Arbuscular mycorrhizal fungi alter plant allometry and biomass-density relationships

Background and Aims

Plant biomass–density relationships during self-thinning are determined mainly by allometry. Both allometry and biomass–density relationship have been shown to vary with abiotic conditions, but the effects of biotic interactions have not been investigated. Arbuscular mycorrhizal fungi (AMF) can promote plant growth and affect plant form. Here experiments were carried out to test whether AMF affect plant allometry and the self-thinning trajectory.

Methods

Two experiments were conducted on Medicago sativa L., a leguminous species known to be highly dependent on mycorrhiza. Two mycorrhizal levels were obtained by applying benomyl (low AMF) or not (high AMF). Experiment 1 investigated the effects of AMF on plant growth in the absence of competition. Experiment 2 was a factorial design with two mycorrhizal levels and two plant densities (6000 and 17 500 seeds m⁻²). Shoot biomass, root biomass and canopy radius were measured 30, 60, 90 and 120 d after sowing. The allometric relationships among these aspects of size were estimated by standardized major axis regression on log-transformed data.

Key Results

Shoot biomass in the absence of competition was lower under low AMF treatment. In self-thinning populations, the slope of the log (mean shoot biomass) vs. log density relationship was significantly steeper for the high AMF treatment (slope = –1·480) than for the low AMF treatment (–1·133). The canopy radius–biomass allometric exponents were not significantly affected by AMF level, but the root–shoot allometric exponent was higher in the low AMF treatment. With a high level of AMF, the biomass–density exponent can be predicted from the above-ground allometric model of self-thinning, while this was not the case when AMF were reduced by fungicide.

Conclusions

AMF affected the importance of below-ground relative to above-ground interactions and changed root vs. shoot allocation. This changed allometric allocation of biomass and altered the self-thinning trajectory.     

Arbuscular mycorrhizal fungi alter phosphorus relations of broomsedge (Andropogon virginicus L.) plants

Broomsedge (Andropogon virginicus L.) is a dominant grass revegetating many abandoned coal-mined lands in West Virginia, USA. Residual soils on such sites are often characterized by low pH, low nutrients, and high aluminium. Experiments were conducted to assess the resistance of broomsedge to limited phosphorus (Pi) availability and to investigate the role that arbuscular mycorrhizal (AM) fungi play in aiding plant growth under low Pi conditions. Pregerminated mycorrhizal and non-mycorrhizal seedlings were grown in a sand-culture system with nutrient solutions containing Pi concentrations ranging from 10 to 100 microM for 8 weeks. Non-mycorrhizal plants exhibited severe inhibition of growth under Pi limitation (<60 microM). Colonization by AM fungi (combined Glomus clarum Nicolson & Schenck and Gigaspora gigantea (Nicol. & Gerd.) Gerd. & Trappe) greatly enhanced host plant growth at low Pi concentrations, but did not benefit growth when Pi was readily available (100 microM). In comparison to non-mycorrhizal plants, mycorrhizal plants had higher phosphorus use efficiency at low Pi concentrations and maintained nearly constant tissue nutrient concentrations across the gradient of Pi concentrations investigated. Manganese (Mn) and sodium (Na) accumulated in shoots of non-mycorrhizal plants under Pi limitation. Mycorrhizal plants exhibited lower instantaneous Pi uptake rates and significantly lower C(min) values compared to non-mycorrhizal plants. These patterns suggest that the symbiotic association between broomsedge roots and AM fungi effectively maintains nutrient homeostasis through changes in physiological properties, including nutrient uptake, allocation and use. The mycorrhizal association is thus a major adaptation that allows broomsedge to become established on infertile mined lands.     

A thymol derivative from Inula crithmoides

Re-investigation of the aerial parts and roots of Inula crithmoides afforded, in addition to known compounds, a new epoxythymol isovalerate. Its structure has been determined as 10-isovaleryloxy-8,9-epoxythymol-3-isovalerate     

Arbuscular mycorrhizal fungi and nitrogen uptake

Nitrogen (N) is among the most important macro-nutrients significantly affecting plant growth and yield production. Accordingly, N must be supplied adequately so that optimum amounts of yield are resulted. There are different ways of supplying N to the plant including the use of chemical and biological fertilization. The chemical properties of N make it very mobile, especially under humid conditions. Hence, N must not be overfertilized with respect to the economical and environmental points of view. N Biological fertilization includes the use of plant growth-promoting rhizobacteria (PGPR) including the N-fixing bacteria, rhizobium. There are also arbuscular mycorrhizal (AM) fungi in the soil, which are symbiotic to most terrestrial plants enhancing plant growth and yield production through increasing the uptake of water and nutrients by the host plant. Numerous experiments have indicated the important role of AM fungi in enhancing P uptake by plant. However, it is yet a matter of debate that how AM fungi may affect soil N dynamic and hence plant N uptake. Some of the most important and recent aspects regarding such effects by AM fungi are highlighted, which can be of significance to health and productivity of the ecosystem.     

