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Respiratory Costs of Mycorrhizal Associations

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Plant Respiration

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 18))

Summary

Mycorrhizal fungi form symbiotic and often mutually beneficial relationships with the roots of most terrestrial plants. In this chapter we review current literature concerned with plant respiratory requirements for supporting this important plant-fungal association, and its effect on the overall plant carbon economy. Controlled studies indicate that mycorrhizal respiratory costs are considerable, consuming between 2 to 17% of the photosynthate fixed daily, varying depending on the host and fungal species involved, the stage of colonization, and the environmental conditions. Respiratory energy is required by the mycobiont for construction of new intraradical and extraradical fungal tissue (including reproductive structures), for maintenance and repair of existing fungal tissue, and for cellular processes in the fungal tissue associated with the absorption, translocation and transfer of nutrients from the soil to the host. Additional respiration is also required by the host plant for stimulated root cellular processes, and potentially for increased production of root biomass. Field studies of these important processes will eventually lead us to better understand how significant mycorrhizal fungi are to the total carbon budgets of natural and managed plant communities.

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References

  • Abuzinadah RA and Read DJ (1986) The role of proteins in the nitrogen nutrition of ectomycorrhizal plants. III. Protein utilization by Betula, Picea and Pinus in ectomycorrhizal association with Hebeloma crustuliniforme. New Phytol 103: 506–514

    Google Scholar 

  • Amijee F, Tinker PB and Stribley DP (1989) The development of endomycorrhizal root systems. VII. A detailed study of effects of soil phosphorus on colonization. New Phytol 111: 435–446

    Google Scholar 

  • An ZQ, Guo BZ and Hendrix JW (1993) Populations of spores and propagules of mycorrhizal fungi in relation to the life-cycles of tall fescue and tobacco. Soil Biol Biochem 25: 813–817

    Article  Google Scholar 

  • Anderson CP (2003) Source-sink balance and carbon allocation below ground in plants exposed to ozone. New Phytol 157: 213–228

    Google Scholar 

  • Andersen CP and Rygiewicz PT (1995) Allocation of carbon in mycorrhizal Pinus ponderosa seedlings exposed to ozone. New Phytol 131: 471–480

    CAS  Google Scholar 

  • Andrews JA, Harrison KG, Matamala R and Schlesinger WH (1999) Separation of root respiration from soil respiration using carbon-13 labeling during Free-Air Carbon Enrichment (FACE). J Soil Sci Soc Am 63: 1429–1435

    CAS  Google Scholar 

  • Antibus RK and Sinsabaugh RL (1993) The extraction and quantification of ergosterol from ectomycorrhizal fungi and roots. Mycorrhiza 3: 137–144

    Article  CAS  Google Scholar 

  • Azcón-Aguilar C and Barea JM (1992) Interactions between mycorrhizal fungi and other rhizosphere microorganisms. In: Allen MF (ed) Mycorrhizal Functioning. An Integrative Plant-Fungal Process, pp. 163–198. Chapman and Hall, New York

    Google Scholar 

  • Baas R and Lambers H (1988) Effects of vesicular-arbuscular mycorrhizal infection and phosphate on Plantago major spp. pleiosperma in relation to the internal phosphate concentration. Physiol Plant 74: 701–707

    CAS  Google Scholar 

  • Baas R, Werf AVD and Lambers H (1989) Root respiration and growth in Plantago major as affected by vesicular-arbuscular mycorrhizal infection. Plant Physiol 91: 227–232

    Google Scholar 

  • Bago B, Pfeffer PE, Douds DD, Brouillette J, Bécard G and Shachar-Hill Y (1999) Carbon metabolism in spores of the arbuscular mycorrhizal fungus Glomus intraradices as revealed by nuclear magnetic resonance spectroscopy. Plant Physiol 121: 263–272

    Article  PubMed  CAS  Google Scholar 

  • Bago B, Pfeffer PE, Zipfel W, Lammers P and Shachar-Hill Y (2002) Tracking metabolism and imaging transport in arbuscular mycorrhizal fungi. Plant Soil 244: 189–197

    Article  CAS  Google Scholar 

  • Ball AS and Drake BG (1998) Stimulation of soil respiration by carbon dioxide enrichment of marsh vegetation. Soil Biol Biochem 30: 1203–1205

    Article  CAS  Google Scholar 

  • Berta G, Tagliasacchi AM, Fusconi A, Gerlero D and Trotta A (1991) The mitotic cycle in root apical meristems of Allium porrum L. is controlled by the mycorrhizal fungus Glomus sp. Strain E. Protoplasma 161: 12–16

    Article  Google Scholar 

  • Berta G, Fusconi A, Lingua G, Trotta A and Sgorbati S (1996) Influence of arbuscular mycorrhizal infection on nuclear structure and activity during root morphogenesis. In: Azcón-Aguilar C and Barea JM (eds) Mycorrhizas in Integrated Systems: From Genes to Plant Development, pp 174–177. European Commission, Brussels

    Google Scholar 

  • Bidartondo MI, Ek H, Wallander H and Söderström B (2001) Do nutrient additions alter carbon sink strength of ectomycorrhizal fungi? New Phytol 151: 543–550

