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Vesicular-arbuscular mycorrhizas: An ubiquitous symbiosis between fungi and roots of vascular plants
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VESICULAR·ARBUSCULAR MYCORRHIZAS: AN UBIQUITOUS SYMBIOSIS BETWEEN FUNGI AND ROOTS OF VASCULAR PLANTS FIROZ AMIJEE* Wye College, University of London, Wye, Ashford, Kent TN25 5AH Vascular plants form a series of symbioses with filamentous fungi and have probably done so ever since they evolved. 'Symbiosis' is used here in the broad sense of de Bary (1887), meaning a prolonged and intimate association of two organisms living together. The word 'mycorrhiza' (fungus root) was first proposed by Frank (1885) to describe an ectomycorrhizal fungal infection in tree species of Cupuliferae where the roots were externally invested by an invading mycelium. He suggested that the association between the tree and fungus was mutualistic and the fungus obtained its carbon compounds from the host, which in tum absorbed soil mineral nutrients through the fungus. A second mycorrhizal type, the vesicular- arbuscular (VA) mycorrhizas, are classed as endomycorrhizas because the invading fungus is closely associated with the internal tissues of the host root. The fungi all belong to the Endogonales (Benjamin, 1979). The term VA refers to characteristic fungal structures, the arbuscules and vesicles (Fig. 1) found in the root cortex. Trappe (1987) has examined most of the existing data on the VA mycorrhizal status of plant species and found that they occur in almost all vascular plants growing in a variety of ecosystems. It seems reasonable to propose that in global terms there is more biomass of VA mycorrhizas than of any other symbiotic association (Nicolson, 1967) and that in almost all cases, the plants receive a direct benefit from the presence of the fungus. Infection by VA mycorrhizal fungi is not systemic and must be established de novo in young seedlings. Development and spread is a dynamic process (Tinker, 1975), with the fungus colonizing a
growing host at a regulated rate so that one partner does not outgrow the other, a requisite for mutualistic symbioses (Smith, 1981). The pattern of establishment of infection is well known from studies using axenic cultures (Mosse & Hepper, 1975). Infection may be initiated from chlamydospores, external hyphae or infected roots. Upon contact with the root epidermis, the invading hyphae form an appressorium or entry point. Hyphae then grow between cells of the epidermis and invade the cortex where they occupy the intercellular space. Cortical cell walls are penetrated by the hyphae which invaginate the plasmalemma of the host cells and A
B
Fig. 1, Vesicular-arbuscular mycorrhizal (Glomus mosseae) infection of a leek root. (A) Internal hyphae bearing arbuscules within the root cortical cells, x400; (B) Internal hyphae with vesicles in the root cortex, x150.
* Present address: School of Agriculture. Aberdeen University. Aberdeen AB9 IUD, Scotland.
branch repeatedly to form a structure known as the arbuscule (Fig. 1a). More than one arbuscule may be formed within a host cell which responds by hypertrophy of its cytoplasm. These structures are ephemeral and disintegrate after several days. The role of the arbuscule may be analogous to the haustoria formed by other biotrophic fungi, e.g. mildews, for it is thought that transfer of nutrients between the symbionts occurs at the arbuscule. Development of arbuscules is followed by formation of vesicles between the cortical cells (Fig. tb), These are terminal swellings on the hyphae which contain lipid droplets and are thought to have a storage function. This sequence of infection development is described in detail by Holley & Peterson (1979), but was recognised formerly by Gallaud (1904) who broadly classified it into two types: (a) where fungal growth is exclusively intercellular, and (b) where there is considerable intracellular growth of the hyphae. Most species of VA mycorrhizas follow this pattern of infection development, although variations in the extent to which they form hyphae or vesicles with dissimilar morphology do exist (Abbott, 1982). Cox & Sanders (1974) used the term 'infection unit' for the extent of internal colonization from a single entry point and implied that longitudinally it was determinate, reaching a maximum length of 5mm. Transversely, infection is also constant, reaching a density which occupies 5% of root volume (Amijee, Stribley & Tinker, 1986). After the fungal hyphae have successfully penetrated the cortex, they ramify over the root surface and form further appressoria and internal infection. This stimulates the growth of external mycelium (Fig. 2) which extends a considerable distance away from the root to infect adjacent roots. The symbioses of VA mycorrhizas can profoundly affect the physiology of the host. Numerous experiments in pots and in the field (see Jeffries, 1987) have demonstrated beyond doubt that VA mycorrhizas are more efficient than are
