Arbuscular mycorrhizas are beneficial under both deficient and toxic soil zinc conditions

Background and aims

Arbuscular mycorrhizas (AM) play different roles in plant Zn nutrition depending on whether the soil is Zn-deficient (AM enhancement of plant Zn uptake) or Zn-toxic (AM protection of plant from excessive Zn uptake). In addition, soil P concentration modifies the response of AM to soil Zn conditions. We undertook a glasshouse experiment to study the interactive effects of P and Zn on AM colonisation, plant growth and nutrition, focusing on the two extremes of soil Zn concentration—deficient and toxic.

Methods

We used a mycorrhiza-defective tomato (Solanum lycopersicum) genotype (rmc) and compared it to its wild-type counterpart (76R). Plants were grown in pots amended with five soil P addition treatments, and two soil Zn addition treatments.

Results

The mycorrhizal genotype generally thrived better than the non-mycorrhizal genotype, in terms of biomass and tissue P and Zn concentrations. This was especially true under low soil Zn and P conditions, however there was evidence of the ‘protective effect’ of mycorrhizas when soil was Zn-contaminated. Above- and below-ground allocation of biomass, P and Zn were significantly affected by AM colonisation, and toxic soil Zn conditions.

Conclusions

The relationship between soil Zn and soil P was highly interactive, and heavily influenced AM colonisation, plant growth, and plant nutrition.     

Moderating mycorrhizas: arbuscular mycorrhizas modify rhizosphere chemistry and maintain plant phosphorus status within narrow boundaries

Pastures often experience a pulse of phosphorus (P) when fertilized. We examined the role of arbuscular mycorrhizal fungi (AMF) in the uptake of P from a pulse. Five legumes (Kennedia prostrata, Cullen australasicum, Bituminaria bituminosa, Medicago sativa and Trifolium subterraneum) were grown in a moderate P, sterilized field soil, either with (+AMF) or without (?AMF) addition of unsterilized field soil. After 9–10 weeks, half the pots received 15 mg P kg^?1 of soil. One week later, we measured: shoot and root dry weights; percentage of root length colonized by AMF; plant P, nitrogen and manganese (Mn) concentrations; and rhizosphere carboxylates, pH and plant‐available P. The P pulse raised root P concentration by a similar amount in uncolonized and colonized plants, but shoot P concentration increased by 143% in uncolonized plants and 53% in colonized plants. Inoculation with AMF decreased the amount of rhizosphere carboxylates by 52%, raised rhizosphere pH by ～0.2–0.7 pH units and lowered shoot Mn concentration by 38%. We conclude that AMF are not simply a means for plants to enhance P uptake when P is limiting, but also act to maintain shoot P within narrow boundaries and can affect nutrient uptake through their influence on rhizosphere chemistry.     

Phosphorus and intraspecific density alter plant responses to arbuscular mycorrhizas

We investigated how phosphorus availability, intraspecific density, and their interaction affect plant responses to arbuscular mycorrhizas. Four facultatively mycotrophic species: chile, cilantro, tomato, and corn were examined separately in pot experiments that employed a tropical phosphorus-immobilizing soil. Each experiment comprised nine soluble phosphorus additions, two levels of intraspecific plant density, and inoculation with arbuscular mycorrhizal fungi or not. High phosphorus signi- ficantly diminished mycorrhizal colonization of corn, cilantro, and tomato, but not chile, which was highly variably colonized. Corn roots were colonized by other root-inhabiting fungi, and mycorrhizas significantly reduced colonization by these potential root parasites. High phosphorus significantly increased relative growth rates (RGR) of all species, and high density significantly reduced RGR of cilantro, tomato, and corn. Chile showed little growth at any but the highest phosphorus additions, and consequently had no RGR response to density or mycorrhizas. Mycorrhiza inoculation caused transient depression of corn growth during the first month, but mycorrhizas increased corn RGR during the second month of growth. Both RGR and dry weights at harvest, cilantro, tomato, and corn benefited from mycorrhizas at low phosphorus availability, but this benefit diminished or changed to disadvantage as phosphorus availability increased. At low phosphorus availability, high density increased the dry weight of mycorrhizal cilantro and thereby amplified the benefit of mycorrhizas. At high phosphorus availability, increased density diminished the effects of mycorrhizas on dry weight, reducing mycorrhiza benefit to tomato and chile and reducing mycorrhiza detriment to cilantro. This study demonstrates that for three of the four plant species examined, phosphorus availability, intraspecific density, and their interaction significantly modify plant responses to arbuscular mycorrhizas.     