Arbuscular mycorrhizal fungi benefit drought-stressed Salsola laricina

Plant Ecology - Due to its contribution to plant drought tolerance, arbuscular mycorrhizae (AM) may play an important role in the revegetation of degraded pastures in semi-arid and arid regions....     

Arbuscular mycorrhizal fungi enhance aluminium resistance of broomsedge (Andropogon virginicus L.)

In the eastern United States, broomsedge (Andropogon virginicus L.) is found growing on abandoned coal-mined lands that have extremely acidic soils with high residual aluminium (Al) concentrations. Broomsedge may be inherently metal-resistant and nutrient-efficient or may rely on the arbuscular mycorrhizal (AM) fungal association to overcome limitations on such sites. Broomsedge plants were grown with and without an acidic ecotype AM fungal consortium and exposed to controlled levels of Al in two experiments. The AM fungal consortium conferred Al resistance to broomsedge. Arbuscular mycorrhizal fungi reduced Al uptake and translocation in host plants, potentially reflecting measured reductions in inorganic Al availability in the rhizosphere of mycorrhizal plants. Mycorrhizal plants exhibited lower shoot P concentrations, higher phosphorus use efficiency, and lower root acid phosphatase rates than non-mycorrhizal plants. Aluminium significantly reduced calcium (Ca) and magnesium (Mg) tissue concentrations in both mycorrhizal and non-mycorrhizal plants. However, plant response to any change in nutrient acquisition was substantially less pronounced in mycorrhizal plants. The exclusion of Al and greater stability of tissue biomass accretion-tissue nutrient relationships in mycorrhizal broomsedge plants exposed to Al may be important mechanisms that allow broomsedge to grow on unfavourable acidic soils.     

Arbuscular mycorrhizal fungi in terms of symbiosis-parasitism continuum

Arbuscular mycorrhizal fungi are forming the most wide-spread mycorrhizal relationships on Earth. Mycorrhiza contributes to phosphorous acquisition, water absorption and resistance to diseases. The fungus promotes the absorption of nutrients and water from soil, meanwhile the host plant offers photosynthetic assimilates in exchange, like carbohydrates, as energy source. The plant benefits from the contribution of symbiotic partner only when nutrients are in low concentrations in soil and the root system would not be able to absorb sufficiently the minerals. When the help of mycorrhizal fungi is not necessarily needed, the host plant is making an economy of energy, suppressing the development of fungi in the internal radicular space. In this moment, the nature of relationship turns from symbiotic to parasitic, triggering a series of defensive reactions from the plant. Also, there were several cases reported when the presence of arbuscular mycorrhizal fungi negatively influenced the host plant. For example, in adverse environmental conditions, like very high temperatures, instead of determining a higher plant biomass and flowering, the mycorrhiza reduces the growth of the host plant. We conducted a pot experiment with hydroponic culture to examine the effect of arbuscular mycorrhiza on development of French marigold as a host plant. As experimental variants, the phosphorous content in nutrient medium and temperature varied. Plants were artificially infected with arbuscular mycorrhizal fungi using a commercial inoculum containing three fungal species, as following: Glomus intraradices, Glomus etunicatum and Glomus claroideum. Colonization intensity and arbuscular richness were checked using root staining with aniline blue and estimation with the Trouvelot method. To observe the differences between plants from the experimental variants, we examined the number of side shoots, flower buds and fully developed flowers, fresh biomass and total leaf area. Results show that adverse climatic conditions, like temperature shock at the beginning of growing period modified the nature of symbiosis. In this case, the physiological parameters were reduced at colonized plants, while usual, constant growing conditions permitted the normal, efficient and beneficial development of symbiosis.     