177 non-symbiotic roots in taking up phosphorus from the soil. There is a general agreement about the mechanism of this effect (Sanders & Tinker, 1971). In most soils, phosphorus is strongly adsorbed onto the solid phase and is in equilibrium with phosphorus in solution at very low concentration. Because of this, the rate limiting step in the movement of phosphorus to the root is the rate of diffusion (Nye & Tinker, 1977). Thus a zone of phosphorus-depleted soil is quickly formed around an absorbing root. The external hyphae (Fig. 2) of VA mycorrhizas extend into the soil to absorb phosphorus from beyond this depletion zone, before it is transported into the host root in the form of polyphosphate-granules (Callow et ul, 1978). The external mycelium of VA mycorrhizas therefore increases the effective diameter of the root in a way analogous to root hairs (Baylis, 1972). It is interesting to note that as long ago as 1877, Pfeffer suggested that mycorrhizal hyphae substituted for root hairs in their function. The fungus in a VA mycorrhiza obtains its carbon from the photosynthate of the host (Ho & Trappe, 1973). Recent studies have indicated presence of putative trehalose in VA mycorrhizal fungi (Amijee & Stribley, 1987), suggesting that the endophyte may sequester its carbon in a similar way to the fungus of ectotrophic mycorrhizas (Lewis & Harley, 1965). Increased flow of carbon to VA mycorrhizas results not only from the requirement of the fungus for carbon for growth and respiration, but also from the hypertrophy of cytoplasm that occurs in infected cells (Cox & Tinker, 1976). The loss of total fixed carbon by below-ground respiration can be 10% greater in mycorrhizal plants than in uninfected plants of similar rate of growth (Snellgrove et nl, 1982). This carbon drain may account for the depressions in yield resulting from mycorrhizal infection of plants that are adequately supplied with phosphate [Mosse, 1973). The effects of phosphorus and carbon physiology are the two major influences of VA mycorrhizas on
178
Fig. 2, A leek root with external VA mycorrhizal hyphae [Glomus mosseae).
can be explained in terms of them. Occasionally other effects of VA mycorrhizas have been observed; their involvement in uptake of nutrients other than phosphate, e. g. nitrogen, potassium, calcium, sulphur and zinc. Some have reported tolerance of VA mycorrhizal plants to moisture stress, whereas others have shown a greater resistance of VA mycorrhizal roots to disease. Harley & Smith (1983) fully describe details on these additional effects. The study of colonization of roots by the fungal partner of VA mycorrhizae is fundamental in understanding the effects on the physiology of the host plant (Tinker, 1978). There is strong evidence that the rate of colonization of a developing root system is a major determinant of the efficiency of the fungus in increasing phosphorus uptake from the soil by the host (Sanders et ul, 1977). This can be influenced by many factors of the physical and chemical environment of the plant and the soil (Mosse, Stribley
& Le Tacon, 1981). Of the chemical factors in the soil, it is the concentration of phosphate that has the most marked and consistent effect upon development of infection (Harley & Smith, 1983). Repeatedly it has been shown that at low concentration of soluble. phosphate in the soil VA mycorrhizal infection is highest, but when this concentration is increased, VA mycorrhizal infection is significantly reduced (e.g. Stribley, Tinker & Snellgrove, 1980). An elegant study by Sanders (1975) in which hollow leaves of Allium cepa were foliar fed with phosphorus clearly showed that effect of phosphorus upon VA mycorrhizal colonization was mediated via the host. A recent study undertaken at Rothamsted (Amijee, Tinker & Stribley, 1989) showed that when bicarbonate-soluble phosphate in the soil exceeded 140 ppm, root colonization of Allium porrum by the VA mycorrhizal fungus Glomus mosseae (Nicolson & Gerdem.) Gerdem. & Trappe, was markedly reduced in three ways: (a) the time taken to form en-
