Báo cáo khoa học: "The role of ectomycorrhizal fungi in calcareous soil tolerance by "symbiocalcicole" woody plants"

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Original article The role of ectomycorrhizal fungi in calcareous soil tolerance by "symbiocalcicole" woody plants F Lapeyrie INRA, Centre de Recherches Forestières de Nancy, Champenoux, 54280 Seichamps, France (Received 29 March 1990; accepted 5 October 1990) Summary — There are now a few examples in the literature of trees or dwarf shrub which can toler- ate calcareous soils only in association with mycorrhizal fungi; these plants could be termed symbio- calcicole. An integrative flow-diagram which summarizes probable interactions between calcareous soil, mycorrhizal fungi and roots of symbiocalcicole plants is presented and discussed. Solubilisa- tion, mobilisation and/or assimilation of phosphorus, calcium, nitrogen, iron and carbonate from cal- careous soil are considered successively. mycorrhizas / calcareous soil / calcium / calcifuge / symbiocalcicole Résumé — Les champignons ectomycorhiziens et la tolérance des sols calcaires par les plantes ligneuses "symbiocalcicoles". Quelques cas d’arbres ou d’arbustes nains tolérant les sols calcaires uniquement lorsqu’ils sont associés à des champignons ectomycorhiziens ont fait l’objet d’une publication. Ces plantes pourraient être dénommées "symbiocalcicoles". Un diagramme résumant les interactions probables existant entre sol calcaire, champignon mycorhizien et racine d’une plante symbiocalcicole est présenté et discuté. Sont envisagées successivement, la solubilisa- tion, la mobilisation et/ou l’assimilation du phosphore, du calcium, de l’azote, du fer et des carbo- nates d’un sol calcaire. mycorhizes / sol calcaire / calcicole / calcifuge / symbiocalcicole INTRODUCTION this into consideration in the selection of plant species for the different soil types to achieve maximum results. The physiologi- It has been known that cal basis for this classification is still the long plants, some tree species, can be categorized subject of active investigation since no including according to their ability to grow in calcare- complete explanation as to the mechanism soils acidic soils, ie the calcicole for the differential tolerance of the two ous or plants growing in calcareous soil, and the types of soil is currently available. Many calcifuge plants unable to tolerate calcare- hypotheses have been proposed, and ous soils. From a practical point of view, these have been the subject of a number both foresters and agronomists have taken of reviews (Burstrom, 1968; Kinzel, 1983).
Invariably, ion balances have been impli- eous soil due to their association with my- cated but in most cases the experimental corrhizal fungi. A summary of these results models have included growing plants in and experimental conditions is presented aseptic conditions or in soils where the in table I. mycorrhizal status was not determined. It is interesting to note that, although However, during the last 10 years, 4 stud- these experiments were not carried out un- ies comparing sterile and non sterile condi- der the same conditions, the general con- tions for plant growth in calcareous sub- clusions are remarkably similar. In the 4 strate have indicated that some plants can specific examples published, plant growth tolerate calcareous soils only in associa- and development was compared in the tion with mycorrhizal fungi. This suggests presence and absence of mycorrhizas ei- that the ecological and physiological status ther in calcareous soil only (Kianmehr, of the plants have been altered in the pres- 1978; Piou, 1979), or in calcareous and ence of a symbiotic partner. These four acidic substrates (Le Tacon, 1978; Lapey- published studies will be reviewed here. rie and Chilvers, 1985). In the first situation To understand the possible role of mycor- the calcareous soil toxicity was indicated in rhizal fungi in plant tolerance to calcareous leaf chlorosis and plant death, and this soil, hypotheses based on current know- was relieved by mycorrhizal infection. In ledge about calcareous soil toxicity and the second situation, the calcareous soil plant/fungus relationship will be proposed toxicity was even more obvious when com- and discussed. paring plant growth and mortality between sterile acidic and sterile calcareous sub- strates. While growth was strongly inhibit- CASE REVIEWS ed in calcareous sterile substrate, following inoculation there was no difference be- tween plant growth in both types of sub- There have been 4 reported examples to- date of plants showing tolerance to calcar- strate, acidic or calcareous.
