Systemic inhibition of arbuscular mycorrhiza development by root exudates of cucumber plants colonized by<Emphasis Type="Italic"> Glomus mosseae</Emphasis>

The arbuscular mycorrhizal (AM) non-host plants mustard, sugar beet, lupin and the AM host plant cucumber were used as test plants. Cucumber plants were grown either in the absence of the AM fungus (AMF) Glomus mosseae or in a split-root system, with one side mycorrhizal and one side non-mycorrhizal. Root exudates of the AM non-host plants, the non-mycorrhizal cucumber plants and the mycorrhizal and the non-mycorrhizal side of the split-root system of mycorrhizal cucumber plants were collected and applied to cucumber plants inoculated with the AMF. Root exudates of non-mycorrhizal cucumber plants showed a significant stimulatory effect on root colonization, whereas root exudates from the mycorrhizal and the non-mycorrhizal sides of a split-root system of a mycorrhizal cucumber plant did not show this stimulatory effect and were even slightly inhibitory. Root exudates of the two AM non-host plants mustard and sugar beet significantly reduced root colonization in cucumber plants, whereas no such effect was observed when root exudates of the AM non-host plant lupin were applied.     

An active factor from tomato root exudates plays an important role in efficient establishment of mycorrhizal symbiosis

Root exudates play an important role in the early signal exchange between host plants and arbuscular mycorrhizal fungi. M161, a pre-mycorrhizal infection (pmi) mutant of the tomoto (Solanum lycopersicum) cultivar Micro-Tom, fails to establish normal arbuscular mycorrhizal symbioses, and produces exudates that are unable to stimulate hyphal growth and branching of Glomus intraradices. Here, we report the identification of a purified active factor (AF) that is present in the root exudates of wild-type tomato, but absent in those of M161. A complementation assay using the dual root organ culture system showed that the AF could induce fungal growth and branching at the pre-infection stage and, subsequently, the formation of viable new spores in the M161 background. Since the AF-mediated stimulation of hyphal growth and branching requires the presence of the M161 root, our data suggest that the AF is essential but not sufficient for hyphal growth and branching. We propose that the AF, which remains to be chemically determined, represents a plant signal molecule that plays an important role in the efficient establishment of mycorrhizal symbioses.     

Relationship between the concentration of sugars in the roots and VA mycorrhizal infection

Summary The VA-infected wheat varieties showed an increase of total (Lozano var.) and reducing (Lozano and Pane vars.) sugars in their root extracts. However, no clear relationship between sugar concentration in the root and VA mycorrhizal infection level could be established.In addition, the VA mycorrhizal hosts sorghum, alfalfa, sunflower and maize, and non-host radish and cabbage plants were tested for sugar content in their root extracts after fifteen days of growth. Sugars present in the root extracts of these plants did not seem to be a decisive factor in plant susceptibility to VA infection.     

Development of a model system to assess the impact of genetically modified corn and aubergine plants on arbuscular mycorrhizal fungi

We developed an experimental model system to monitor the impact of generically modified (GM) plants on arbuscular mycorrhizal (AM) fungi, a group of non-target soil microorganisms, fundamental for soil fertility and plant nutrition. The system allowed us to study the effects of root exudates of both commercial Bt corn and aubergine plants expressing Dm-AMP1 defensin on different stages of the life cycle of the AM fungal species G. mosseae. Root exudates of Bt 176 corn significantly reduced pre-symbiotic hyphal growth, compared to Bt 11 and non-transgenic plants. No differences were found in mycelial growth in the presence of Dm-AMP1 and control plant root exudates. Differential hyphal morphogenesis occurred irrespective of the plant line, suggesting that both exuded Bt toxin and defensin do not interfere with fungal host recognition mechanisms. Bt 176 affected the regular development of appressoria, 36% of which failed to produce viable infection pegs. Our experimental model system represents an easy assay for testing the impact of GM plants on non-target soil-borne AM fungi.     

Role of the modification in root exudation induced by arbuscular mycorrhizal colonization on the intraradical growth of Phytophthora nicotianae in tomato

We studied the role of modification in root exudation induced by colonization with Glomus intraradices and Glomus mosseae in the growth of Phytophthora nicotianae in tomato roots. Plants were grown in a compartmentalized plant growth system and were either inoculated with the AM fungi or received exudates from mycorrhizal plants, with the corresponding controls. Three weeks after planting, the plants were inoculated or not with P. nicotianae growing from an adjacent compartment. At harvest, P. nicotianae biomass was significantly reduced in roots colonized with G. intraradices or G. mosseae in comparison to non-colonized roots. Conversely, pathogen biomass was similar in non-colonized roots supplied with exudates collected from mycorrhizal or non-mycorrhizal roots, or with water. We cannot rule out that a mycorrhiza-mediated modification in root exudation may take place, but our results did not support that a change in pathogen chemotactic responses to host root exudates may be involved in the inhibition of P. nicotianae.     