    Article  CAS  Google Scholar 

  • Bloom AJ, Chapin III FS and Mooney HA (1985) Resource limitations in plants—an economic analogy. Annu Rev Ecol Syst 16: 363–392

    Google Scholar 

  • Bouma TJ and Bryla DR (2000) On the assessment of root respiration for soils of different textures: Interactions with soil moisture and soil CO2 concentrations. Plant Soil 227: 215–221

    Article  CAS  Google Scholar 

  • Bouma TJ, Bryla DR, Li Y and Eissenstat DM (2000) Is maintenance respiration in roots constant? In: Stokes A (ed) The Supporting Roots of Trees and Woody Plants: Form, Function and Physiology, Vol 87, pp 391–396. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Bouma TJ, Yanai RD, Elkin AD, Hartmond U, Flores-Alva DE and Eissenstat DM (2001) Estimating age-dependent costs and benefits of roots with contrasting life span: Comparing apples and oranges. New Phytol 150: 685–695

    Article  Google Scholar 

  • Brouwer R (1983) Functional equilibrium: Sense or nonsense? Neth J Agric Sci 31: 335–348

    Google Scholar 

  • Bryla DR and Koide RT (1990) Role of mycorrhizal infection in the growth and reproduction of wild vs. cultivated plants. II. Eight wild accessions and two cultivars of Lycopersicon esculentum Mill. Oecologia 84: 82–92

    Google Scholar 

  • Bryla DR, Bouma TJ and Eissenstat DM (1997) Root respiration in citrus acclimates to temperature and slows during drought. Plant, Cell Environ 20: 1411–1420

    Article  Google Scholar 

  • Bryla DR, Bouma TJ, Hartmond U and Eissenstat DM (2001) Influence of temperature and soil drying on respiration of individual roots in citrus: Integrating greenhouse observations into a predictive model for the field. Plant, Cell Environ 24: 781–790

    Article  Google Scholar 

  • Bücking H and Heyser W (2003) Uptake and transfer of nutrients in ectomycorrhizal associations: Interactions between photosynthesis and phosphate nutrition. Mycorrhiza 13: 59–68

    PubMed  Google Scholar 

  • Burgess T, Dell B and Malajczuk N (1994) Variation in mycorrhizal development and growth stimulation of 20 isolates of Pisolithus inoculated onto Eucalyptus grandis W. Hill ex Maiden. New Phytol 127: 731–739

    Google Scholar 

  • Burton AJ, Pregitzer KS, Zogg GP and Zak DR (1998) Drought reduces root respiration in sugar maple forest. Ecol Appl 8: 771–778

    Google Scholar 

  • Burton AJ, Pregitzer KS, Ruess RW, Hendrik RL and Allen MF (2002) Root respiration in North American forests: Effects of nitrogen concentration and temperature across biomes. Oecologia 131: 559–568

    Google Scholar 

  • Buwalda JG and Goh KM (1982) Host-fungus competition for carbon as a cause of growth depressions in vesicular-arbuscular mycorrhizal ryegrass. Soil Biol Biochem 14: 103–106

    Article  CAS  Google Scholar 

  • Cairney JWG and Alexander IJ (1992) A study of spruce (Picea sitchensis (Bong.) Carr.) ectomycorrhizas. II. Carbohydrate allocation to ageing Picea sitchenis/Tylospora fibrillosa (Burt.) Donk ectomycorrhizas. New Phytol 122: 153–158

    CAS  Google Scholar 

  • Cairney JWG, Ashford AE, and Allaway WG (1989) Distribution of photosynthetically fixed carbon within root systems of Eucalyptus pilularis plants ectomycorrhizal with Pisolithus tinctorius. New Phytol 112: 495–500

    Google Scholar 

  • Chambers CA, Smith SE and Smith FA (1980) Effects of ammonium and nitrate ions on mycorrhizal infection, nodulation and growth of Trifolium subterraneum. New Phytol 85: 47–62

    CAS  Google Scholar 

  • Colpaert JV, van Assche JA and Luijtens K (1992) The growth of the extramatrical mycelium of ectomycorrhizal fungi and the growth response of Pinus sylvestris L. New Phytol 120: 127–135

    Google Scholar 

  • Cox G, Sanders FE, Tinker PB and Wild JA (1975) Ultrastructural evidence relating to host-endophyte transfer in a vesicular-arbuscular mycorrhiza. In: Sanders FE, Mosse B and Tinker PB (eds) Endomycorrhizas, pp. 297–312. Academic Press, London

    Google Scholar 

  • de Miranda JCC, Harris PJ and Wild A (1989) Effects of soil and plant phosphorus concentration on vesicular-arbuscular mycorrhiza in sorghum plants. New Phytol 112: 405–410

    Google Scholar 

  • Douds DD Jr, Johnson CR and Koch KE (1988) Carbon cost of the fungal symbiont relative to net leaf P accumulation in a split-root VA mycorrhizal symbiosis. Plant Physiol 86: 491–496

    CAS  Google Scholar 

  • Douds DD, Pfeffer PE and Shachar-Hill Y (2000) Carbon partitioning, cost and metabolism of arbuscular mycorrhizae. In: Kapulnick Y and Douds DD (eds) Arbuscular Mycorrhizas: Physiology and Function, pp. 107–130. Kluwer Academic Press, New York