179
form internal infection was increased; (b) the rate of lateral spread of the fungus within the cortex was decreased; and (c) the density of internal infection was reduced. Following the theory proposed by Bjorkman (1942), that high concentration of carbohydrate in the root favours ectomycorrhizal infection, it has been suggested that the mechanism underlying inhibition of VA mycorrhizal fungi by high amounts of phosphate is related to a reduced rate of root exudation (Graham, Leonard & Menge, 1981) and a decreased soluble carbohydrate supply to the root (Thomson, Robson & Abbott, 1986). This hypothesis was tested (Amijee, Stribley & Tinker, 1989) and it was found that there was no concomitant decrease in soluble carbohydrate in the root when VA mycorrhizal infection was inhibited. On the contrary, increased supply of phosphorus resulting from either added phosphorus or VA mycorrhizal infection increased the concentration of soluble carbohydrate in the host roots. When the carbon demand of the fungus was calculated (Amijee, 1986), it indicated that the concentration of soluble carbohydrate in the root greatly exceeds that required by the fungus of VA mycorrhizas and thus would rarely be a limiting factor for colonization. The mechanism by which high amounts of phosphate inhibits VA mycorrhizal colonization remains unknown. The observation of an increased number of abortive entry points on roots grown at high phosphate concentration (Amijee, Tinker & Stribley, 1989) would suggest anatomical changes of the root associated with addition of phosphate as the likely cause for low levels of infection. It seems fruitless to erect hypotheses to account for the effects of host physiology upon VA mycorrhizal colonization until in depth studies at the cellular level have been accomplished. Studies over the past two decades on VA mycorrhizas have shown that the formation of this important symbioses has profound implications upon the host plant. The wide range of effects observed from these studies make it difficult
to identify a particular field of research for VA mycorrhizas. Its study should not only be of interest to mycologists or microbiologists, but also to students of plant physiology and soil-plant nutrition. To conclude, the term 'rnycorrhizas' as used today covers a wide assemblage of symbioses between fungi and roots of vascular plants, which have the common attributes that the fungus is biotrophic and mutualistic. The vesicular-arbuscular mycorrhizas abide to this rule, however, in some types of mycorrhizas (e.g. Bryophytes and Pteridophytes) physiological relationships between the partners have not been fully studied, and therefore the term mutualism should be applied with care. I am most grateful to Dr D P Stribley and Dr P B Tinker for their constructive comments. REFERENCES
ABBOTT, L K (1982). Comparative anatomy of vesicular-arbuscular mycorrhizas formed on subterranean clover. Australian Journal of Botany 30, 485-499. AMIJEE, F (1986). Colonization of Root Systems by Vesicular-Arbuscular Mycorrhizal Fungi. Ph.D. Thesis, University of Leeds. AMIJEE, F & STRIBLEY, D P (1987). Soluble carbohydrates of vesicular-arbuscular mycorrhizal fungi. The Mycologist 1, 20-21. AMIJEE, F, STRIBLEY, D P & TINKER, P B (1986). The development of endomycorrhizal root systems. VI. The relationship between development of infection, and intensity of infection in young leek roots. New Phytologist 102, 293·301. AMlTEE, F, TINKER, P B & STRIBLEY, D P (1989). The development of endomycorrhizal root systems. VII. A detailed study of effects of soil phosphorus on development and spread of vesicular-arbuscular mycorrhizal infection. New Phytologist 111, 435-446. AMIJEE, F, STRIBLEY, D P & TINKER, P B (1989). The development of endomycorrhizal root systems. VIII. A detailed study of effects of soil phosphorus on soluble carbohydrate concentration in roots and vesiculararbuscular mycorrhizal infection. New Phytologist (submitted). BARY, A DE (1887). Comparative Morphology and Biology of the Fungi, Mycetozoa and Bacteria. English translation of 1884 edition. Clarendon Press, Oxford.