The role of arbuscular mycorrhizas in improving plant zinc nutrition under low soil zinc concentrations: a review

Many of the world’s soils are zinc (Zn) deficient. Consequently, many crops experience reduced growth, yield and tissue Zn concentrations. Reduced concentrations of Zn in the edible portions of crops have important implications for human Zn nutrition; this is a cause of global concern. Most terrestrial plant species form arbuscular mycorrhizas (AM) with a relatively limited number of specialized soil fungi. Arbuscular mycorrhizal fungi (AMF) can take up nutrients, including Zn, and transfer them to the plant, thereby enhancing plant nutrition. Under high soil Zn concentrations the formation of AM can also ‘protect’ against the accumulation of Zn in plant tissues to high concentrations. Here, a short review focusing on the role of AM in enhancing plant Zn nutrition, principally under low soil Zn concentrations, is presented. Effects of Zn on the colonisation of roots by AMF, direct uptake of Zn by AMF, the role of AM in the Zn nutrition of field grown plants, and emerging aspects of Zn molecular physiology of AM, are explored. Emergent knowledge gaps are identified and discussed in the context of potential future research.     

Arbuscular mycorrhizas in phosphate-polluted soil: interrelations between root colonization and nitrogen

To investigate whether arbuscular mycorrhizal fungi (AMF) – abundant in a phosphate-polluted but nitrogen-poor field site – improve plant N nutrition, we carried out a two-factorial experiment, including N fertilization and fungicide treatment. Percentage of root length colonized (% RLC) by AMF and tissue element concentrations were determined for four resident plant species. Furthermore, soil nutrient levels and N effects on aboveground biomass of individual species were measured. Nitrogen fertilization lowered % RLC by AMF of Artemisia vulgaris L., Picris hieracioides L. and Poa compressa L., but not of Bromus japonicus Thunb. This – together with positive N addition effects on N status, N:P-ratio and aboveground biomass of most species – suggested that plants are mycorrhizal because of N deficiency. Fungicide treatment, which reduced % RLC in all species, resulted in lower N concentrations in A. vulgaris and P. hieracioides, a higher N concentration in P. compressa, and did not consistently affect N status of B. japonicus. Evidently, AMF had an influence on the N nutrition of plants in this P-rich soil; however – potentially due to differences in their mycorrhizal responsiveness – not all species seemed to benefit from a mycorrhiza-mediated N uptake and accordingly, N distribution.     

Arbuscular mycorrhizas and their role in plant growth, nitrogen interception and soil gas efflux in an organic production system

Background and aims

Roots and mycorrhizas play an important role in not only plant nutrient acquisition, but also ecosystem nutrient cycling.

Methods

A field experiment was undertaken in which the role of arbuscular mycorrhizas (AM) in the growth and nutrient acquisition of tomato plants was investigated. A mycorrhiza defective mutant of tomato (Solanum lycopersicum L.) (named rmc) and its mycorrhizal wild type progenitor (named 76R) were used to control for the formation of AM. The role of roots and AM in soil N cycling was studied by injecting a ¹⁵N-labelled nitrate solution into surface soil at different distances from the 76R and rmc genotypes of tomato, or in plant free soil. The impacts of mycorrhizal and non-mycorrhizal root systems on soil greenhouse gas (CO₂ and ¹⁴⁺¹⁵N₂O and ¹⁵N₂O) emissions, relative to root free soils, were also studied.

Results

The formation of AM significantly enhanced plant growth and nutrient acquisition, including interception of recently applied NO ₃ ^? . Whereas roots caused a small but significant decrease in ¹⁵N₂O emissions from soils at 23?h after labeling, compared to the root-free treatment, arbuscular mycorrhizal fungi (AMF) had little effect on N₂O emissions. In contrast soil CO₂ emissions were higher in plots containing mycorrhizal root systems, where root biomass was also greater.

Conclusions

Taken together, these data indicate that roots and AMF have an important role to play in plant nutrient acquisition and ecosystem N cycling.     