    Google Scholar 

  • Durall DM, Jones MD and Tinker PB (1994) Allocation of 14Ccarbon in ectomycorrhizal willow. New Phytol 128: 109–114

    CAS  Google Scholar 

  • Eissenstat DM, Graham JH, Syvertsen JP and Drouillard DL (1993) Carbon economy of sour orange in relation to mycorrhizal colonization and phosphorus status. Ann Bot 71: 1–10

    Article  CAS  Google Scholar 

  • Eltrop L and Marschner H (1996) Growth and mineral nutrition of non-mycorrhizal and mycorrhizal Norway spruce (Picea abies) seedlings grown in semi-hydroponic sand culture. II. Carbon partitioning in plants supplied with ammonium or nitrate. New Phytol 133: 479–486

    CAS  Google Scholar 

  • Espeleta JF and Eissenstat DM (1998) Responses of citrus fine roots to localized soil drying: A comparison of seedlings with adult fruit trees. Tree Physiol 18: 113–119

    PubMed  Google Scholar 

  • Espeleta JF, Eissenstat DM and Graham JH (1998) Citrus root responses to localized drying soil: A new approach to studying mycorrhizal effects on the root of mature trees. Plant Soil 206: 1–10

    Article  CAS  Google Scholar 

  • Estaún V, Calvet C and Hayman DS (1987) Influence of plant genotype on mycorrhizal infection: Response of three pea cultivars. Plant Soil 103: 295–298

    Google Scholar 

  • Finlay R and Söderström B (1992) Mycorrhiza and carbon flow to the soil. In: MF Allen (ed), Mycorrhizal Functioning. An Integrative Plant-Fungal Process, pp. 134–160. Chapman & Hall, New York

    Google Scholar 

  • Fitter AH, Graves JD, Watkins NK, Robinson D and Scrimgeour C (1998) Carbon transfer between plants and its control in networks of arbuscular mycorrhizas. Funct Ecol 12: 406–412

    Article  Google Scholar 

  • Francis R and Read DJ (1984) Direct transfer of carbon between plants connected by vesicular-arbuscular mycorrhizal fungi. Nature 307: 53–56

    Article  CAS  Google Scholar 

  • Fredeen AL and Terry N (1988) Influence of vesicular-arbuscular mycorrhizal infection and soil phosphorus level on growth and carbon metabolism of soybean. Can J Bot 66: 2311–2316

    Google Scholar 

  • Frey B and Schüepp H (1992) Transfer of symbiotically fixed nitrogen from berseem (Trifolium alexandrium L.) to maize via vesicular arbuscular mycorrhizal hyphae. New Phytol 122: 447–454

    CAS  Google Scholar 

  • Gansert D (1994) Root respiration and its importance for the carbon balance of beech saplings (Fagus slyvatica L.) in a montane beech forest. Plant Soil 167: 109–119

    Article  CAS  Google Scholar 

  • Garbaye J (1994) Helper bacteria: A new dimension to the mycorrhizal symbiosis. New Phytol 128: 197–210

    Google Scholar 

  • Giovannetti M and Hepper CM (1985) Vesicular-arbuscular mycorrhizal infection in Hedysarum coronarium and Onobrychis viciifolia: Host-endophyte specificity. Soil Biol Biochem 17: 899–900

    Article  Google Scholar 

  • Gorissen A, Joosten NN and Jansen AE (1991) Effects of ozone and ammonium-sulfate on carbon partitioning to mycorrhizal roots of juvenile Douglas fir. New Phytol 119: 243–250

    CAS  Google Scholar 

  • Graham JH and Eissenstat DM (1994) Host genotype and the formation and function of VA mycorrhizae. Plant Soil 159: 179–185

    Google Scholar 

  • Graham JH, Leonard RT and Menge JA (1982a) Interactions of light intensity and soil temperature with phosphorus inhibition of vesicular-arbuscular mycorrhizal formation. New Phytol 91: 683–690

    CAS  Google Scholar 

  • Graham JH, Linderman RG and Menge JA (1982b) Development of external hyphae by different isolates of mycorrhizal Glomus spp. in relation to root colonization and growth of Troyer citrange. New Phytol 91: 183–189

    Google Scholar 

  • Graham JH, Hodge NC and Morton JB (1995) Fatty acid methyl ester profiles for characterization of Glomalean fungi and their mycorrhizae. Appl Environ Microbiol 61: 58–64

    CAS  Google Scholar 

  • Graves JD, Watkins NK, Fitter AH, Robinson D and Scrimgeour C (1997) Instraspecific transfer of carbon between plants linked by a common mycorrhizal network. Plant Soil 192: 153–159

    Article  CAS  Google Scholar 

  • Grime JP, Mackey JML, Hillier SH and Read DJ (1987) Floristic diversity in a model system using experimental microcosms. Nature 328: 420–422

    Article  Google Scholar 

  • Harris D, Packovsky RS and Paul EA (1985) Carbon economy of soybean-Rhizobium-Glomus associations. New Phytol 101: 427–440

