Direct and indirect influences of arbuscular mycorrhizal fungi on phosphorus uptake by two root hemiparasitic Pedicularis species: do the fungal partners matter at low colonization levels?

Background and Aims

Because most parasitic plants do not form mycorrhizal associations, the nutritional roles of arbuscular mycorrhizal (AM) fungi in them have hardly been tested. Some facultative root hemiparasitic Pedicularis species form AM associations and hence are ideal for testing both direct and indirect effects of AM fungi on their nutrient acquisition. The aim of this study was to test the influence of AM inoculation on phosphorus (P) uptake by Pedicularis rex and P. tricolor.

Methods

³²P labelling was used in compartmented pots to assess the contribution of the AM pathway and the influence of AM inoculation on P uptake from a host plant into the root hemiparasites. Laboratory isolates of fungal species (Glomus mosseae and G. intraradices) and the host species (Hordeum vulgare ‘Fleet’) to which the two Pedicularis species showed obvious responses in haustorium formation and growth in previous studies were used.

Key Results

The AM colonization of both Pedicularis spp. was low (<15 % root length) and only a very small proportion of total plant P (<1 %) was delivered from the soil via the AM fungus. In a separate experiment, inoculation with AM fungi strongly interfered with P acquisition by both Pedicularis species from their host barley, almost certainly because the numbers of haustoria formed by the parasite were significantly reduced in AM plants.

Conclusions

Roles of AM fungi in nutrient acquisition by root parasitic plants were quantitatively demonstrated for the first time. Evidence was obtained for a novel mechanism of preventing root parasitic plants from overexploiting host resources through AM fungal-induced suppression of the absorptive structures in the parasites.     

Inoculation with arbuscular mycorrhizal fungi suppresses initiation of haustoria in the root hemiparasite Pedicularis tricolor

Background and Aims

Plant parasitism and arbuscular mycorrhizal (AM) associations have many parallels and share a number of regulatory pathways. Despite a rapid increase in investigations addressing the roles of AM fungi in regulating interactions between parasitic plants and their hosts, few studies have tested the effect of AM fungi on the initiation and differentiation of haustoria, the parasite-specific structures exclusively responsible for host attachment and nutrient transfer. In this study, we tested the influence of AM fungi on haustorium formation in a root hemiparasitic plant.

Methods

Using a facultative root hemiparasitic species (Pedicularis tricolor) with the potential to form AM associations, the effects of inoculation were tested with two AM fungal species, Glomus mosseae and Glomus intraradices, on haustorium initiation in P. tricolor grown alone or with Hordeum vulgare ‘Fleet’ (barley) as the host plant. This study consisted of two greenhouse pot experiments.

Key Results

Both AM fungal species dramatically suppressed intraspecific haustorium initiation in P. tricolor at a very low colonization level. The suppression over-rode inductive effects of the parasite''s host plant on haustoria production and caused significant growth depression of P. tricolor.

Conclusions

AM fungi had strong and direct suppressive effects on haustorium formation in the root hemiparasite. The significant role of AM fungi in haustorium initiation of parasitic plants was demonstrated for the first time. This study provides new clues for the regulation of haustorium formation and a route to development of new biocontrol strategies in management of parasitic weeds.     

Medicago truncatula Mtha1-2 mutants loose metabolic responses to mycorrhizal colonization

Bidirectional nutrient transfer is one of the key features of the arbuscular mycorrhizal symbiosis. Recently we were able to identify a Medicago truncatula mutant (mtha1-2) that is defective in the uptake of phosphate from the periarbuscular space due to a lack of the energy providing proton gradient provided by the symbiosis specific proton ATPase MtHA1¹ In order to further characterize the impact of fungal colonization on the plant metabolic status, without the beneficial aspect of improved mineral nutrition, we performed leaf ion analyses in mutant and wildtype plants with and without fungal colonization. Although frequency of fungal colonization was unaltered, the mutant did not show a positive growth response to mycorrhizal colonization. This indicates that nutrient transfer into the plant cell fails in the truncated arbuscules due to lacking expression of a functional MtHA1 protein. The leaves of wildtype plants showed clear metabolic responses to root mycorrhizal colonization, whereas no changes of leaf metabolite levels of mycorrhizal mtha1-2 plants were detected, even though they were colonized. These results show that MtHa1 is indispensable for a functional mycorrhizal symbiosis and, moreover, suggest that fungal root colonization per se does not depend on nutrient transfer to the plant host.     

