas. In: Sanders, F.E.; Mosse, B.; Tinker, P.B. Endomycorrhizas. Academic Press, London, 1975, 469-484 pp.
• ²⁵
  Newman, E.I. Mycorrhizal links between plants: their functioning and ecological significance. Adv. in Ecol. Res., 18:243-270, 1988.
• ²⁶
  Newman, E.I.; Eason, W.R. Rates of phosphorus transfer within and between ryegrass (Lolium perenne) plants. Funct. Ecol., 7: 242-248, 1993.
• ²⁷
  Rao, A.V.; Giller, K.E. Nitrogen fixation and its transfer from Leucaena to Grass using N¹⁵ . Ecol. Manag., 61: 221-227, 1994.
• ²⁸
  Read, D.J. The structure and function of the vegetative mycelium of mycorrhizal roots. In: Jennings, D.H.; Rayner, A.D.M. The Ecology and Physiology of the Fungal Mycelium, Cambridge: Cambridge University Press. 1984, 215-240 pp.
• ²⁹
  Read, D.J.; Birch, C.P.D. The effects and implications of disturbance of mycorrhizal mycelial systems. Proc. Royal Soc. Edinb., 94: 13-24, 1986.
• ³⁰
  Read, D.J.; Kouchecki, H.K.; Hodgson , J. VA mycorrhiza in natural vegetation systems. I The occurrence of infection. New Phytol., 77: 641-53, 1976.
• ³¹
  Ritz, K.; Newman, E.I. Evidence for rapid cycling of phosphorus from dying roots to living plants. Oikos, 45: 174-180, 1985.
• ³²
  Tomm, G.O.; Kessel, G.V.; Slinkard, A.E. Bidirectional transfer of nitrogen between alfafa and bromegrass: Short and long term evidence. Plant and Soil 164: 77-86, 1994. 
• ³³
  Tommerup, I.C. Spore dormancy in VA mycorrhizal fungi. Trans. Br. Mycol. Soc., 81: 37-45, 1983.
• ³⁴
  Van Kessel, C.; Singleton, P.W.; Hoben, H. Enhanced N-transfer from a soybean to maize by VA mycorrhizal fungi. Plant Physiol., 79:562-563, 1985.
• ³⁵
  Whittingham, J.; Read, D.J. Nutrient transfer between plants with mycorrhizal interconnections: Vesicular-arbuscular mycorrhiza in natural vegetation systems. New Phytol., 90: 277-284, 1981.

Publication Dates

• Publication in this collection
  27 May 1999
• Date of issue
  Oct 1998

History

• Accepted
  23 July 1998
• Reviewed
  04 June 1998
• Received
  07 July 1997