Arbuscular mycorrhizal fungi enhance P uptake and alter plant morphology in the invasive plant Microstegium vimineum

Invasive plant species can interact with native soil microbes in ways that change how they use nutrients and allocate biomass. To examine whether Microstegium vimineum form symbiotic associations with arbuscular mycorrhizal fungi (AMF) and whether AMF mediate nutrient acquisition and growth of the plant, we conducted a field survey in Raleigh, NC and Hangzhou, China and two experiments in growth chambers. This is the first report that M. vimineum is mycorrhizal, with colonization rates of 47 and 21 % in its native and invaded range, respectively. In the growth chamber, addition of an AMF inoculum mixture significantly promoted M. vimineum biomass accumulation in both field and sterilized soils, particularly after 64 days of growth. Arbuscular mycorrhizal fungi also increased plant phosphorous (P) uptake but did not consistently affect total plant nitrogen (N) acquisition, leading to decreases in plant N:P ratios. More interestingly, AMF significantly altered plant morphology, increasing the number of stolons and aerial roots per individual (59 and 723 %), aerial roots per gram aboveground biomass (374 %) and aerial roots per stolon (404 %). Our results suggest that mycorrhizal enhancement of plant growth by stimulating tillering may serve as another mechanism by which M. vimineum can quickly take over new territory. Future studies on invasive plant-microbial interactions are needed to understand the mechanisms through which microbes contribute to the competitive ability of invasive plants.     

Arbuscular mycorrhizal structure and fungi associated with mosses

We investigated the colonization and diversity of arbuscular mycorrhizal (AM) fungi associated with 24 moss species belonging to 16 families in China. AM fungal structures, i.e. spores, vesicles, hyphal coils (including intracellular hyphae), or intercellular nonseptate hyphae, were found in 21 moss species. AM fungal structures (vesicles, hyphal coils, and intercellular nonseptate hyphae) were present in tissues of 14 moss species, and spores and nonseptate hyphae on the surface of gametophytes occurred in 15 species. AM fungal structures were present in 11 of the 12 saxicolous moss species and in six of the ten terricolous moss species, but absent in two epixylous moss species. AM fungal structures were only observed in moss stem and leaf tissues, but not in rhizoids. A total of 15 AM fungal taxa were isolated based on trap culture with clover, using 13 moss species as inocula. Of these AM fungi, 11 belonged to Glomus, two to Acaulospora, one to Gigaspora, and one to Paraglomus. Our results suggest that AM fungal structures commonly occur in most mosses and that diverse AM fungi, particularly Glomus species, are associated with mosses.     

Arbuscular mycorrhizal fungi as (agro)ecosystem engineers

Symbiotic interactions have been shown to facilitate shifts in the structure and function of host plant communities. For example, parasitic plants can induce changes in plant diversity through the suppression of competitive community dominants. Arbuscular mycorrhizal (AM) fungi have also be shown to induce shifts in host communities by increasing host plant nutrient uptake and growth while suppressing non-mycorrhizal species. AM fungi can therefore function as ecosystem engineers facilitating shifts in host plant communities though the presumed physiological suppression of non-contributing or non-mycorrhizal plant species. This dichotomy in plant response to AM fungi has been suggested as a tool to suppress weed species (many of which are non-mycorrhizal) in agro-ecosystems where mycorrhizal crop species are cultivated. Rinaudo et al. (2010), this issue, have demonstrated that AM fungi can suppress pernicious non-mycorrhizal weed species including Chenopodium album (fat hen) while benefiting the crop plant Helianthus annuus (sunflower). These findings now suggest a future for harnessing AM fungi as agro-ecosystem engineers representing potential alternatives to costly and environmentally damaging herbicides.     

Arbuscular mycorrhizal fungi in two mangroves in South China

The symbiosis between arbuscular mycorrhizal fungi (AMF) and mangrove plant species was investigated in two mangrove swamps in south China. AMF were mostly found in the form of hyphae and were commonly associated with all the mangrove species we investigated. Six AMF species belonging to the genera Glomus or Acaulospora were identified. Multiple step-wise linear regression analyses showed that hydrological conditions and phosphorus levels in the rhizosphere were the main abiotic factors affecting the colonization of mangrove species by AMF. A greenhouse experiment was conducted to evaluate the effects of AMF inoculation on the growth and nutrient uptake of a true mangrove plant species, Sonneratia apetala B. Ham. The inoculated AMF significantly improved growth, resulting in greater plant height, diameter at ground level and plant biomass, as well as increased absorption of N, P and K. These findings suggest that AMF play important roles in mangrove ecosystems.     

Arbuscular mycorrhizal fungi induced alteration to root longevity of poplar

Root longevity is an important element determining the fluxes of nutrients and carbon within terrestrial ecosystems. The effect of colonisation by an arbuscular mycorrhizal (AM) fungus on root longevity of poplar was determined using a minirhizotron camera to make direct observation of roots in situ in conjunction with image analysis. significant influences of colonisation on the longevity of roots were observed with most colonised roots surviving for a shorter period than non-colonised roots: only 16% of colonised roots survived for longer than 49 days compared to 49% of non-colonised roots. After 21 days approximately 5 times as many colonised as non-colonised roots had died. Possible mechanisms are discussed.     