AM Fungal Diversity in Selected Medicinal Plants of Kanyakumari District,Tamil Nadu,India

The association of Arbuscular Mycorrhizal Fungi (AMF) with three medicinally important plants viz., Eclipta prostrata, Indigofera aspalathoides, I. tinctoria collected from three different localities of Kanyakumari District, South India was examined. The study reports the colonization percentage, diversity and species richness of different AM fungi in the rhizosphere of the three medicinal plants and discusses the impact of soil physicochemical characteristics such as soil texture, pH and available macro- and micro nutrient content on AM fungal communities. A total 21 AM fungal species were identified in field conditions of the three plants from three sites. AM fungal species richness, colorization percentage and Shannon index were found to be high in the two Indigofera sp. growing in the hilly areas of Kanyakumari District and were low in E. prostrata collected from the damp regions in the foothills of the three study sites. Five species registered 100% frequency in all the study sites of the three medicinally important plants with Glomus as the dominant genera. The study states that the mean colonization and diversity patterns were dependant on edaphic factors and type of vegetation.     

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.     

Gibberellin regulates infection and colonization of host roots by arbuscular mycorrhizal fungi

Arbuscular mycorrhiza (AM) is established by the entry of AM fungi into the host plant roots and the formation of symbiotic structures called arbuscules. The host plant supplies photosynthetic products to the AM fungi, which in return provide phosphate and other minerals to the host through the arbuscules. Both partners gain great advantages from this symbiotic interaction, and both regulate AM development. Our recent work revealed that gibberellic acids (GAs) are required for AM development in the legume Lotus japonicus. GA signaling interact with symbiosis signaling pathways, directing AM fungal colonization in host roots. Expression analysis showed that genes for GA biosynthesis and metabolism were induced in host roots around AM fungal hyphae, suggesting that the GA signaling changes with both location and time during AM development. The fluctuating GA concentrations sometimes positively and sometimes negatively affect the expression of AM-induced genes that regulate AM fungal infection and colonization.     

Growth,root colonization and nutrient status of Helianthemum sessiliflorum Desf. inoculated with a desert truffle Terfezia boudieri Chatin

This study aims to investigate the effects of inoculation using Terfezia boudieri Chatin ascospores (ectomycorrhizal fungus) on growth, root colonization and nutrient status of Helianthemum sessiliflorum Desf. seedlings grown in pots on two-soil types (gypseous and sandy loam). Mycorrhizal seedlings had significantly increased their height and leaf number compared to non-mycorrhizal ones. Regardless of mycorrhizal inoculation treatments, the plants growing on gypseous soil showed higher growth as compared to sandy loam one. It appears that inoculation with T. boudieri changed root morphology, increasing branching of first-order lateral roots of H. sessiliflorum seedlings. The highest root mycorrhizal colonization was recorded in inoculated seedlings on sandy loam soil (89%) when compared to gypseous one (52%). N, P and K concentrations in mycorrhizal seedlings were significantly improved by fungal inoculation. It can be concluded that inoculation of H. sessiliflorum with T. boudieri increased growth attributes and improved plant nutritional status.     

Interaction of Vesicular-arbuscular Mycorrhizal Fungi and Phosphorus with Meloidogyne incognita on Tomato

The influence of two vesicular-arbuscular mycorrhizal fungi and phosphorus (P) nutrition on penetration, development, and reproduction by Meloidogyne incognita on Walter tomato was studied in the greenhouse. Inoculation with either Gigaspora margarita or Glomus mosseae 2 wk prior to nematode inoculation did not alter infection by M. incognita compared with nonmycorrhizal plants, regardless of soil P level (either 3 μg [low P] or 30 μg [high P] available P/g soil). At a given soil P level, nematode penetration and reproduction did not differ in mycorrhizal and nonmycorrhizal plants. However, plants grown in high P soil had greater root weights, increased nematode penetration and egg production per plant, and decreased colonization by mycorrhizal fungi, compared with plants grown in low P soil. The number of eggs per female nematode on mycorrhizal and nonmycorrhizal plants was not influenced by P treatment. Tomato plants with split root systems grown in double-compartment containers which had either low P soil in both sides or high P in one side and low P in the other, were inoculated at transplanting with G. margarita and 2 wk later one-half of the split root system of each plant was inoculated with M. incognita larvae. Although the mycoorhizal fungus increased the inorganic P content of the root to a level comparable to that in plants grown in high P soil, nematode penetration and reproduction were not altered. In a third series of experiments, the rate of nematode development was not influenced by either the presence of G. margarita or high soil P, compared with control plants grown in low P soil. These data indicate that supplemental P (30 μ/g soil) alters root-knot nematode infection of tomato more than G. mosseae and G. margarita.     