Plant growth strategy determines the magnitude and direction of drought-induced changes in root exudates in subtropical forests

Root exudates are an important pathway for plant–microbial interactions and are highly sensitive to climate change. However, how extreme drought affects root exudates and the main components, as well as species-specific differences in response magnitude and direction, are poorly understood. In this study, root exudation rates of total carbon (C) and its components (e.g., sugar, organic acid, and amino acid) were measured under the control and extreme drought treatments (i.e., 70% throughfall reduction) by in situ collection of four tree species with different growth rates in a subtropical forest. We also quantified soil properties, root morphological traits, and mycorrhizal infection rates to examine the driving factors underlying variations in root exudation. Our results showed that extreme drought significantly decreased root exudation rates of total C, sugar, and amino acid by 17.8%, 30.8%, and 35.0%, respectively, but increased root exudation rate of organic acid by 38.6%, which were largely associated with drought-induced changes in tree growth rates, root morphological traits, and mycorrhizal infection rates. Specifically, trees with relatively high growth rates were more responsive to drought for root exudation rates compared with those with relatively low growth rates, which were closely related to root morphological traits and mycorrhizal infection rates. These findings highlight the importance of plant growth strategy in mediating drought-induced changes in root exudation rates. The coordinations among root exudation rates, root morphological traits, and mycorrhizal symbioses in response to drought could be incorporated into land surface models to improve the prediction of climate change impacts on rhizosphere C dynamics in forest ecosystems.     

Striga seed-germination activity of root exudates and compounds present in stems of Striga host and nonhost (trap crop) plants is reduced due to root colonization by arbuscular mycorrhizal fungi

Root colonization by arbuscular mycorrhizal (AM) fungi reduces stimulation of seed germination of the plant parasite Striga (Orobanchaceae). This reduction can affect not only host plants for Striga, resulting in a lower parasite incidence, but also false hosts or trap crops, which induce suicidal Striga seed germination, thereby diminishing their effectiveness. In order to better understand these AM-induced effects, we tested the influence of root colonization by different AM fungi on the seed-germination activity of root exudates of the Striga hermonthica nonhost plants cowpea and cotton on S. hermonthica. We also tested the effect of AM fungi on the seed-germination activity of the Striga gesnerioides host plant cowpea on S. gesnerioides. Moreover, we studied whether mycorrhization affects the transport of seed-germination activity to above-ground plant parts. Mycorrhization not only resulted in a lower seed germination of S. gesnerioides in the presence of root exudates of the S. gesnerioides host cowpea but also seed germination of S. hermonthica was also lower in the presence of root exudates of the S. hermonthica nonhosts cowpea and cotton. Downregulation of the Striga seed-germination activity occurs not only in root exudates upon root colonization by different AM fungi but also in the compounds produced by stems. The lowered seed-germination activity does not appear to depend on the presence of seed germination inhibitors in the root exudates of mycorrhizal plants. The implication for Striga control in the field is discussed.     

Effect of onion (Allium cepa) root exudates on the hyphal growth of Gigaspora margarita

 The effect of root exudates from onions differing in P status on spore germination and hyphal growth of arbuscular mycorrhizal fungi was investigated. Onion (Allium cepa) was grown in solution culture at different phosphorus concentrations (0, 0.1, 1.0, 8.0 and 24.0 mg P l^–1) and root exudates were collected. When spores of the arbuscular mycorrhizal fungus, Gigaspora margarita were incubated with these root exudates, spore germination was only slightly affected but hyphal growth was greatly affected, particularly with exudates from P-deficient plants. This suggests that the P nutrition of host plants influences the composition of root exudates and thereby the hyphal growth of arbuscular mycorrhizal fungi. Accepted: 25 June 1995     

Mycorrhizal infection of wild oats: maternal effects on offspring growth and reproduction

Summary The objective of this study was to determine whether infection of Avena fatua L. plants by the mycorrhizal fungus Glomus intraradices Schenck & Smith could influence the vigor of the offspring generation. Two experiments demonstrated that mycorrhizal infection of the maternal generation had slight but persistent positive effects on offspring leaf expansion in the early stages of growth. In two other experiments, mycorrhizal infection of mother plants had several long lasting effects on their offspring. Offspring produced by mycorrhizal mother plants had greater leaf areas, shoot and root nutrient contents and root:shoot ratios compared to those produced by non-mycorrhizal mother plants. Moreover, mycorrhizal infection of mother plants significantly reduced the weight of individual seeds produced by offspring plants while it increased the P concentrations of the seeds and the number of seeds per spikelet produced by offspring plants. The effects of mycorrhizal infections of maternal plants on the vigor and performance of offspring plants were associated with higher seed phosphorus contents but generally lighter seeds. The results suggest that mycorrhizal infection may influence plant fitness by increasing offspring vigor and offspring reproductive success in addition to previously reported increases in maternal fecundity.     