    CAS  Google Scholar 

  • Haselwandter K, Bobleter O and Read DJ (1990) Degradation of 14C-labelled lignin and dehydropolymer of coniferyl alcohol by ericoid and ectomycorrhizal fungi. Arch Microbiol 153: 352–354

    Article  CAS  Google Scholar 

  • Hawkins HJ, Cramer MD and George E (1999) Root respiratory quotient and nitrate uptake in hydroponically grown non-mycorrhizal and mycorrhizal wheat. Mycorrhiza 9: 57–60

    Article  CAS  Google Scholar 

  • Hayman DS (1970) Endogone spore number in soil and vesicular-arbuscular mycorrhiza in wheat as influenced by season and soil treatment. Trans British Mycol Soc 54: 53–63

    Google Scholar 

  • Henry A and Kosola K (1999) Root age and phosphorus effects on colonization of Andropogon gerardii by mycorrhizal fungi. Soil Biol Biochem 31: 1657–1660

    Article  CAS  Google Scholar 

  • Hepper CM (1977) A colorimetric method for estimating vesicular-arbuscular mycorrhizal infection in roots. Soil Biol Biochem 9: 15–18

    Article  Google Scholar 

  • Ho I and Trappe JM (1973) Translocation of 14C from Festuca plants to their endomycorrhizal fungi. Nature 244: 30–31

    CAS  Google Scholar 

  • Ho I and Trappe JM (1981) Effects of ozone exposure on mycorrhiza formation and growth of Festuca arundinacea. Environ Exp Bot 24: 71–74

    Google Scholar 

  • Högberg MN and Högberg P (2002) Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest. New Phytol 154: 791–795.

    Google Scholar 

  • Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Lofvenius M and Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411: 789–792

    PubMed  Google Scholar 

  • Hungate BA, Holland EA, Jackson RB, Chapin FS III, Mooney HA and Field CB (1997) The fate of carbon in grasslands under carbon dioxide enrichment. Nature 388: 576–579

    Article  CAS  Google Scholar 

  • Ineichen K, Wiemken V and Wiemken A (1995) Shoots, roots and ectomycorrhiza formation of pine seedlings at elevated atmospheric carbon dioxide. Plant Cell Environ 18: 703–709

    Google Scholar 

  • Ingestad T, Arveby A and Kähr M (1986) The influence of ectomycorrhiza on nitrogen nutrition and growth of Pinus sylvestris seedlings. Physiol Plant 68: 575–582

    Google Scholar 

  • Jabaji-Hare S (1988) Lipid and fatty acid profiles of some vesicular-arbuscular mycorrhizal fungi: Contribution to taxonomy. Mycologia 80: 622–629

    CAS  Google Scholar 

  • Jackobsen I and Rosendahl L (1990) Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol 115: 77–83

    Google Scholar 

  • Jackobsen I, Abbott LK and Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots. New Phytol 120: 371–380

    Google Scholar 

  • Jifon JL, Graham JH, Drouillard DL and Syvertsen JP (2002) Growth depression of mycorrhizal citrus seedlings grown at high phosphorus supply is mitigated by elevated CO2. New Phytol 153: 133–142

    Article  Google Scholar 

  • Johnson C (1994) Fruiting of hypogeous fungi in dry sclerophyll forest in Tasmania, Australia — seasonal variation and annual production. Can J Bot 98: 1173–1182

    Google Scholar 

  • Johnson D, Leake JR and Read DJ (2002a) Transfer of recent photosynthate into mycorrhizal mycelium of an upland grassland: Short-term respiratory losses and accumulation of 14C. Soil Biol Biochem 34: 1521–1524

    CAS  Google Scholar 

  • Johnson D, Leake JR, Ostle N, Ineson P and Read DJ (2002b) In situ 13CO2 pulse-labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil. New Phytol 153: 327–334

    Article  CAS  Google Scholar 

  • Jones MD, Durall DM and Tinker PB (1990) Phosphorus relationships and production of extramatrical hyphae by two types of willow ectomycorrhizas at different soil phosphorus levels. New Phytol 115: 259–267

    CAS  Google Scholar 

  • Koch KE and Johnson CR (1984) Photosynthesis partitioning in split-root citrus seedlings with mycorrhizal and nonmycorrhizal root systems. Plant Physiol 75: 26–30

    CAS  Google Scholar 

  • Koide RT (1985) The nature of growth depressions in sunflower caused by vesicular-arbuscular mycorrhizal infection. New Phytol 99: 449–462

    Google Scholar 

  • Koide R and Elliott G (1989) Cost, benefit and efficiency of the vesicular-arbuscular mycorrhizal symbiosis. Funct Ecol 3: 249–255

    Google Scholar 

  • Koide RT and Li M (1990) On host regulation of the vesicular-arbuscular mycorrhizal symbiosis. New Phytol 114: 59–65

    Google Scholar 

  • Koide RT and Dickie IA (2002) Effects of mycorrhizal fungi on plant populations. Plant Soil 244: 307–317

    Article  CAS  Google Scholar 

  • Krishna KR, Shetty KG, Dart PJ and Andrews DJ (1985) Genotype dependent variation in mycorrhizal colonization and response to inoculation of pearl millet. Plant Soil 86: 113–125