MIZ1-regulated hydrotropism functions in the growth and survival of Arabidopsis thaliana under natural conditions

Background and Aims

Root hydrotropism is a response to water-potential gradients that makes roots bend towards areas of higher water potential. The gene MIZU-KUSSEI1 (MIZ1) that is essential for hydrotropism in Arabidopsis roots has previously been identified. However, the role of root hydrotropism in plant growth and survival under natural conditions has not yet been proven. This study assessed how hydrotropic response contributes to drought avoidance in nature.

Methods

An experimental system was established for the study of Arabidopsis hydrotropism in soil. Characteristics of hydrotropism were analysed by comparing the responses of the miz1 mutant, transgenic plants overexpressing MIZ1 (MIZ1OE) and wild-type plants.

Key Results

Wild-type plants developed root systems in regions with higher water potential, whereas the roots of miz1 mutant plants did not show a similar response. This pattern of root distribution induced by hydrotropism was more pronounced in MIZ1OE plants than in wild-type plants. In addition, shoot biomass and the number of plants that survived under drought conditions were much greater in MIZ1OE plants.

Conclusions

These results show that hydrotropism plays an important role in root system development in soil and contributes to drought avoidance, which results in a greater yield and plant survival under water-limited conditions. The results also show that MIZ1 overexpression can be used for improving plant productivity in arid areas.     

Interactions among plants,bacteria, and fungi reduce extracellular enzyme activities under long‐term N fertilization

Atmospheric nitrogen (N) deposition has enhanced soil carbon (C) stocks in temperate forests. Most research has posited that these soil C gains are driven primarily by shifts in fungal community composition with elevated N leading to declines in lignin degrading Basidiomycetes. Recent research, however, suggests that plants and soil microbes are dynamically intertwined, whereby plants send C subsidies to rhizosphere microbes to enhance enzyme production and the mobilization of N. Thus, under elevated N, trees may reduce belowground C allocation leading to cascading impacts on the ability of microbes to degrade soil organic matter through a shift in microbial species and/or a change in plant–microbe interactions. The objective of this study was to determine the extent to which couplings among plant, fungal, and bacterial responses to N fertilization alter the activity of enzymes that are the primary agents of soil decomposition. We measured fungal and bacterial community composition, root–microbial interactions, and extracellular enzyme activity in the rhizosphere, bulk, and organic horizon of soils sampled from a long‐term (>25 years), whole‐watershed, N fertilization experiment at the Fernow Experimental Forest in West Virginia, USA. We observed significant declines in plant C investment to fine root biomass (24.7%), root morphology, and arbuscular mycorrhizal (AM) colonization (55.9%). Moreover, we found that declines in extracellular enzyme activity were significantly correlated with a shift in bacterial community composition, but not fungal community composition. This bacterial community shift was also correlated with reduced AM fungal colonization indicating that declines in plant investment belowground drive the response of bacterial community structure and function to N fertilization. Collectively, we find that enzyme activity responses to N fertilization are not solely driven by fungi, but instead reflect a whole ecosystem response, whereby declines in the strength of belowground C investment to gain N cascade through the soil environment.     

Reduced mycorrhizal colonization (rmc) tomato mutant lacks expression of SymRK signaling pathway genes

Comparison of the expression of 13 genes involved in arbuscular mycorrhizal (AM) symbiosis was performed in a wild type tomato (Solanum lycopersicum cv 76R) and its reduced mycorrhizal colonization mutant rmc in response to colonization with Glomus fasiculatum. Four defense-related genes were induced to a similar extent in the mutant and wild type AM colonized plants, indicating a systemic response to AM colonization. Genes related to nutrient exchange between the symbiont partners showed higher expression in the AM roots of wild type plants than the mutant plants, which correlated with their arbuscular frequency. A symbiosis receptor kinase that is involved in both nodulation and AM symbiosis was not expressed in the rmc mutant. The fact that some colonization was observed in rmc was suggestive of the existence of an alternate colonization signaling pathway for AM symbiosis in this mutant.     

High effectiveness of exotic arbuscular mycorrhizal fungi is reflected in improved rhizobial symbiosis and trehalose turnover in Cajanus cajan genotypes grown under salinity stress

Arbuscular mycorrhizal fungi (AMF) improve functioning of legume-Rhizobium symbiosis under salinity. However, plant responses to mycorrhization vary depending on the plant and fungal species. The current study aimed to compare the effectiveness of a native inoculum from saline soil and two exotic isolates, Funneliformis mosseae and Rhizophagus irregularis on two Cajanus cajan (pigeonpea) genotypes (Paras, Pusa 2002) subjected to NaCl stress. Salinity depleted nodulation and nutrient status in both genotypes with higher negative effects in Paras. Although all AM fungi improved growth, R. irregularis performed better by promoting higher biomass accumulation, nodulation, N₂ fixation and N, P uptake which correlated with higher AM colonization. R. irregularis inoculated plants also accumulated higher trehalose in nodules due to decreased trehalase and increased trehalose-6-P synthase, trehalose-6-phosphatase activities. The results suggest that higher stability of R. irregularis-pigeonpea symbiosis under salt stress makes it an effective ameliorator for overcoming salt stress in pigeonpea.     