Rapid and sensitive bioassay to study signals between root exudates and arbuscular mycorrhizal fungi**

A sensitive bioassay was developed to provide a way to detect chemical signals from host plants which induce changes in hyphal growth patterns of germinated spores of arbuscular mycorrhizal (AM) fungi. The assay can be used to test host root exudates, as well as particulate fractions (root cap border cells and root mucilage), for their ability to affect AM fungal growth. Hyphal branching, induced by various host root components, can be detected as early as 4 h although results of the bioassay were usually determined after 16 to 24 h. The type of branching pattern observed was dose-dependent.     

Anisohydric behaviour in grapevines results in better performance under moderate water stress and recovery than isohydric behaviour

Aims

Arbuscular mycorrhizal fungi (AMF) can control root-knot nematode infection, but the mode of action is still unknown. We investigated the effects of AMF and mycorrhizal root exudates on the initial steps of Meloidogyne incognita infection, namely movement towards and penetration of tomato roots.

Methods

M. incognita soil migration and root penetration were evaluated in a twin-chamber set-up consisting of a control and mycorrhizal (Glomus mosseae) plant compartment (Solanum lycopersicum cv. Marmande) connected by a bridge. Penetration into control and mycorrhizal roots was also assessed when non-mycorrhizal or mycorrhizal root exudates were applied and nematode motility in the presence of the root exudates was tested in vitro.

Results

M. incognita penetration was significantly reduced in mycorrhizal roots compared to control roots. In the twin-chamber set-up, equal numbers of nematodes moved to both compartments, but the majority accumulated in the soil of the mycorrhizal plant compartment, while for the control plants the majority penetrated the roots. Application of mycorrhizal root exudates further reduced nematode penetration in mycorrhizal plants and temporarily paralyzed nematodes, compared with application of water or non-mycorrhizal root exudates.

Conclusions

Nematode penetration was reduced in mycorrhizal tomato roots and mycorrhizal root exudates probably contributed at least partially by affecting nematode motility.     

Phosphorus deficiency in red clover promotes exudation of orobanchol,the signal for mycorrhizal symbionts and germination stimulant for root parasites

Plant derived sesquiterpene strigolactones, which have previously been characterized as germination stimulants for root parasitic plants, have recently been identified as the branching factors which induce hyphal branching morphogenesis, a critical step in host recognition by arbuscular mycorrhizal (AM) fungi. We show here that, in red clover plants (Trifolium pratense L.), which is known as a host for both AM fungi and the root holoparasitic plant Orobanche minor Sm., reduced supply of phosphorus (P) but not of other elements examined (N, K, Mg, Ca) in the culture medium significantly promotes the release of a strigolactone, orobanchol, by the roots of this plant. In red clover plants, the level of orobanchol exudation appeared to be regulated by P availability and was in good agreement with germination stimulation activity of the root exudates. This implies that under P deficiency, plant roots attract not only symbiotic fungi but also root parasitic plants through the release of strigolactones. This is the first report demonstrating that nutrient availability influences both symbiotic and parasitic interactions in the rhizosphere.     

Effect of root exudates of mycorrhizal tomato plants on microconidia germination of Fusarium oxysporum f. sp. lycopersici

The effect of root exudates from mycorrhizal and non-mycorrhizal tomato plants on microconidia germination of the tomato pathogen Fusarium oxysporum f. sp. lycopersici was tested. Microconidia germination was enhanced in the presence of root exudates from mycorrhizal tomato plants. Tomato plants were colonised by the arbuscular mycorrhizal fungus Glomus fasciculatum, indicating that alterations of the exudation pattern depended on the degree of root AM colonisation. Testing the exudates from plants with a high and a low P level revealed that the alterations of the root exudates from mycorrhizal plants, resulting in a changed effect on microconidia germination, are not due to an improved P status of mycorrhizal plants.     