Arbuscular mycorrhizas in cycads of southern India

Root and soil samples of three potted or ground-grown cycads ( Cycas circinalis, C. revoluta, Zamiasp.) were collected between November 1999 and June 2000 and surveyed for arbuscular mycorrhizal (AM) colonization and spore populations. AM fungi were associated with all root systems and rhizosphere samples examined. Root colonization was of a typical Arum type and AM colonization levels differed significantly between species and between potted and ground-grown cycads. Mycorrhizal colonization levels were inversely related to root hair number and length. Spores of nine morphotypes belonging to three genera ( Acaulospora, Glomus, Scutellospora) were extracted from soil. The percentage root length colonized by AM fungi was not related to soil factors, but total AM fungal spore numbers in the rhizosphere soil were inversely related to soil nitrogen and phosphorus levels. AM fungal spore numbers in the soil were linearly related to root length colonized. The co-occurrence of septate non-mycorrhizal fungi was recorded for the first time in cycads. These observations and the relationship between plant mycorrhizal status and soil nutrients are discussed.     

Arbuscular mycorrhizas reduce nitrogen loss via leaching

The capacity of mycorrhizal and non-mycorrhizal root systems to reduce nitrate (NO₃ ⁻) and ammonium (NH₄ ⁺) loss from soils via leaching was investigated in a microcosm-based study. A mycorrhiza defective tomato mutant and its mycorrhizal wildtype progenitor were used in this experiment in order to avoid the indirect effects of establishing non-mycorrhizal control treatments on soil nitrogen cycling and the wider soil biota. Mycorrhizal root systems dramatically reduced nitrate loss (almost 40 times less) via leaching, compared to their non-mycorrhizal counterparts, following a pulse application of ammonium nitrate to experimental microcosms. The capacity of AM to reduce nutrient loss via leaching has received relatively little attention, but as demonstrated here, can be significant. Taken together, these data highlight the need to consider the potential benefits of AM beyond improvements in plant nutrition alone.     

Arbuscular mycorrhizas and biological control of soil-borne plant pathogens – an overview of the mechanisms involved

 Biological control of plant pathogens is currently accepted as a key practice in sustainable agriculture because it is based on the management of a natural resource, i.e. certain rhizosphere organisms, common components of ecosystems, known to develop antagonistic activities against harmful organisms (bacteria, fungi, nematodes etc.). Arbuscular mycorrhizal (AM) associations have been shown to reduce damage caused by soil-borne plant pathogens. Although few AM isolates have been tested in this regard, some appear to be more effective than others. Furthermore, the degree of protection varies with the pathogen involved and can be modified by soil and other environmental conditions. This prophylactic ability of AM fungi could be exploited in cooperation with other rhizospheric microbial angatonists to improve plant growth and health. Despite past achievements on the application of AM in plant protection, further research is needed for a better understanding of both the ecophysiological parameters contributing to effectiveness and of the mechanisms involved. Although the improvement of plant nutrition, compensation for pathogen damage, and competition for photosynthates or colonization/infection sites have been claimed to play a protective role in the AM symbiosis, information is scarce, fragmentary or even controversial, particularly concerning other mechanisms. Such mechanisms include (a) anatomical or morphological AM-induced changes in the root system, (b) microbial changes in rhizosphere populations of AM plants, and (c) local elicitation of plant defence mechanisms by AM fungi. Although compounds typically involved in plant defence reactions are elicited by AM only in low amounts, they could act locally or transiently by making the root more prone to react against pathogens. Current research based on molecular, immunological and histochemical techniques is providing new insights into these mechanisms. Accepted: 29 October 1996     

Arbuscular mycorrhizal fungi from three genera induce two-phase plant growth responses on a high P-fixing soil

Plant growth enhancing effects of arbuscular mycorrhizal (AM) fungi are suitably quantified by comparisons of mycorrhizal and non-mycorrhizal plant growth responses to added phosphorus (P). The ratio between the amounts of added P required for the same yield of mycorrhizal and non-mycorrhizal plants is termed the relative effectiveness of the mycorrhiza. Variation in this relative effectiveness was examined for subterranean clover grown on a high P-fixing soil. Plants were either left non-mycorrhizal or inoculated with one of three AM fungal species with well-characterised differences in external hyphal spread. With no P added, plants from all treatments produced <10% of their maximum growth achieved at non-limiting P supply. The growth response of non-mycorrhizal plants was markedly sigmoid. Mycorrhizal growth responses were not sigmoid but their shape was two-phased. The first phase was an asymptotic approach to 25–30% of maximum growth, followed by a second asymptotic rise to maximum growth. Growth effects of Glomus invermaium and Acaulospora laevis were quite similar. Plants in these treatments produced up to four times greater shoot dry biomass than non-mycorrhizal plants. Scutellospora calospora was less effective. The relative effectiveness of AM fungi varied with the level of P application. This is expected to apply to all soils on which a sigmoid response is obtained for growth of non-mycorrhizal plants. In a simple approximation the relative effectiveness was calculated to range from 1.46 to 15.57. Shoot P contents were increased by up to 25 times by A. laevis, significantly more than by the other two fungi. The further mycelial spread of this fungus is thought to have contributed to its relatively greater effect on plant P content.     