Fertilization and forb:graminoid ratio affect arbuscular mycorrhiza in seedlings but not adult plants of Plantago lanceolata

Aims

Nutrients play a key role in arbuscular mycorrhizal (AM) symbiosis. We quantified the response of AM symbiosis of seedlings and adult plants of Plantago lanceolata to fertilization under field conditions in managed grasslands differing in nutrient availability and soil moisture.

Methods

The AM symbiosis was measured as the total extent of AM fungal colonization and frequency of arbuscules or vesicles, and as the relative proportions of morphotypes. We further examined the effects of the surrounding vegetation upon AM symbiosis.

Results

Fertilization decreased total AM colonization and relative arbuscular frequency of the whole mycorrhizal community and of Acaulospora and “fine endophyte” morphotypes in seedling roots, but it had no effect upon the mycorrhiza in adult plants. The decline in arbuscular frequency in seedling roots due to fertilization was greater at the sites with higher nutrient availability and lower N:P ratio. Seedlings surrounded by more forbs had a greater total AM colonization and higher vesicular frequency.

Conclusions

Increased nutrient availability in the initial stages of seedling development has a prominent effect upon AM symbiosis development, but these effects seem to diminish over the long term, as evidenced by the results obtained for adult plants and from the limited effects of parameters characterizing long-term nutrient availability.     

Nitrogen limitation impairs plant control over the arbuscular mycorrhizal symbiosis in response to phosphorus and shading in two European sand dune species

The symbiosis of plants with arbuscular mycorrhizal fungi (AMF) may become parasitic if the cost:benefit ratio (carbon:phosphorus ratio) increases. In case of mycorrhizal parasitism, a plant may prevent growth depression through the reduction of root colonization as a form of control over the symbiosis. In this greenhouse study, we attempted to manipulate the cost:benefit ratio of the arbuscular mycorrhizal symbiosis by shading and/or phosphorus (P) fertilization in the differentially mycotrophic plant species Hieracium pilosella and Corynephorus canescens. By repeated sampling of soil cores, we assessed the temporal progress of plant investment towards mycorrhizal structures as a measure of plant control over the AMF. Unexpectedly, we found no obvious treatment effects on mycorrhizal growth dependency (MGD), most likely caused by constant N-limitation in AM plants being enhanced by P-fertilization and shade probably not exacerbating plant C-budget for AMF. This highlights the importance of N:P:C stoichiometry for the outcome of the symbiosis. Nevertheless, we found possible control mechanisms in shaded H. pilosella, with considerably higher resource investments into root than into hyphal growth, while root colonization was only marginally suppressed. This control only manifested after 4 weeks of growth under potentially detrimental conditions, emphasizing the importance of time in plant control over the arbuscular mycorrhizal symbiosis. In contrast, the less mycotrophic C. canescens did not exhibit obvious changes in mycorrhizal investments in reaction to shading and P-fertilization, possibly because the low mycotrophy and AMF colonization already imposes a functioning control mechanism in this species. Our study suggests that highly mycotrophic plants may have a stronger need to keep AMF in check than less mycotrophic plants, which may have implications for the role of mycotrophy in the outcome of symbiotic interactions in natural situations.     

Azospirillum and arbuscular mycorrhizal colonization enhance rice growth and physiological traits under well-watered and drought conditions