Root exudates of mycorrhizal tomato plants exhibit a different effect on microconidia germination of Fusarium oxysporum f. sp. lycopersici than root exudates from non-mycorrhizal tomato plants

The effect of root exudates from mycorrhizal and non-mycorrhizal tomato plants on microconidia germination of the tomato pathogen Fusarium oxysporum f. sp. lycopersici was tested. Microconidia germination was enhanced in the presence of root exudates from mycorrhizal tomato plants. The more tomato plants were colonized by the arbuscular mycorrhizal fungus Glomus mosseae, the more microconidia germination was increased, indicating that alterations of the exudation pattern depended on the degree of root AM colonization. Moreover, alterations of the exudation pattern of mycorrhizal plants are not only local, but also systemic. Testing the exudates from plants with a high and a low P level revealed that the alterations of the root exudates from mycorrhizal plants, resulting in a changed effect on microconidia germination, are not due to an improved P status of mycorrhizal plants.     

Manganese reduction in the rhizosphere of mycorrhizal and nonmycorrhizal maize

The influence of rhizosphere microorganisms and vesicular-arbuscular (VA) mycorrhiza on manganese (Mn) uptake in maize (Zea mays L. cv. Tau) plants was studied in pot experiments under controlled environmental conditions. The plants were grown for 7 weeks in sterilized calcareous soil in pots having separate compartments for growth of roots and of VA mycorrhizal fungal hyphae. The soil was left either uninoculated (control) or prior to planting was inoculated with rhizosphere microorganisms only (MO-VA) or with rhizosphere microorganisms together with a VA mycorrhizal fungus [Glomus mosseae (Nicol and Gerd.) Gerdemann and Trappe] (MO+VA). Mycorrhiza treatment did not affect shoot dry weight, but root dry weight was slightly inhibited in the MO+VA and MO-VA treatments compared with the uninoculated control. Concentrations of Mn in shoots decreased in the order MO-VA > MO+VA > control. In the rhizosphere soil, the total microbial population was higher in mycorrhizal (MO+VA) than nonmycorrhizal (MO-VA) treatments, but the proportion of Mn-reducing microbial populations was fivefold higher in the nonmycorrhizal treatment, suggesting substantial qualitative changes in rhizosphere microbial populations upon root infection with the mycorrhizal fungi. The most important microbial group taking part in the reduction of Mn was fluorescent Pseudomonas. Mycorrhizal treatment decreased not only the number of Mn reducers but also the release of Mn-solubilizing root exudates, which were collected by percolation from maize plants cultivated in plastic tubes filled with gravel quartz sand. Compared with mycorrhizal plants, the root exudates of nonmycorrhizal plants had two fold higher capacity for reduction of Mn. Therefore, changes in both rhizosphere microbial population and root exudation are probably responsible for the lower acquisition of Mn in mycorrhizal plants.     

Arbuscular mycorrhizal fungi reduce growth and infect roots of the non‐host plant Arabidopsis thaliana

The arbuscular mycorrhizal (AM) symbiosis is widespread throughout the plant kingdom and important for plant nutrition and ecosystem functioning. Nonetheless, most terrestrial ecosystems also contain a considerable number of non‐mycorrhizal plants. The interaction of such non‐host plants with AM fungi (AMF) is still poorly understood. Here, in three complementary experiments, we investigated whether the non‐mycorrhizal plant Arabidopsis thaliana, the model organism for plant molecular biology and genetics, interacts with AMF. We grew A. thaliana alone or together with a mycorrhizal host species (either Trifolium pratense or Lolium multiflorum) in the presence or absence of the AMF Rhizophagus irregularis. Plants were grown in a dual‐compartment system with a hyphal mesh separating roots of A. thaliana from roots of the host species, avoiding direct root competition. The host plants in the system ensured the presence of an active AM fungal network. AM fungal networks caused growth depressions in A. thaliana of more than 50% which were not observed in the absence of host plants. Microscopy analyses revealed that R. irregularis supported by a host plant was capable of infecting A. thaliana root tissues (up to 43% of root length colonized), but no arbuscules were observed. The results reveal high susceptibility of A. thaliana to R. irregularis, suggesting that A. thaliana is a suitable model plant to study non‐host/AMF interactions and the biological basis of AM incompatibility.     