    Article  Google Scholar 

  • Kucy RMN and Paul EA (1982) Carbon flow, photosynthesis, and N2 fixation in mycorrhizal and nodulated faba beans (Vicia faba L.). Soil Biol Biochem 14: 407–412

    Google Scholar 

  • Kutsch WL, Staack A, Wojtzel J, Middlehoff U and Kappen L (2001) Field measurements of root respiration and total soil respiration in an alder forest. New Phytol 150: 157–168

    Article  Google Scholar 

  • Lambers H, Atkins OK and Millenaar FF (2002) Respiratory patterns in roots in relation to their functioning. In: Waisel Y, Eshel A and Kafkafi U (eds) Plant Roots. The Hidden Half. Third Edition, pp. 521–552. Marcel Dekker, Inc., New York

    Google Scholar 

  • Lamhamedi MS, Godbout C and Fortin JA (1994) Dependence of Laccaria bicolor basidiome development on current photosynthesis of Pinus strobus seedlings. Can J For Res 24: 1797–1804

    Google Scholar 

  • Last FT, Pelham J, Mason PA and Ingleby K (1979) Influence of leaves on sporophore production by fungi forming sheating mycorrhizas with Betula spp. Nature 180: 168–169

    Google Scholar 

  • Lerat S, Lapointe L, Gutjahr S, Piché Y and Vierheilig H (2003) Carbon partitioning in a split-root system of arbuscular mycorrhizal plants is fungal and plant species dependent. New Phytol 157: 589–595

    Article  Google Scholar 

  • Lewis DH and Harley JH (1965a) Carbohydrate physiology of mycorrhizal roots of beech. I. Identity of endogenous sugars and utilization of exogenous sugars. New Phytol 64: 224–231

    CAS  Google Scholar 

  • Lewis DH and Harley JH (1965b) Carbohydrate physiology of mycorrhizal roots of beech. II. Utilization of exogenous sugars by uninfected and mycorrhizal roots. New Phytol 64: 238–255

    CAS  Google Scholar 

  • Lewis DH and Harley JH (1965c) Carbohydrate physiology of mycorrhizal roots of beech. III. Movement of sugars between host and fungus. New Phytol 64: 256–269

    CAS  Google Scholar 

  • Linderman RG (1992) Vesicular-arbuscular mycorrhizae and soil microbial interactions. In: Bethlenfalvay GJ and Linderman RG (eds) Mycorrhizae in Sustainable Agriculture, pp 45–70. ASA Special Publication Number 54, ASA-CSSA-SSSA, Madison

    Google Scholar 

  • Ling-Lee M, Ashford AE and Chilvers GA (1977) A histochemical study of polysaccharide distribution in eucalypt mycorrhizas. New Phytol 78: 329–335

    CAS  Google Scholar 

  • Lioi L and Giovannetti M (1987) Variable effectivity of three vesicular-arbuscular mycorrhizal endophytes in Hedysarum coronarium and Medicago sativa. Biol Fertil Soils 4: 193–197

    Article  Google Scholar 

  • Lu SJ, Mattson KG, Zaerr JB and Marshall JD (1998) Root respiration of Douglas fir seedlings: Effects of N concentration. Soil Biol Biochem 30: 331–336

    Article  CAS  Google Scholar 

  • Maijala P, Fagerstedt KF and Raudaskoski M (1991) Detection of extracellular cellulolytic and proteolytic activity in ectomycorrhizal fungi and Heterobasidion annosum (Fr.) Bref. New Phytol 117: 643–648

    CAS  Google Scholar 

  • Marschner H (1995) Mineral Nutrition of Higher Plants, 2nd Edition. Academic Press: New York.

    Google Scholar 

  • Martin F, Ramstedt M and Soderhall K (1987) Carbon and nitrogen metabolism in ectomycorrhizal and ectomycorrhizas. Biochimie 69: 569–581

    Article  PubMed  CAS  Google Scholar 

  • McCool PM and Menge JA (1984) Influence of ozone on carbon partitioning in tomato: Potential role of carbon flow in regulation of mycorrhizal symbiosis under conditions of stress. New Phytol 94: 241–247

    Google Scholar 

  • Meier S, Grand LF, Schoeneberger MM, Reinert RA and Bruck RI (1990) Growth, ectomycorrhizae and nonstructural carbohydrates of loblolly pine seedlings exposed to ozone and soil water deficit. Environ Poll 64: 11–27

    Article  CAS  Google Scholar 

  • Menge JA (1984) Inoculum production. In: Powell CL and Bagyaraj DJ (eds) VA Mycorrhiza, pp. 187–203. CRC Press, Inc., Boca Raton

    Google Scholar 

  • Miller RM, Reinhardt DR and Jastrow JD (1995) External hyphal production of vesicular-arbuscular mycorrhizal fungi in pasture and tallgrass prairie communities. Oecologia 103: 17–23

    Article  Google Scholar 

  • Modjo HS and Hendrix JW (1986) The mycorrhizal fungus, Glomus macrocarpum as a cause of tobacco stunt disease. Phytopath 76: 668–691