soil, normal nitrogen metabolism, ie Different techniques were used to intro- ous amino acid and protein synthesis, was re- duce the mycorrhizal fungi, ranging from stored following plant inoculation (Clément monospecific inoculum (Kianmehr, 1978), et al, 1977). Improvement of plant phos- 10% of unsterile soil (Lapeyrie and Chil- phorus nutrition was observed with Euca- vers, 1985), 100% of unsterile soil (Piou, lyptus dumosa (Lapeyrie and Chilvers, 1979), or plantation of seedlings previously 1985). Reduction of the calcium concentra- raised in a non sterile soil (Le Tacon, tion in the leaves was noticed with Euca- 1978). In three out of four cases, ectomy- lyptus dumosa (Lapeyrie and Chilvers, corrhizas were found conferring tolerance 1985) and Pinus nigra nigricans (Le Tac- to calcareous soils (Kianmehr, 1978; Le Tacon, 1978; Piou, 1979), in one case the on, 1978). host plant was infected simultaneously with endomycorrhizal and ectomycorrhizal DISCUSSION fungi (Lapeyrie and Chilvers, 1985). In this example, the endomycorrhizas were the dominant mycorrhizal form during the first two months conferring resistance to calcar- Calcicole and symbio-calcicole plants soil, being progressively replaced by eous ectomycorrhizas after this period (Chilvers It appears that the ecological classification et al, 1987). This suggests that both endo- between calcicole and calcifuge plants mycorrhizas-VA and ectomycorrhizas have could be enriched by taking into account similar protecting effects on plants growing their mycorrhizal dependency on calcare- in calcareous soils. ous soils, some plants being able to toler- ate calcareous soils only in association While the four species cited in table I, with mycorrhizal fungi while other do so Eucalyptus dumosa, Pinus halepensis, Helianthemum chamaecistus and Pinus ni- even under sterile conditions. The new gra nigricans can tolerate calcareous soils group of plants, could be termed "symbio- calcicole plants", implying that their ability following mycorrhizal infection, others, in- to tolerate calcareous soil is strictly depen- cluding Cupressus sempervirens or Cu- dent on their symbiotic status. The defini- pressus arizonica, are indifferent to the presence of calcium carbonate even in tion of calcicole and calcifuge plants would sterile conditions (Piou, 1979). Yet, an- therefore be altered slightly: the calcicole other group of plants, including Eucalyptus plants would refer to plants which tolerate dalrympleana, E populnea, E grandis, E calcareous soils even in the absence of largiflorens, E dives, E gunii, E maidenii, E mycorrhizal fungi, the calcifuge plants would become plants which do not tolerate globulus sp bicostata (Lapeyrie, 1987) or Picea excelsa (Le Tacon, 1978) do not tol- calcareous soils even in the presence of erate calcium carbonate even after infec- mycorrhizal fungi. tion by the same mycorrhizal strain which Obviously, the existence of strictly calci- were protecting other species. cole trees could be questioned because, Since these studies did not aim to inves- while in their ecosystem, trees are always tigate the physiological aspects of resis- associated with mycorrhizal fungi and be- tance to calcareous soil, questions re- cause pot experiments in sterile substrate mains to the mechanisms involved. are always carried out for a limited period as of time; always very short compared with However, where Pinus nigra nigricans was used the tree life span. It could therefore be and grown in calcare- test plant as a
this statement has been demon- argued that survival in sterile calcareous porting strated by Dell et al (1988) who showed soils (Piou, 1979), is a temporary phenom- that, for at least the fungal NADP gluta- refer to annual However, if enon. we mate dehydrogenase, its activity can be plants, carnations produced commercially expressed or repressed in ectomycorrhi- either in soil or under hydroponic condi- zas depending on the host plant. tions are, in both cases, behaving as a cal- cicole species. The optimum nutrient solu- tion for hydroponic culture is characterized Fungus-calcareous soil interface by high pH and calcium concentration (Brun and Montarone, 1987). Endomycor- rhizal fungi are absent in such conditions, Irrespective of the direct action of the fun- without any symptoms of toxicity for the on the plant metabolism (Al Abras et gus plant, while the same medium would be al, 1988) including hormonal metabolism toxic for a calcifuge crop species. (Gay, 1987) or on the plant gene expres- Such distinction into three groups could sion (Hilbert and Martin, 1988), the role of important to consider, before undertak- be mycorrhizal fungi in calcareous soil could ing any comparative physiological work also be considered through their action at aimed at understanding why some plants the soil-plant