Arbuscular mycorrhizal fungi and biochar improves drought tolerance in chickpea

Arbuscular mycorrhizal fungi (AMF) inoculation and biochar amendment has been reported to improve growth of several crop plants however their role in stress amelioration individually as well as in combination has not been worked out. This experiment was conducted to evaluate the application of AMF and biochar on the performance of chickpea under drought stress. The treatments included the individual as well as combined treatment of AMF and biochar to drought stressed and normal chickpea plants. Plants inoculation improved growth in terms of shoot and root length, leaf area and number of branches which was observed to show a steep decline due to drought stress. Drought declined the AMF colonization potential though biochar amendment ameliorated the negative effects of drought significantly by improving the spore population, number of mycelium, vesicle and arbuscules and the percentage of colonization as well. Increased chlorophyll synthesis in biochar and AMF treated plants was obvious, which lead to significant enhancement in the net photosynthetic efficiency. Drought stress also declined the relative water content (RWC) and membrane stability index (MSI), while treatment of biochar and AMF either individually or in combination mitigated the deleterious effects to considerable extent and caused a significant enhancement in RWC and MSI under normal conditions. Amendments with biochar and AMF inoculation increased the nitrogen fixation attributes including the number and weight of nodules, leghemoglobin content and activity of nitrate reductase enzyme leading to greater uptake and assimilation of nitrogen in them when compared to drought stressed plants. Drought stressed chickpea plants exhibited considerable reduction in uptake of nitrogen and phosphorous which was ameliorated by biochar and AMF treatments. It could be suggested that increase in growth and physiological attributes in chickpea due to biochar amendments and AMF inoculation under drought stress were plausibly due to their involvement in nitrogen and phosphorous uptake, chlorophyll synthesis and photosynthesis.     

Arbuscular mycorrhizal fungi might alleviate aluminium toxicity in banana plants

Under defined laboratory conditions it was shown that two glucosinolate-containing plant species, Tropaeolum majus and Carica papaya , were colonized by arbuscular mycorrhizal (AM) fungi, whereas it was not possible to detect AM fungal structures in other glucosinolate-containing plants (including several Brassicaceae). Benzylglucosinolate was present in all of the T. majus cultivars and in C. papaya it was the major glucosinolate. 2-Phenylethylglucosinolate was found in most of the non-host plants tested. Its absence in the AM host plants indicates a possible role for the isothiocyanate produced from its myrosinase-catalysed hydrolysis as a general AM inhibitory factor in non-host plants. The results suggest that some of the indole glucosinolates might also be involved in preventing AM formation in some of the species. In all plants tested, both AM hosts and non-hosts, the glucosinolate pattern was altered after inoculation with one of three different AM fungi ( Glomus mosseae , Glomus intraradices and Gigaspora rosea ), indicating signals between AM fungi and plants even before root colonization. The glucosinolate induction was not specifically dependent on the AM fungus. A time-course study in T. majus showed that glucosinolate induction was present during all stages of mycorrhizal colonization.     

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.     

Arbuscular mycorrhizal fungi associated with sedges on the Tibetan plateau

The arbuscular mycorrhizal (AM) status of nine dominant sedge species and the diversity of AM fungi in Tibetan grassland were surveyed in the autumn of 2003 and 2004. Most of the sedge species and ecotypes examined were mycorrhizal, but Carex moorcroftii and Kobresia pusilla were of doubtful AM status, and Kobresia humilis was facultatively mycorrhizal. This is the first report of the mycorrhizal status of eight of the nine sedge species examined. Intraradical vesicles and aseptate hyphae were the structures most frequently observed. Appressoria, coils, and arbuscules were found in the roots of a few sedge species. A strong negative correlation was found between soil organic matter content and the extent of mycorrhizal colonization. Using trap cultures, 26 species of AM fungi belonging to six genera, Glomus, Acaulospora, Paraglomus, Archaeospora, Pacispora, and Scutellospora, were isolated from the soil samples collected. The frequency of occurrence of different taxa of AM fungi varied greatly. Glomus and Acaulospora were the dominant genera, and Acaulospora scrobiculata was the most frequent and abundant species. The species richness of AM fungi was 2.73 in the study area. Species richness and diversity index differed among the sedge species but were not correlated with soil factors such as pH, available P, or organic matter content.     