    Google Scholar 

  • Molina R and Chamard J (1983) Use of the ectomycorrhizal fungus Laccaria laccata in forestry. II. Effects of fertilizer forms and levels on ectomycorrhizal development and growth of container-grown Douglas-fir and ponderosa pine. Can J For Res 13: 89–95

    Google Scholar 

  • Nagy S and Nordby HE (1980) Composition of lipids in roots of six citrus cultivars infected with the vesicular-arbuscular mycorrhizal fungus, Glomus mosseae. New Phytol 85: 377–384

    CAS  Google Scholar 

  • Newman EI and Reddell P (1987) The distribution of mycorrhizas among families of vascular plants. New Phytol 106: 745–751

    Google Scholar 

  • Newman EI, Ritz K and Jupp AP (1989) The functioning of roots in the grassland ecosystem. Asp Appl Biol 22: 263–269

    Google Scholar 

  • Nielson KL, Bouma TJ, Lynch JP and Eissenstat DM (1998) Effect of phosphorus availability and vesicular-arbuscular mycorrhizas on the carbon budget of common bean (Phaseolus vulgaris). New Phytol 139: 647–656

    Google Scholar 

  • Nilsson LO and Wallander H (2003) Production of external mycelium by ectomycorrhizal fungi in a Norway spruce forest was reduced in response to nitrogen fertilizer. New Phytol 158: 409–416

    Article  Google Scholar 

  • Olsson PA (1999) Signature of fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol Ecol 29: 303–310

    CAS  Google Scholar 

  • Olsson PA and Johansen A (2000) Lipid and fatty acid composition of hyphae and spores of arbuscular mycorrhizal fungi at different growth stages. Mycol Res 104: 429–434

    CAS  Google Scholar 

  • Pacovsky RS and Fuller G (1988) Mineral and lipid composition of Glycine-Glomus-Bradyrhizobium symbioses. Physiol Plant 72: 733–746

    CAS  Google Scholar 

  • Palta JA and Nobel PS (1989a) Influences of water status, temperature, and root age on daily patterns of root respiration for two cactus species. Ann Bot 63: 651–662

    Google Scholar 

  • Palta JA and Nobel PS (1989b) Root respiration for Agave deserti: Influence of temperature, water status, and root age on daily patterns. J Exp Bot 40: 181–186

    Google Scholar 

  • Pang PC and Paul EA (1980) Effects of vesicular-arbuscular mycorrhiza on 14C and 15N distribution in nodulated fababeans. Can J Soil Sci 60: 241–250

    CAS  Google Scholar 

  • Paul EA and Kucey RMN (1981) Carbon flow in plant microbial associations. Science 213: 473–474

    CAS  Google Scholar 

  • Pearson JN and Jakobsen I (1993) Symbiotic exchange of carbon and phosphorus between cucumber and three arbuscular mycorrhizal fungi. New Phytol 124: 481–488

    CAS  Google Scholar 

  • Peng SB, Eissenstat DM, Graham JH, Williams K and Hodge NC (1993) Growth depression in mycorrhizal citrus at high-phosphorus supply. Plant Physiol 101: 1063–1071

    PubMed  CAS  Google Scholar 

  • Perotto S and Bonfante P (1997) Bacterial association with mycorrhizal fungi: Close and distant friends in the rhizosphere. Trends Microbiol 5: 496–501

    Article  PubMed  CAS  Google Scholar 

  • Piché Y, Fortin JA and Lafontaine JG (1981) Cytoplasmic phenols and polysaccharides in ectomycorrhizal and nonmycorrhizal short roots of pine. New Phytol 88: 695–703

    Google Scholar 

  • Plassard C, Barry D, Eltrop L and Mousain D (1994) Nitrate uptake in maritime pine (Pinus pinaster Soland in Ait.) and the ectomycorrhizal fungus Hebeloma cylindrosporum: Effect of ectomycorrhizal symbiosis. Can J Bot 72: 189–197

    Google Scholar 

  • Read DJ (1992) The mycorrhizal mycelium. In: MF Allen (ed), Mycorrhizal Functioning. An Integrative Plant-Fungal Process, pp. 102–133. Chapman & Hall, New York

    Google Scholar 

  • Read DJ and Boyd R (1986) Water relations of mycorrhizal fungi and their host plants. In: Ayres P and Boddy L (eds) Water, Fungi and Plants, pp. 287–303. Cambridge University Press, Cambridge

    Google Scholar 

  • Reich PB (2002) Root-shoot relations: Optimality in acclimation and adaptation or the ‘Emperor’s New Clothes?’ In: Waisel Y, Eshel A and Kafkafi U (eds) Plant Roots. The Hidden Half. Third Edition, pp 205–220. Marcel Dekker, Inc., New York

    Google Scholar 

  • Reich PB, Schoettle AW, Stroo HF and Amundson RG (1986) Acid rain and ozone influence mycorrhizal infection in tree seedlings. J Air Pollution Control Association 36: 724–726

    CAS  Google Scholar 

  • Reid CPP, Kidd FA and Ekwebelam SA (1983) Nitrogen nutrition, photosynthesis and carbon allocation to ectomycorrhizal pine. Plant Soil 71: 415–432