180 BAYUs, G T S (1972). Fungi, phosphorus and the evolution of plant roots. Search 3, 257-258. BENJAMIN, R K (1979). Zygomycetes and their spores. in W B Kendrick (ed.), The Whole Fungus 2, 573-621, Ottawa, National Museums of Canada. BJORKMAN, E (1942). Ober die Bedingungen der mykorrhizabildung bei Kiefer und Fichte. Symbolae Botanicae Upsalienses, 6, 1-90. CALLOW, J A, CAPACCIO, L C M, PARISH, G & TINKER, P B (1978). Detection and estimation of polyphosphate in vesiculararbuscular mycorrhizas. New Phytologist 80, 125-134. Cox, G & SANDERS, FE (1974). Ultrastructure of the host-fungus interface in a vesiculararbuscular mycorrhiza. New Phytologist 73, 901-912 . Cox , G & TINKER, P B (1976) . Translocation and transfer of nutrients in vesiculararbuscular mycorrhizas. I. The arbuscule and phosphorus transfer: a quantitative ultrastructural study. New Phytologist 77, 371-378. FRANK, A B (1885). Ober die auf wurzelymbiose beruhende Erniihrung gewisser Bliume durch unterirdische Pilze. Berichte der Deutschen Botanischen Gesellschaft 3 , 128-145. GALLAUD, M Is (1904) . Etudes sur les Mycorh izes Endotrophes. Theses Faculte des Sciences de Paris. GRAHAM, J H , LEoNARD, R T & MENGE, J A (1981) . Membrane-mediated decrease in root exudation responsible for phosphorus inh ibiti on of vesicular-arbuscular mycorrhiza formation. Plant Physiology 68, 548-552. lfARLEy, J L & SMfITI, S E (1983). Mycorrhizal Symbiosis . Academic Press, London. Ho , I & TRApPE, J M (1973). Translocation of HC from Festuca plants to their endomycorrhizal fungi. Nature 244, 30-31. HoLLEY, JD & P!rrERsoN, R L (1979). Development of a vesicular-arbuscular mycorrhiza in bean roots. Canadian Journal of Botany 57, 1960-1978. JEFFRIES, P (1987). Use of mycorrhizae in agriculture. In: CRC Critical Reviews in Biotechnology 5, 319-357. LEwIs, D H & HARLEY, J L (1965). Carbohydrate physiology of mycorrhizal roots of beech. m. Movement of sugars between host and fungus. New Phytologist 64, 256-269. MaSSE, B (1973) . Plant growth responses to vesicular-arbuscular mycorrhiza. IV. In soil given additional phosphate . New Phytologist 72, 127-136. MaSSE, B & HEPPER, C (1975) . Vesiculararbuscular mycorrhizal infection in root organ cultures . Physiological Plant Pathology 5, 215-223.
MOSSE, B, STRIBLEY, D P & 1E TACON, F (1981). Ecology ofmycorrhizae and mycorrhizal fung i. Advances in Microbial Ecology 5 , 137-210. NICOLSON, T H (1967) . Vesicular-arbuscular mycorrhiza - a universal plant symbiosis. Science Progress 55, 561-581. NYE, PH & TiNKER, P B (1977). Solute Movement in the Soil-Root System. Blackwell Scientific Publications, Oxford. PFEFFER, W (1877). Ober fleischfressende Pflanzen und uber die Erniihrung durch aufnahme organischer Stoffe liberhaupt. Landwirtschaftliche Jahrbilcher 6 , 969-998. SANDERS, F E (1975). The effect of foliarapplied phosphate on the mycorrhizal infections of onion roots. In : Endomycorrhizas (Ed. by FE Sanders , B Mosse & P B Tinker) , pp261-276. Academic Press, London. SANDERS, FE & TiNKER, P B (1971) . Mechanism of absorption of phosphate from soil by Endogone mycorrhizas . Nature 233, 278-279. SANDERS, F E, TINKER, P B, BLACK, R L B & PALMERLEY, S M (1977). The development of endomycorrhizal root systems. I. Spread of infection and growth-promoting effects with four species of vesicular-arbuscular endophyte. New Phytologist 78, 257-268. SMfITI, DC (1981) . Presidential address: The symbiotic way of life . Transactions of the British Mycological Society 77, 1-8. SNELLGROVE, R C, SPLITSTOESSER , W E, STRIBLEY, D P & TINKER, P B (1982) . The carbon distribution and the demand of the fungal symbiont in leek plants with vesicular-arbuscular mycorrhizas. New Phytologist 92 , 75-81. STRIBLEY, D P, TiNKER , P B & SNELLGROVE, R C (1980). Effects of vesicular-arbuscular mycorrhizal fungi on the relations of plant growth, internal phosphorus concentration and soil phosphate analyses. Journal of Soil Science 31, 655-672 . THOMSON, B D, ROBSON, A D & ABBOTT, L K (1986). Effects of phosphorus on the formation of mycorrhizas by Gigaspora calospora and Glomus farsiculatum in relation to root carbohydrates. New Phytologist 103, 751-765. TINKER, P B (1975). Effects of vesiculararbuscular mycorrhizas on higher plants. Symposia of the Society for Experimental Biology 29, 325-349. TINKER, P B (1978) . Effects of vesiculararbuscular mycorrhizas on plant nutrition and plant growth. Physiologie Vegetale 16, 743-751. TRApPE, J M (1987) . Phytogenic and ecologic aspects of mycotrophy in the angiosperms from an evolutionary standpoint. In: Ecophysiology of VA Mycorrhizal Plants.. Ed. by G R Safir, CRC Press Inc, Florida, USA .