Density-dependent response to mycorrhizal infection in Abutilon theophrasti Medic

Summary One purpose of this study was to determine whether an increase in plant density would result in a decrease in response to mycorrhizal infection (particularly as measured by phosphorus content). Increases in plant density generally result in increases in root density in the volume of soil occupied by the plants. Root density, in turn, largely determines phosphorus uptake. If mycorrhizal plants had significantly higher effective root densities than non-mycorrhizal plants due to the fungal hyphae and thus were more thorough in exploiting a given volume of soil for phosphorus, then a given increase in root density might result in a greater proportional increase in phosphorus uptake for non-mycorrhizal plants than for mycorrhizal plants. Two experiments were performed in which mycorrhizal infection and available soil volume per plant were manipulated; one in which the number of plants within a given pot size was varied (experiment 1), and another in which single plants were grown in pots of differing volume (experiment 2). The two experiments yielded similar results but for apparently different reasons. In the first experiment, for a given increase in root density, non-mycorrhizal plants had a greater proportional increase in phosphorus uptake than mycorrhizal plants. Thus, as predicted, response to mycorrhizal infection was greatest at the lowest planting density (highest available soil volume per plant, lowest root density). In experiment 2, response to infection was also greatest at the highest available soil volume per plant (largest pot), but pot size did not influence root density. These results show that the benefit from mycorrhizal infection may be partly determined by root density and they suggest that plants either occurring in patches of contrasting root density in a given community, or occurring in different communities with inherently different root densities may differ in their reliance upon mycorrhizal fungi for phosphorus uptake.     

Effects of vesicular-arbuscular mycorrhizal infection and phosphate on Plantago major ssp. pleiosperma in relation to the internal phosphate concentration

Two experiments were carried out to study physiological effects of vesicular-arbuseular mycorrhizal infection on Plantago major L., ssp. pleiosperma (Pilger). In the first experiment, infection by the Glomus fasciculatum (Thaxt. sensu Gerdemann) Gerdemann and Trappe increased growth, shoot to root ratio, P concentrations in both shoot and roots and total uptake of P per plant. The percentages of dry matter in both shoot and roots were lower in mycorrhizal plants.
In the second experiment different P treatments were applied to both mycorrhizal and non-mycorrhizal P. major plants to separate any effects of mycorrhizal infection from increased uptake of P. In addition to the effects found in the first experiment, mycorrhizal, P, and mycorrhizal x P interaction effects were found on root respiration rate and the concentration of soluble sugars in the roots. No clear effects on total dry weight, N and starch concentrations in shoot and roots and sugar concentraion in the shoot were found. Irrespective of the mycorrhizal treatment, increased P concentration in the shoot correlated with an increased shoot to root ratio and root respiration rate, and a decreased percentage dry matter and sugar concentration in the roots. However, the root respiration rate and the P concentration in the roots of mycorrhizal plants were enhanced more than expected from the increased P concentrations in the shoots of these plants.     

Mycorrhizal symbiosis increases growth,reproduction and recruitment of Abutilon theophrasti Medic. in the field

We examined in the field the effect of the vesicular-arbuscular (VA) mycorhizal symbiosis on the reproductive success of Abutilon theophrasti Medic., an early successional annual member of the Malvaceae. Mycorrhizal infection greatly enhanced vegetative growth, and flower, fruit and seed production, resulting in significantly greater recruitment the following year. In addition, the seeds produced by mycorrhizal plants were significantly larger and contained significantly more phosphorus than seeds from non-mycorrhizal plants, an effect which may improve offspring vigor. Infection by mycorrhizal fungi may thus contribute to the overall fitness of a host plant and strongly influence long-term plant population dynamics.     

Casuarina root exudates alter the physiology, surface properties, and plant infectivity of Frankia sp. strain CcI3

The actinomycete genus Frankia forms nitrogen-fixing symbioses with 8 different families of actinorhizal plants, representing more than 200 different species. Very little is known about the initial molecular interactions between Frankia and host plants in the rhizosphere. Root exudates are important in Rhizobium-legume symbiosis, especially for initiating Nod factor synthesis. We measured differences in Frankia physiology after exposure to host aqueous root exudates to assess their effects on actinorhizal symbioses. Casuarina cunninghamiana root exudates were collected from plants under nitrogen-sufficient and -deficient conditions and tested on Frankia sp. strain CcI3. Root exudates increased the growth yield of Frankia in the presence of a carbon source, but Frankia was unable to use the root exudates as a sole carbon or energy source. Exposure to root exudates caused hyphal "curling" in Frankia cells, suggesting a chemotrophic response or surface property change. Exposure to root exudates altered Congo red dye binding, which indicated changes in the bacterial surface properties at the fatty acid level. Fourier transform infrared spectroscopy (FTIR) confirmed fatty acid changes and revealed further carbohydrate changes. Frankia cells preexposed to C. cunninghamiana root exudates for 6 days formed nodules on the host plant significantly earlier than control cells. These data support the hypothesis of early chemical signaling between actinorhizal host plants and Frankia in the rhizosphere.