The response of rice plants to inoculation with an arbuscular mycorrhizal (AM) fungus, Azospirillum brasilense, or combination of both microorganisms, was assayed under well-watered or drought stress conditions. Water deficit treatment was imposed by reducing the amount of water added, but AM plants, with a significantly higher biomass, received the same amount of water as non-AM plants, with a poor biomass. Thus, the water stress treatment was more severe for AM plants than for non-AM plants. The results showed that AM colonization significantly enhanced rice growth under both water conditions, although the greatest rice development was reached in plants dually inoculated under well-watered conditions. Water level did not affect the efficiency of photosystem II, but both AM and A. brasilense inoculations increased this value. AM colonization increased stomatal conductance, particularly when associated with A. brasilense, which enhanced this parameter by 80% under drought conditions and by 35% under well-watered conditions as compared to single AM plants. Exposure of AM rice to drought stress decreased the high levels of glutathione that AM plants exhibited under well-watered conditions, while drought had no effect on the ascorbate content. The decrease of glutathione content in AM plants under drought stress conditions led to enhance lipid peroxidation. On the other hand, inoculation with the AM fungus itself increased ascorbate and proline as protective compounds to cope with the harmful effects of water limitation. Inoculation with A. brasilense also enhanced ascorbate accumulation, reaching a similar level as in AM plants. These results showed that, in spite of the fact that drought stress imposed by AM treatments was considerably more severe than non-AM treatments, rice plants benefited not only from the AM symbiosis but also from A. brasilense root colonization, regardless of the watering level. However, the beneficial effects of A. brasilense on most of the physiological and biochemical traits of rice plants were only clearly visible when the plants were mycorrhized. This microbial consortium was effective for rice plants as an acceptable and ecofriendly technology to improve plant performance and development.     

Increasing flavonoid concentrations in root exudates enhance associations between arbuscular mycorrhizal fungi and an invasive plant

Many invasive plants have enhanced mutualistic arbuscular mycorrhizal (AM) fungal associations, however, mechanisms underlying differences in AM fungal associations between introduced and native populations of invasive plants have not been explored. Here we test the hypothesis that variation in root exudate chemicals in invasive populations affects AM fungal colonization and then impacts plant performance. We examined flavonoids (quercetin and quercitrin) in root exudates of native and introduced populations of the invasive plant Triadica sebifera and tested their effects on AM fungi and plant performance. We found that plants from introduced populations had higher concentrations of quercetin in root exudates, greater AM fungal colonization and higher biomass. Applying root exudates more strongly increased AM fungal colonization of target plants and AM fungal spore germination when exudate donors were from introduced populations. The role of root exudate chemicals was further confirmed by decreased AM fungal colonization when activated charcoal was added into soil. Moreover, addition of quercetin into soil increased AM fungal colonization, indicating quercetin might be a key chemical signal stimulating AM fungal associations. Together these results suggest genetic differences in root exudate flavonoids play an important role in enhancing AM fungal associations and invasive plants’ performance, thus considering root exudate chemicals is critical to unveiling mechanisms governing shifting plant-soil microbe interactions during plant invasions.Subject terms: Population dynamics, Community ecology, Plant ecology     

Association of Criconemella xenoplax and Fusarium spp. with Root Necrosis and Growth of Peach

Criconemella xenoplax, Fusarium solani, and F. oxysporum caused necrosis of Nemaguard peach feeder roots in greenhouse tests. Root necrosis was more extensive in the presence of either fungus than wtih C. xenoplax alone. Shoot growth and plant height were less for plants inoculated with F. oxysporum or F. solani than for plants inoculated with the fungi plus C. xenoplax. Neither synergistic nor additive effects on root necrosis or plant growth occurred between C. xenoplax and the fungal pathogens.     

Plant–fungus competition for nitrogen erases mycorrhizal growth benefits of Andropogon gerardii under limited nitrogen supply

Considered to play an important role in plant mineral nutrition, arbuscular mycorrhizal (AM) symbiosis is a common relationship between the roots of a great majority of plant species and glomeromycotan fungi. Its effects on the plant host are highly context dependent, with the greatest benefits often observed in phosphorus (P)‐limited environments. Mycorrhizal contribution to plant nitrogen (N) nutrition is probably less important under most conditions. Moreover, inasmuch as both plant and fungi require substantial quantities of N for their growth, competition for N could potentially reduce net mycorrhizal benefits to the plant under conditions of limited N supply. Further compounded by increased belowground carbon (C) drain, the mycorrhizal costs could outweigh the benefits under severe N limitation. Using a field AM fungal community or a laboratory culture of Rhizophagus irregularis as mycorrhizal inoculants, we tested the contribution of mycorrhizal symbiosis to the growth, C allocation, and mineral nutrition of Andropogon gerardii growing in a nutrient‐poor substrate under variable N and P supplies. The plants unambiguously competed with the fungi for N when its supply was low, resulting in no or negative mycorrhizal growth and N‐uptake responses under such conditions. The field AM fungal communities manifested their potential to improve plant P nutrition only upon N fertilization, whereas the R. irregularis slightly yet significantly increased P uptake of its plant host (but not the host's growth) even without N supply. Coincident with increasing levels of root colonization by the AM fungal structures, both inoculants invariably increased nutritional and growth benefits to the host with increasing N supply. This, in turn, resulted in relieving plant P deficiency, which was persistent in non‐mycorrhizal plants across the entire range of nutrient supplies.