VESICULAR·ARBUSCULAR MYCORRHIZAS: AN UBIQUITOUS SYMBIOSIS BETWEEN FUNGI AND ROOTS OF VASCULAR PLANTS FIROZ AMIJEE* Wye College, University of London, Wye, Ashford, Kent TN25 5AH Vascular plants form a series of symbioses with filamentous fungi and have probably done so ever since they evolved. 'Symbiosis' is used here in the broad sense of de Bary (1887), meaning a prolonged and intimate association of two organisms living together. The word 'mycorrhiza' (fungus root) was first proposed by Frank (1885) to describe an ectomycorrhizal fungal infection in tree species of Cupuliferae where the roots were externally invested by an invading mycelium. He suggested that the association between the tree and fungus was mutualistic and the fungus obtained its carbon compounds from the host, which in tum absorbed soil mineral nutrients through the fungus. A second mycorrhizal type, the vesicular- arbuscular (VA) mycorrhizas, are classed as endomycorrhizas because the invading fungus is closely associated with the internal tissues of the host root. The fungi all belong to the Endogonales (Benjamin, 1979). The term VA refers to characteristic fungal structures, the arbuscules and vesicles (Fig. 1) found in the root cortex. Trappe (1987) has examined most of the existing data on the VA mycorrhizal status of plant species and found that they occur in almost all vascular plants growing in a variety of ecosystems. It seems reasonable to propose that in global terms there is more biomass of VA mycorrhizas than of any other symbiotic association (Nicolson, 1967) and that in almost all cases, the plants receive a direct benefit from the presence of the fungus. Infection by VA mycorrhizal fungi is not systemic and must be established de novo in young seedlings. Development and spread is a dynamic process (Tinker, 1975), with the fungus colonizing a
growing host at a regulated rate so that one partner does not outgrow the other, a requisite for mutualistic symbioses (Smith, 1981). The pattern of establishment of infection is well known from studies using axenic cultures (Mosse & Hepper, 1975). Infection may be initiated from chlamydospores, external hyphae or infected roots. Upon contact with the root epidermis, the invading hyphae form an appressorium or entry point. Hyphae then grow between cells of the epidermis and invade the cortex where they occupy the intercellular space. Cortical cell walls are penetrated by the hyphae which invaginate the plasmalemma of the host cells and A
B
Fig. 1, Vesicular-arbuscular mycorrhizal (Glomus mosseae) infection of a leek root. (A) Internal hyphae bearing arbuscules within the root cortical cells, x400; (B) Internal hyphae with vesicles in the root cortex, x150.
* Present address: School of Agriculture. Aberdeen University. Aberdeen AB9 IUD, Scotland.