    Article  CAS  Google Scholar 

  • Rillig MC, Allen MF, Klironomos JN and Field CB (1998) Arbuscular mycorrhizal percent root infection and infection intensity of Bromus hordeaceous grown in elevated atmospheric CO2. Mycologia 90: 199–205

    Google Scholar 

  • Robinson D and Fitter AH (1999) The magnitude and control of carbon transfer between plants linked by a common mycorrhizal network. J Exp Bot 50: 9–13

    Article  CAS  Google Scholar 

  • Rouhier H and Read DJ (1998) The role of mycorrhiza in determining the response of Plantago lanceolata to CO2 enrichment. New Phytol 139: 367–373

    Article  Google Scholar 

  • Rousseau JVD and Reid CPP (1991) Effects of phosphorus fertilization and mycorrhizal development on phosphorus nutrition and carbon balance of loblolly pine. New Phytol 117: 319–326

    CAS  Google Scholar 

  • Rousseau JVD, Sylvia DM and Fox AJ (1994) Contribution of ectomycorrhizas to the potential nutrient absorbing surface of pine. New Phytol 128: 639–644

    Google Scholar 

  • Rygiewicz PT and Andersen CP (1994) Mycorrhizae alter quality and quantity of carbon allocated below ground. Nature 369: 58–60

    Article  Google Scholar 

  • Sanders FE, Tinker PB, Black RLB and Palmerley SM (1977) The development of endomycorrhizal root systems. I. Spread of infection and growth promoting effects with four species of vesicular-arbuscular mycorrhizas. New Phytol 78: 257–268

    Google Scholar 

  • Sanders IR (1996) Plant-fungal interactions in a CO2-rich world. In: Korner C and Bazzaz FA (eds) Carbon Dioxide, Populations, and Communities, pp. 265–272. Academic Press, New York

    Google Scholar 

  • Sanders IR, Streitwolf-Engel R, van der Heijden MGA, Boller T and Wiemken A (1998) Increased allocation to external hyphae of arbuscular mycorrhiza fungi under CO2 enrichment. Oecologia 117: 496–503

    Article  Google Scholar 

  • Scagel CF and Andersen CP (1997) Seasonal changes in root and soil respiration of ozone-exposed Ponderosa pine (Pinus ponderosa) grown in different substrates. New Phytol 136: 627–643

    Article  CAS  Google Scholar 

  • Sieverding E, Toro S and Mosquera O (1989) Biomass production and nutrient concentrations in spores of VA mycorrhizal fungi. Soil Biol Biochem 21: 60–72

    Article  Google Scholar 

  • Simard SW, Perry DA, Jone MD, Myrold DD, Durall DM and Molina R (1997) Net carbon transfer between ectomycorrhizal tree species in the field. Nature 388: 579–582

    Article  CAS  Google Scholar 

  • Simmons GL and Kelly JM (1989) Influence of O3, rainfall acidity, and soil Mg status on growth and ectomycorrhizal colonization of loblolly pine roots. Water Air Soil Poll 44: 159–171

    Article  CAS  Google Scholar 

  • Smith SE and Read DJ (1997) Mycorrhizal Symbiosis. Second Edition. Academic Press, New York

    Google Scholar 

  • Snellgrove RC, Splittstoesser WE, Stribley DP and Tinker PB (1982) The distribution of carbon and the demand of the fungal symbiont in leek plants with vesicular-arbuscular mycorrhizas. New Phytol 92: 75–87

    Google Scholar 

  • Söderström BE and Read DJ (1987) Respiratory activity of intact and excised ectomycorrhizal mycelial systems growing in unsterilized soil. Soil Biol Biochem 19: 231–236

    Google Scholar 

  • Son CL and Smith SE (1988) Mycorrhizal growth responses: Interactions between photon irradiance and phosphorus nutrition. New Phytol 108: 305–314

    Google Scholar 

  • Staddon PL, Fitter AH and Robinson D (1999) Effects of mycorrhizal colonization and elevated atmospheric carbon dioxide on carbon fixation and below-ground carbon partitioning in Plantago lanceolata. J Exp Bot 50: 853–860

    Article  CAS  Google Scholar 

  • Stroo HF, Reich PB, Schoettle AW and Amundson RG (1988) Effects of ozone and acid rain on white pine (Pinus strobus) seedlings grown in five soils. II. Mycorrhizal infection. Can J Bot 66: 1510–1516

    CAS  Google Scholar 

  • Taylor J and Harrier L (2000) A comparison of nine species of arbuscular mycorrhizal fungi on the development and nutrition of micropropagated Rubus idaeus L. cv. Glen Prosen (Red Raspberry). Plant Soil 225: 53–61

    Article  CAS  Google Scholar 

  • Tester M, Smith SE, Smith FA and Walker NA (1986) Effects of photon irradiance on the growth of shoots and roots, on the rate of initiation of mycorrhizal infection and the growth of infection units in Trifolium subterraneum L. New Phytol 103: 375–390

    Google Scholar 

  • Thomson BD, Robson AD and Abbott LK (1986) Effects of phosphorus on the formation of mycorrhizas by Gigaspora calospora and Glomus fasciculatum in relation to root carbohydrates. New Phytol 103: 751–765