Arbuscular mycorrhizal fungi species-specifically affect induced plant responses to a spider mite

It is widely recognized that arbuscular mycorrhizal fungi (AMF) improve plant growth and nutrient conditions, but their effects can vary from negative to positive depending on AMF species. Since the performance of herbivorous arthropods varies with plant quality, different AMF species should differently affect the density of herbivorous arthropods on plants and the herbivore-induced plant responses. We examined the indirect effects of AMF on the number of spider mites (Tetranychus urticae) and the number of damaged leaves in an outdoor glass-chamber experiment, using Lotus japonicus plants inoculated with one of four different AMF species (Gigaspora margarita, Glomus etunicatum, Gl. intraradices, and Acaulospora longula). Plants with Gi. margarita and A. longula had significantly fewer female mites than plants with Gl. etunicatum and Gl. intraradices, and plants with Gi. margarita had the fewest damaged leaves, followed by plants with A. longula, Gl. intraradices, and Gl. etunicatum. To examine species-specific effects of AMF on herbivore-induced plant responses, we carried out a bioassay with eggs laid by spider mites, and analyses of leaf chemicals (carbon, nitrogen, phosphorus, and total phenolics) using plants subjected or not subjected to herbivory. The bioassay showed that mite egg production and its changes following mite herbivory changed depending on the AMF species. In addition, Principal component analysis for leaf chemicals revealed not only mite-induced changes in leaf chemical composition, but also AMF effects on the herbivore-induced response in a species-specific way. Thus, we need to pay more attention to the species identity of AMF as an important factor in determining the strength of effects of belowground AMF on the performance and/or preferences of aboveground herbivores.     

Arbuscular mycorrhizas in southeastern Australian processing tomato farm soils

Here we report the results of a study of the formation and functioning of AM in processing tomato farm soils from across southeastern Australia. In a survey, which included the majority of processing tomato producers in the industry, mycorrhizal colonization of roots was generally low, and in many instances, completely absent. This result can be explained by the use of soil fumigants on many farms. While previous cropping history did not explain levels of AM colonization, the proportion of mycorrhizal crops in the rotation had an influence on soil C, which was generally low across most sites. In an effort to further explore the functioning of AM, a targeted glasshouse experiment was undertaken, in which a mycorrhiza defective tomato mutant and its mycorrhizal wild-type progenitor were grown under uniform conditions. While AM colonization of plants was highest when grown in soil collected from an un-farmed site in this glasshouse experiment, AM provided a greater benefit (in terms of root Zn nutrition) when grown in soil collected from more fertile farm sites. Together, these data indicate that farm management decisions (in this case soil fumigation) may have consequences for the formation of AM, which in turn, may reduce the benefits of AM in these farm soils.     

Arbuscular mycorrhizas in a valley-type savanna in southwest China

The arbuscular mycorrhizal (AM) status of 67 plant species in a savanna community in the hot, dry valley of Jinsha River, southwest China was surveyed. It was found that about 95% of the plant species formed AM and 5% possibly formed AM. The composition of AM fungi (AMF) in the rhizosphere soils was also investigated. The AMF spore density ranged from 5 to 6,400 per 100 g soil, with an average of 1,530, and these spores/sporocarps were identified as belonging to six genera. Fungi belonging to the genera Glomus and Acaulospora were the dominant AMF. High densities of AMF spores in the rhizosphere soils, and the intensive colonization of the plant roots, indicated that plants grown in this valley-type savanna may be highly dependent on AM.     

The reflectance properties of plant internodes modify elongation responses to lateral far-red radiation

The quality and quantity of light reflected from Nicotinia tabacum L. internodes was monitored as the angle of incidence was varied. Reflectance of incident light, which was either normal or longitudinal to the internode axis, was investigated. Increasing the angle of incidence caused a greater proportion of incident light to be reflected. Light striking N. tabacum internodes was always modified prior to reflection, and smaller incident angles produced greater modification of the reflected light quality. At larger angles, interactions with the internode were reduced. As a parallel investigation, the extension growth rate of light-grown Sinapis alba L. seedlings was monitored continuously using sensitive linear displacement transducers. When the angle of illumination by fibre-optic probes, presenting far-red light to the growing internode, was changed from 0° to 45°, an increase was observed in stem extension rate. There is a possibility that this rate increase was the result of a fall in the red:far-red ratio (R:FR) present inside the plant internode as the angle of incidence was altered. However, it is more likely that it was due to the larger surface area of stem being illuminated. The consequences of these observations are discussed in relation to the potential influence of such modified reflections on canopy light environments and resultant shade responses which may occur when light of known R:FR impinges on plant internodes at angles other than 0°. The possibility is discussed that plants may perceive the quality of reflected radiation from neighbouring plants to be substantially different dependent upon the angle at which it is reflected.     