branch repeatedly to form a structure known as the arbuscule (Fig. 1a). More than one arbuscule may be formed within a host cell which responds by hypertrophy of its cytoplasm. These structures are ephemeral and disintegrate after several days. The role of the arbuscule may be analogous to the haustoria formed by other biotrophic fungi, e.g. mildews, for it is thought that transfer of nutrients between the symbionts occurs at the arbuscule. Development of arbuscules is followed by formation of vesicles between the cortical cells (Fig. tb), These are terminal swellings on the hyphae which contain lipid droplets and are thought to have a storage function. This sequence of infection development is described in detail by Holley & Peterson (1979), but was recognised formerly by Gallaud (1904) who broadly classified it into two types: (a) where fungal growth is exclusively intercellular, and (b) where there is considerable intracellular growth of the hyphae. Most species of VA mycorrhizas follow this pattern of infection development, although variations in the extent to which they form hyphae or vesicles with dissimilar morphology do exist (Abbott, 1982). Cox & Sanders (1974) used the term 'infection unit' for the extent of internal colonization from a single entry point and implied that longitudinally it was determinate, reaching a maximum length of 5mm. Transversely, infection is also constant, reaching a density which occupies 5% of root volume (Amijee, Stribley & Tinker, 1986). After the fungal hyphae have successfully penetrated the cortex, they ramify over the root surface and form further appressoria and internal infection. This stimulates the growth of external mycelium (Fig. 2) which extends a considerable distance away from the root to infect adjacent roots. The symbioses of VA mycorrhizas can profoundly affect the physiology of the host. Numerous experiments in pots and in the field (see Jeffries, 1987) have demonstrated beyond doubt that VA mycorrhizas are more efficient than are
177 non-symbiotic roots in taking up phosphorus from the soil. There is a general agreement about the mechanism of this effect (Sanders & Tinker, 1971). In most soils, phosphorus is strongly adsorbed onto the solid phase and is in equilibrium with phosphorus in solution at very low concentration. Because of this, the rate limiting step in the movement of phosphorus to the root is the rate of diffusion (Nye & Tinker, 1977). Thus a zone of phosphorus-depleted soil is quickly formed around an absorbing root. The external hyphae (Fig. 2) of VA mycorrhizas extend into the soil to absorb phosphorus from beyond this depletion zone, before it is transported into the host root in the form of polyphosphate-granules (Callow et ul, 1978). The external mycelium of VA mycorrhizas therefore increases the effective diameter of the root in a way analogous to root hairs (Baylis, 1972). It is interesting to note that as long ago as 1877, Pfeffer suggested that mycorrhizal hyphae substituted for root hairs in their function. The fungus in a VA mycorrhiza obtains its carbon from the photosynthate of the host (Ho & Trappe, 1973). Recent studies have indicated presence of putative trehalose in VA mycorrhizal fungi (Amijee & Stribley, 1987), suggesting that the endophyte may sequester its carbon in a similar way to the fungus of ectotrophic mycorrhizas (Lewis & Harley, 1965). Increased flow of carbon to VA mycorrhizas results not only from the requirement of the fungus for carbon for growth and respiration, but also from the hypertrophy of cytoplasm that occurs in infected cells (Cox & Tinker, 1976). The loss of total fixed carbon by below-ground respiration can be 10% greater in mycorrhizal plants than in uninfected plants of similar rate of growth (Snellgrove et nl, 1982). This carbon drain may account for the depressions in yield resulting from mycorrhizal infection of plants that are adequately supplied with phosphate [Mosse, 1973). The effects of phosphorus and carbon physiology are the two major influences of VA mycorrhizas on
178
Fig. 2, A leek root with external VA mycorrhizal hyphae [Glomus mosseae).
can be explained in terms of them. Occasionally other effects of VA mycorrhizas have been observed; their involvement in uptake of nutrients other than phosphate, e. g. nitrogen, potassium, calcium, sulphur and zinc. Some have reported tolerance of VA mycorrhizal plants to moisture stress, whereas others have shown a greater resistance of VA mycorrhizal roots to disease. Harley & Smith (1983) fully describe details on these additional effects. The study of colonization of roots by the fungal partner of VA mycorrhizae is fundamental in understanding the effects on the physiology of the host plant (Tinker, 1978). There is strong evidence that the rate of colonization of a developing root system is a major determinant of the efficiency of the fungus in increasing phosphorus uptake from the soil by the host (Sanders et ul, 1977). This can be influenced by many factors of the physical and chemical environment of the plant and the soil (Mosse, Stribley