    Google Scholar 

  • Tinker PB and Nye PH (2000) Solute Movement in the Rhizosphere. Oxford University Press, Oxford

    Google Scholar 

  • Tinker PB, Durall DM and Jones MD (1994) Carbon use efficiency in mycorrhizas: Theory and sample calculations. New Phytol 128: 115–122

    CAS  Google Scholar 

  • Tisdall JM and Oades JM (1979) Stabilization of soil aggregates by the root systems of ryegrass. Aust J Soil Res 17: 429–441

    Article  Google Scholar 

  • Toro M, Azcon R and Barea JM (1997) Improvement of arbuscular mycorrhiza development by inoculation of soil with phosphate bacteria to improve rock phosphate bioavailability (32P) and nutrient cycling. Appl Environ Microbiol 63: 4408–4412

    CAS  Google Scholar 

  • Trappe JM (1987) Phylogenetic and ecological aspects of mycotrophy in the angiosperms from an evolutionary standpoint. In: Safir GR (ed) Ecophysiology of VA Mycorrhizal Plants, pp 5–25. CRC Press, Boca Raton

    Google Scholar 

  • Van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A and Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69–72

    Google Scholar 

  • Veen BW (1981) Relation between root respiration and root activity. Plant Soil 63: 73–76

    CAS  Google Scholar 

  • Vogt KA, Grier CC, Meier CE and Edmonds RL (1982) Mycorrhizal role in net primary production and nutrient cycling in Abies amabilis ecosystems in western Washington. Ecology 63: 370–380

    Google Scholar 

  • Vogt KA, Publicover DA and Vogt DJ (1991) A critique of the role of ectomycorrhizas in forest ecology. Agric, Ecosyst Environ 35: 171–190

    Google Scholar 

  • Wallander H and Nylund J-E (1991) Effects of excess nitrogen on carbohydrate concentration and mycorrhizal development of Pinus sylvestris seedlings. New Phytol 119: 405–411

    CAS  Google Scholar 

  • Wallander H and Nylund J-E (1992) Effects of excess nitrogen and phosphorus starvation on the extramatrical mycelium of ectomycorrhizas of Pinus sylvestris L. New Phytol 120: 495–503

    CAS  Google Scholar 

  • Wallander H, Nilsson LO, Hagerberg D and Bååth E (2001) Estimation of the biomass and seasonal growth of external mycelium of ectomycorrhizal fungi in the field. New Phytol 151: 753–760

    Article  CAS  Google Scholar 

  • Watkins NK, Fitter AH, Graves JD and Robinson D (1996) Carbon transfer between C3 and C4 plants linked by a common mycorrhizal network, quantified using stable carbon isotopes. Soil Biol Biochem 28: 471–477

    CAS  Google Scholar 

  • Wilcox HE (1996) Mycorrhizae. In: Waisel Y, Eshel A and Kafkafi U (eds) Plant Roots. The Hidden Half. Second Edition, Revised and Expanded, pp 689–721. Marcel Dekker, Inc., New York

    Google Scholar 

  • Wong KKY, Piché Y, Montpetit D and Kropp BR (1989) Differences in the colonisation of Pinus banksiana roots by sib-monokaryotic and dikaryotic strains of ectomycorrhizal Laccaria bicolor. Can J Bot 67: 1717–1726

    Google Scholar 

  • Wong KKY, Piché Y and Fortin JA (1990) Differential development of root colonisation among four closely related genotypes of ectomycorrhizal Laccaria bicolor. Mycol Res 94: 876–884

    Google Scholar 

  • Wright DP, Read DJ and Scholes JD (1998) Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant, Cell Environ 21: 881–891

    Google Scholar 

  • Wright DP, Scholes JD, Read DJ and Rolfe SA (1999) Changes in carbon allocation and expression of carbon transporter genes in Betula pendula Roth. colonized by the ectomycorrhizal fungus Paxillus involutus (Batsch) Fr. Plant, Cell Environ 23: 39–49

    Google Scholar 

  • Wu B, Nara K and Hogetsu T (2001) Can 14C-labeled photosynthetic products move between Pinus densiflora seedlings linked by ectomycorrhizal mycelia? New Phytol 149: 137–146

    Article  CAS  Google Scholar 

  • Yanai RD, Fahey TJ and Miller SL (1995) Efficiency of nutrient acquisition by fine roots and mycorrhizae. In: Smith WK and Hinckley TM (eds) Resource Physiology of Conifers, pp. 75–103. Academic Press, New York

    Google Scholar 

  • Zhu H, Guo D and Dancik B (1990) Purification and characterization of an extracellular acid proteinase from the ectomycorrhizal fungus Hebeloma crustuliniforme. Appl Environ Microbiol 56: 837–843

    CAS  Google Scholar 

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Bryla, D.R., Eissenstat, D.M. (2005). Respiratory Costs of Mycorrhizal Associations. In: Lambers, H., Ribas-Carbo, M. (eds) Plant Respiration. Advances in Photosynthesis and Respiration, vol 18. Springer, Dordrecht. https://doi.org/10.1007/1-4020-3589-6_12

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