interface. It is clearly estab- tolerate calcareous soils and others do lished that some fluxes of ions are depen- not. To explain the physiological differ- dent on the presence of the symbiotic fun- calcifuge plant and a between gus (Rygiewicz and Bledsoe, 1984). In the ences a symbiocalcicole plant, ie why the latter can specific case of calcareous soils, some be rendered tolerant to calcareous soil by pathways for the movement of ions, which the fungus while the former cannot, two could be very important for the host plant hypotheses can be considered. The first status, are presented in figure 1. where both plants do not suffer the same metabolic disorders when planted in sterile Nitrogen nutrition calcareous soil; the metabolic disorders encountered by the symbiocalcicole plant Nitrate is the prominent form of nitrogen in would be such that the associated mycor- calcareous soils. Chlorosis in trees can be rhizal fungus could counteract them, partly related to their nitrogen nutrition as whereas in the case of the calcifuge plant, found with Nordmann fir where different the fungus could not rectify these metabol- types of chlorosis can be induced either by ic disorders. The second hypothesis sup- nitrate or calcium carbonate (Khalil et al, poses that the calcifuge and symbiocalci- 1989). Perturbation of nitrogen metabolism cole plants suffer the same metabolic observed on calcareous soil in the ab- disorders when planted in sterile calcare- sence of mycorrhizas (Le Tacon, 1978) ap- ous soil; however, the plant-fungus rela- pears to be overcome through the symbio- tionship would involve different metabolic sis. pathways in both cases; the symbiotic me- It is well established that the mycorrhi- tabolism involving the symbiocalcicole fungus actively participates in plant ni- zal plant would be able to counteract the host trogen nutrition. Mycorrhizal infection im- plant stress while in the calcifuge plant it proves the nitrogen absorption, and could not. This implies that different plant simultaneously modifies the ratio of influx fungus combinations have specific meta- and efflux of ions (Rygiewicz et al, 1984a; bolic pathways involved. Evidence sup-
sions that ectomycorrhizal fungi exhibit a 1984b). These experiments have been nitrate reductase activity (France and Reid, performed at acidic and neutral pH, and 1979; Salsac et al, 1982). Free amino ac- therefore the conclusions cannot be easily ids can be incorporated by mycorrhizal fun- extrapolated to calcareous soils. However, gi (Carrodus, 1966) and mycorrhizal fungi it has been demonstrated occa- on many
possess proteases (Botton et al, 1986; concentrations of calcium extremely high Plassard et al, 1986) giving them access ions (Lapeyrie al, 1982). At ecological et to soil proteins. Then, the transfer of nitro- concentrations, the mycorrhizal fungus gen to the plant occurs either as ammoni- would mediate most of the nutrient fluxes um or as glutamine and this process is still from the soil to the plant, and could there- under investigation (France and Reid, fore prevent the plant from an over- 1983; Martin et al, 1986), but it has been accumulation. Primarily, mycorrhizal fungi shown that composition of the free amino possess an active efflux regulating the cal- acid pool in the plant is dependent on its cium accumulation (Lapeyrie and Bruchet, 1986), secondarily, calcium ions precipi- symbiotic (Krupa al, 1973; Krupa status et and Branstrom, 1974; Vésina et al, tate outside the fungal cell as calcium oxa- 1989). late. Such crystals have been observed on many occasions in situ (Malajczuk and Calcium fluxes Cromack, 1982) as well as in vitro (Lapey- rie et al, 1984a). These calcium ions pre- to another hypothesis, calcium According cipitated in the close rhizosphere are no ions may be responsible for calcareous longer free for absorption. soil toxicity (Jefferies and Willis, 1964; Using transmission electron microsco- Hall, 1977). In vivo as well as in vitro, cal- fungal intracellular vesicles, concentrat- py, cium ions are absorbed in excess by roots ing calcium associated with carbon hydro- of calcifuge plants from calcareous soil or gen and oxygen, thought to be amorphous calcium ion solutions (Anderson and La- calcium oxalate vesicles have been ob- diges, 1978; Salsac, 1973, 1980). As a served (Lapeyrie et al, 1990). They have consequence, chloroplast thylakoid struc- been described in fungal cell in pure cul- ture would be affected (Cournier et al, ture as well as in association with a host 1982), as well as C3 or C4 photosynthesis plant. They occur in the sheath and as far (Portis et al, 1977; Chevalier and Paris, as the Hartig net when calcium carbonate 1981; Gavalas and Manetas, 1980a, b; is provided in the external medium. Their Portis and Heldt, 1976). These differences role, internal