Arbuscular mycorrhizal fungi and plant symbiosis in a saline-sodic soil

The seasonality of arbuscular mycorrhizal (AM) fungi–plant symbiosis in Lotus glaber Mill. and Stenotaphrum secundatum (Walt.) O.K. and the association with phosphorus (P) plant nutrition were studied in a saline-sodic soil at the four seasons during a year. Plant roots of both species were densely colonized by AM fungi (90 and 73%, respectively in L. glaber and S. secundatum) at high values of soil pH (9.2) and exchangeable sodium percentage (65%). The percentage of colonized root length differed between species and showed seasonality. The morphology of root colonization had a similar pattern in both species. The arbuscular colonization fraction increased at the beginning of the growing season and was positively associated with increased P concentration in both shoot and root tissue. The vesicular colonization fraction was high in summer when plants suffer from stress imposed by high temperatures and drought periods, and negatively associated with P in plant tissue. Spore and hyphal densities in soil were not associated with AM root colonization and did not show seasonality. Our results suggest that AM fungi can survive and colonize L. glaber and S. secundatum roots adapted to extreme saline-sodic soil condition. The symbiosis responds to seasonality and P uptake by the host altering the morphology of root colonization.     

Vesicular-arbuscular mycorrhizas and soil salinity

This review discusses the growth and activity of vesicular-arbuscular (VA) mycorrhizal fungi in saline conditions. The review includes examination of the effects of high concentrations of salts on the occurrence of VA mycorrhizal fungi in field soils, and on spore germination, growth of hyphae, establishment of the symbiosis and production of spores in controlled conditions. Information on the growth and reproduction of VA mycorrhizal fungi under saline conditions is scarce and is often circumstantial. There is clear evidence that germination of spores and subsequent hyphal growth of some VA mycorrhizal fungi are reduced by increasing concentration of salts. However, in plant growth experiments, experimental designs and methodologies have generally not allowed the direct effects of salinity on fungal growth to be separated from plant-mediated effects. There is a need for controlled studies to investigate the responses of VA mycorrhizal fungi to soil salinity. Research is required which distinguishes between effects on different phases of the fungus lifecycle and which includes in its design the ability to separate direct effects from plant-mediated influences on fungal growth and reproduction.     

Arbuscular mycorrhiza in relation to management history,soil nutrients and plant species diversity

Thelow nutrient status of semi-natural grasslands, pastures and meadows,reflects a continuity of nutrient reduction by grazing and hay-making. Ithas been hypothesized that the nutrient depletion itself may reduce competitionbetween individuals, and that mycorrhiza smooths out differences in nutrientuptake and competitive ability, so that competition for nutrients is evenfurther reduced. This interaction between site history, nutrient status andmycorrhiza could thus be one explanation for a high species diversity usuallyfound in semi-natural grasslands. To determine variation in colonizationof arbuscular mycorrhizal fungi (AM), three species(Achillea millefolium L., Ranunculusacris L. and Anthriscus sylvestris L.) weresampled at sites with different management history. All three species hadmycorrhizal colonization. Correlations between species diversity patterns atdifferent spatial scales (0.04,1 and total species number in the site) andmycorrhizal colonization were examined. In addition, soil samples were analysedconcerning P, K, N and pH. When combining measures for the three speciestogether there were significantly higher AM colonization at sites with a longcontinuous management regime, compared to sites with short or interruptedmanagement regime. A significantly positive correlation was also found betweenplant species diversity and colonization of mycorrhiza. Soil nutrient status androot weight density did not differ among the sites with different managementregime. This indicates that increasing nutrient status, or root competition, arenot likely causal mechanisms behind a reduced AM colonization rate at sites withshort or interrupted management regime. The correlation with species diversityis more likely a result of management continuity itself. A long continuousmanagement is associated with an increasing likelihood of successful dispersalof plant species as well as of fungal species.