& Le Tacon, 1981). Of the chemical factors in the soil, it is the concentration of phosphate that has the most marked and consistent effect upon development of infection (Harley & Smith, 1983). Repeatedly it has been shown that at low concentration of soluble. phosphate in the soil VA mycorrhizal infection is highest, but when this concentration is increased, VA mycorrhizal infection is significantly reduced (e.g. Stribley, Tinker & Snellgrove, 1980). An elegant study by Sanders (1975) in which hollow leaves of Allium cepa were foliar fed with phosphorus clearly showed that effect of phosphorus upon VA mycorrhizal colonization was mediated via the host. A recent study undertaken at Rothamsted (Amijee, Tinker & Stribley, 1989) showed that when bicarbonate-soluble phosphate in the soil exceeded 140 ppm, root colonization of Allium porrum by the VA mycorrhizal fungus Glomus mosseae (Nicolson & Gerdem.) Gerdem. & Trappe, was markedly reduced in three ways: (a) the time taken to form en-
179
form internal infection was increased; (b) the rate of lateral spread of the fungus within the cortex was decreased; and (c) the density of internal infection was reduced. Following the theory proposed by Bjorkman (1942), that high concentration of carbohydrate in the root favours ectomycorrhizal infection, it has been suggested that the mechanism underlying inhibition of VA mycorrhizal fungi by high amounts of phosphate is related to a reduced rate of root exudation (Graham, Leonard & Menge, 1981) and a decreased soluble carbohydrate supply to the root (Thomson, Robson & Abbott, 1986). This hypothesis was tested (Amijee, Stribley & Tinker, 1989) and it was found that there was no concomitant decrease in soluble carbohydrate in the root when VA mycorrhizal infection was inhibited. On the contrary, increased supply of phosphorus resulting from either added phosphorus or VA mycorrhizal infection increased the concentration of soluble carbohydrate in the host roots. When the carbon demand of the fungus was calculated (Amijee, 1986), it indicated that the concentration of soluble carbohydrate in the root greatly exceeds that required by the fungus of VA mycorrhizas and thus would rarely be a limiting factor for colonization. The mechanism by which high amounts of phosphate inhibits VA mycorrhizal colonization remains unknown. The observation of an increased number of abortive entry points on roots grown at high phosphate concentration (Amijee, Tinker & Stribley, 1989) would suggest anatomical changes of the root associated with addition of phosphate as the likely cause for low levels of infection. It seems fruitless to erect hypotheses to account for the effects of host physiology upon VA mycorrhizal colonization until in depth studies at the cellular level have been accomplished. Studies over the past two decades on VA mycorrhizas have shown that the formation of this important symbioses has profound implications upon the host plant. The wide range of effects observed from these studies make it difficult
to identify a particular field of research for VA mycorrhizas. Its study should not only be of interest to mycologists or microbiologists, but also to students of plant physiology and soil-plant nutrition. To conclude, the term 'rnycorrhizas' as used today covers a wide assemblage of symbioses between fungi and roots of vascular plants, which have the common attributes that the fungus is biotrophic and mutualistic. The vesicular-arbuscular mycorrhizas abide to this rule, however, in some types of mycorrhizas (e.g. Bryophytes and Pteridophytes) physiological relationships between the partners have not been fully studied, and therefore the term mutualism should be applied with care. I am most grateful to Dr D P Stribley and Dr P B Tinker for their constructive comments. REFERENCES
ABBOTT, L K (1982). Comparative anatomy of vesicular-arbuscular mycorrhizas formed on subterranean clover. Australian Journal of Botany 30, 485-499. AMIJEE, F (1986). Colonization of Root Systems by Vesicular-Arbuscular Mycorrhizal Fungi. Ph.D. Thesis, University of Leeds. AMIJEE, F & STRIBLEY, D P (1987). Soluble carbohydrates of vesicular-arbuscular mycorrhizal fungi. The Mycologist 1, 20-21. AMIJEE, F, STRIBLEY, D P & TINKER, P B (1986). The development of endomycorrhizal root systems. VI. The relationship between development of infection, and intensity of infection in young leek roots. New Phytologist 102, 293·301. AMlTEE, F, TINKER, P B & STRIBLEY, D P (1989). The development of endomycorrhizal root systems. VII. A detailed study of effects of soil phosphorus on development and spread of vesicular-arbuscular mycorrhizal infection. New Phytologist 111, 435-446. AMIJEE, F, STRIBLEY, D P & TINKER, P B (1989). The development of endomycorrhizal root systems. VIII. A detailed study of effects of soil phosphorus on soluble carbohydrate concentration in roots and vesiculararbuscular mycorrhizal infection. New Phytologist (submitted). BARY, A DE (1887). Comparative Morphology and Biology of the Fungi, Mycetozoa and Bacteria. English translation of 1884 edition. Clarendon Press, Oxford.
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