storage or excretion, is still to in calcium absorption and accumulation be determined; presently no excretion fig- have been related to different composition ure have been found, suggesting that of the plasma membrane of calcicole and amorphus calcium oxalate content can be calfigue plants (Rossignol, 1977; Rossig- easily solubilized if some excretion occurs. nol et al, 1977; Lamant and Heller, 1975; Lamant et al, 1977). Calcium ions enter the cell passively, the flow only being de- Phosphorus nutrition pendent on the nature of the membrane. At present, we do not have any informa- While in calcareous soils phosphorus tion about the composition of the plasma evolves toward more and more crystalline, membrane of symbiocalcicole plants com- and less and less soluble forms (Duchau- pared to calcicole or calcifuge plants. The four, 1970), fungal oxalic acid could be an- internal cation concentration of cells is other important factor. The role of oxalic also dependent on an active calcium efflux acid in mineral weathering has been well (Hager and Hermsdorf, 1981). recognized and studied in vitro (Cornell and Schindler, 1987), as well as in vivo While mycorrhizal fungi are more or with lichens where the oxalic acid is secret- less tolerant to calcareous soils, depend- ed by the mycobiont (Jones et al, 1980; ing on their ecological origin, they tolerate
Jones and Wilson, 1985). Oxalic acid is an fuge plant. However, in most of the cases acid as well as chelating agent and after investigated, no consistent iron deficiency excretion in the soil it is particularly effi- has been found in the leaves (Marschner, cient in minerals alteration (Robert et al, 1986). Today, rather than the iron concen- 1979). In calcareous soil, by triggering the tration, its status in the plant is considered formation of complexes with metal ions with reference to metabolically "active" or (Ca, Al, Fe), oxalic acid would release "inactive" iron (Oserkowsky, 1933; Katyal phosphorus from insoluble phosphates and Sharma, 1980; Mengel et al, 1984). It (Graustein et al, 1977; Coleman et al, has been suggested that the calcifuge plants on calcareous soil synthesize in the 1983). sort of "iron inactivator" root system some Abundant oxalic acid synthesis by my- (Rhoads and Wallace, 1960; Falade, 1973; corrhizal fungi is characteristic of calcare- Brown and Jones, 1975). As we know that ous soils: the synthesis is stimulated by ni- some mycorrhizal fungi excrete sidero- trate but inhibited by ammonium ions, it is phores (Szaniszlo et al, 1981; Watteau, slightly stimulated by calcium ions and 1990), as do most soil microorganisms; highly stimulated by carbonate ions (La- these iron-complexing molecules could in- peyrie et al, 1987). Carbonate ions from teract with iron in the soil as well as in the the soil, which can be toxic for the fungus plant organs, counteracting any inactiva- as well as for the plant, are used by the tion. fungus as a carbon substrate, including for oxalate synthesis either directly from oxa- lo-acetate or via citrate, isocitrate and glyoxylate (Lapeyrie, 1988). Futhermore, CONCLUSION the release of fungal phosphatases will al- low the solubilization of organic phosphate (Bousquet et al, 1986). A characteristic difficulty in understanding After absorption by the fungus, phos- the behaviour of calcifuge and calcicole phorus is stored in vacuoles as polyphos- plants is the multiplicity of factors affecting phate granules, eventually containing cal- their response (Kinzel, 1983). It is now ob- cium, before being translocated to the host vious that all these factors interact together plant when required (Ling Lee et al, 1975; with the plant, but we do not understand Strullu et al, 1982; Lapeyrie et al, 1984b; yet all the complexities of these interac- Martin et al, 1985; Orlovich et al, 1989). tions. However, it seems that an extra fac- The plant phosphorus nutrition in calcare- tor, the mycorrhizal fungus, has been ne- ous soil is even more dependent on its my- glected in most of the physiological studies corrhizal status than in acidic soils. aimed at understanding the calcicole calci- fuge phenomenon. The presence of a fun- gus associated with the root system de- Iron assimilation fines new soil-plant interactions, the fungus-soil interface becomes the domi- Iron has been seen as the key deficiency nant one. However, as previously men- of calcareous soil toxicity. Indeed, point tioned, direct interactions between plant calcareous soil chlorosis symptoms can be and fungus should not be neglected either, relieved by iron-chelate fertilization, sug- in an attempt to understand the way in gesting that iron could not be absorbed in plants operate in calcareous soil. which calcareous soil by the roots of the calci-
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