Arbuscular mycorrhizal fungi influence life history traits of a lepidopteran herbivore

Results from pot and microcosm studies in the greenhouse have shown that plant growth and foliar chemistry is altered by the presence and species composition of arbuscular mycorrhizal fungi (AMF). The growth and survival of herbivores which feed on plants could, as a consequence, also be affected by these mutualistic soil fungi. Consequently, interactions between AMF, plants and herbivores could occur. To test this, larvae of the common blue butterfly, Polyommatus icarus (Lycaenidae), were fed with sprigs of Lotus corniculatus (Fabaceae) plants which were inoculated with one of two different AMF species, with a mixture of these AMF species or with sprigs of plants which were not inoculated with AMF. Survival and larval weight of third instar larvae fed with plants colonised by AMF were greater than those of larvae fed with non-mycorrhizal plants. Survival of larvae feeding on non-mycorrhizal plants was 1.6 times lower than that of larvae feeding on plants inoculated with a mixture of AMF species and 3.8 times lower than that of larvae feeding on plants inoculated with single AMF species. Furthermore, larvae fed with non-mycorrhizal plants attained only about half the weight of larvae fed with mycorrhizal plants after 11 days of growth. These differences in larval performance might be explained by differences in leaf chemistry, since mycorrhizal plants had a 3 times higher leaf P concentration and a higher C/N-ratio. Our results, thus, show that the presence of belowground mutualistic soil fungi influences the performance of aboveground herbivores by altering their food quality. Larval consumption, larval food use and adult lipid concentrations of the common blue butterfly differed between larvae which were fed with plants inoculated with different AMF species. This suggests that the performance of herbivores is not only influenced by the presence of AMF but also depends on the identity of the AMF species colonising the host plants. Moreover, a significant interaction term between AMF species and maternal identity of the larvae occurred for adult dry weight, indicating that the performance of offspring from different females was differently influenced by AMF species composition. To our knowledge, these results show for the first time that the species composition of AMF communities can influence life-history traits of butterfly larvae and possibly herbivores in general.     

Arbuscular mycorrhizal potential and mycorrhizal fungi diversity associated with Agave potatorum Zucc. in Oaxaca, Mexico

The status of the arbuscular mycorrhizal association in wild Agave potatorum Zucc. was studied at three semiarid sites over a 1-year period of rhizospheric soil sampling. Root colonization present at all sites and at all times of year, ranged from 20 to 83 %. The extraradical mycelia length was estimated to be from 2.64 to 5.22 m g^?1 of dry soil. Spore number ranged from 20 to 192 in 100 g of soil. The number of viable mycorrhizal propagules ranged from 500 to 2,640 in 100 g of soil. Twenty species of arbuscular mycorrhizal fungi (AMF) were identified, the family Glomeracea comprising the greatest number of species (45 %). Two other fungi families Acaulosporaceae and Gigasporaceae made up 35 and 15 %, respectively. High alpha diversity and low beta diversity of AMF were found in this study. Arbuscular mycorrhizal fungi species richness in A. potatorum is high and the associated fungi appear to be an important component in semiarid ecosystems in this region of Mexico. Arbuscular mycorrhizal fungi species with small spores might be better adapted to the local environment.     

Arbuscular mycorrhizal fungi reduce effects of physiological integration in Trifolium repens

Background and Aims

One of the special properties of clonal plants is the capacity for physiological integration, which can increase plant performance through mechanisms such as resource sharing and co-ordinated phenotypic plasticity when plants grow in microsites with contrasting resource availabilities. However, many clonal plants are colonized by arbuscular mycorrhizal fungi (AMF). Since AMF are likely to reduce contrasts in effective resource levels, they could also reduce these effects of clonal integration on plasticity and performance in heterogeneous environments.

Methods

To test this hypothesis, pairs of connected and disconnected ramets of the stoloniferous herb Trifolium repens were grown. One ramet in a pair was given high light and low nutrients while the other ramet was given high nutrients and low light. The pairs were inoculated with zero, one or five species of AMF.

Key Results

Pairs of ramets grown without AMF developed division of labour and benefited from resource sharing, as indicated by effects of connection on allocation to roots, accumulation of mass, and ramet production. Inoculation with five species of AMF significantly reduced these effects of connection, both by inhibiting them in ramets given high nutrients and inducing them in ramets given high light. Inoculation with one species of AMF also reduced some effects of connection, but generally to a lesser degree.

Conclusions

The results show that AMF can significantly modify the effects of clonal integration on the plasticity and performance of clonal plants in heterogeneous environments. In particular, AMF may partly replace the effects and benefits of clonal integration in low-nutrient habitats, possibly more so where species richness of AMF is high. This provides the first test of interaction between colonization by AMF and physiological integration in a clonal plant, and a new example of how biotic and abiotic factors could interact to determine the ecological importance of clonal growth.Key words: Arbuscular mycorrhizal fungi, biomass allocation, clonal plant, division of labour, environmental heterogeneity, light availability, nutrients, white clover