Sex-specific responses to mycorrhiza in a dioecious species

In most studies about dioecious plants, the role of arbuscular mycorrhizae (AM) and the potential sex-specific differences between the plant hosts have been overlooked. Because plant sexes frequently differ in drought tolerance and AM fungal colonization provides higher resistance to drought, we investigated whether the relation of mycorrhizal fungi with either male or female Antennaria dioica plants differs using a factorial experiment. We hypothesized that because AM usually increase growth rate and male plants usually grow larger than females, males should gain more benefit from the mycorrhizal symbiosis in terms of mineral nutrition and water supply. Because of higher demands of carbohydrates (C) in males, we expected males to allocate less C resources to the mycorrhizal fungus so that the associated fungi should benefit less of the association with males. In contrast to our initial hypothesis, the male plants, although faster growing under drought, did not gain more symbiosis-mediated benefits than did the females, and both sexes seemed to provide resources equally to their fungal symbiont. Therefore, we conclude that the two plant sexual morphs provide equal amounts of C to their fungal root symbionts and that they can gain specific benefits from the symbiosis, which, however, depend on soil water availability.     

Reduced Germination of Orobanche cumana Seeds in the Presence of Arbuscular Mycorrhizal Fungi or Their Exudates

Broomrapes (Orobanche and Phelipanche spp) are parasitic plants responsible for important crop losses, and efficient procedures to control these pests are scarce. Biological control is one of the possible strategies to tackle these pests. Arbuscular Mycorrhizal (AM) fungi are widespread soil microorganisms that live symbiotically with the roots of most plant species, and they have already been tested on sorghum for their ability to reduce infestation by witchweeds, another kind of parasitic plants. In this work AM fungi were evaluated as potential biocontrol agents against Orobanche cumana, a broomrape species that specifically attacks sunflower. When inoculated simultaneously with O. cumana seeds, AM fungi could offer a moderate level of protection against the broomrape. Interestingly, this protection did not only rely on a reduced production of parasitic seed germination stimulants, as was proposed in previous studies. Rather, mycorrhizal root exudates had a negative impact on the germination of O. cumana induced by germination stimulants. A similar effect could be obtained with AM spore exudates, establishing the fungal origin of at least part of the active compounds. Together, our results demonstrate that AM fungi themselves can lead to a reduced rate of parasitic seed germination, in addition to possible effects mediated by the mycorrhizal plant. Combined with the other benefits of AM symbiosis, these effects make AM fungi an attractive option for biological control of O. cumana.     

Sex‐specific interaction between arbuscular mycorrhizal and dark septate fungi in the dioecious plant Antennaria dioica (Asteraceae)

Male and female plants of dioecious species often differ in their resource demands and this has been linked to secondary sexual dimorphism, including sex‐specific interactions with other organisms such as herbivores and pollinators. However, little is known about the interaction between dioecious plants and fungal root endophytes. Plants may be simultaneously colonised by arbuscular mycorrhizal (AM) and dark septate (DS) fungi. While it is well established that AM mutualism involves reciprocal transfer of photosynthates and mineral nutrients between roots of host plants and these fungi, the role of DS fungi remains controversial. Here, we report the temporal and spatial variation in AM and DS fungi in female, male and non‐reproductive Antennaria dioica plants in three natural populations in Finland during flowering and after seed production. Females had higher colonisation by AM fungi, but lower colonisation by DS fungi than male and non‐reproductive plants. The higher AM colonisation was observed during flowering, and this difference varied among populations. Our results suggest that females and males of A. dioica interact with AM and DS fungi differently and that this relationship is dependent on soil fertility.     

Different arbuscular mycorrhizal interactions in male and female plants of wild Carica papaya L.

The different resource demands on male and female plants of dioecious species can lead to secondary sexual dimorphisms. Male and female plants might also interact differently with antagonists and mutualists. We used a repeated measures natural experiment in five subpopulations to investigate secondary sexual dimorphism in Carica papaya including interactions with arbuscular mycorrhizal fungi. Male and female plants did not differ in size or growth rate, but male plants flowered earlier than female plants. We observed different patterns of root colonization by arbuscular mycorrhizal fungi in male and female plants of C. papaya. These differences between the sexes preceded the flowering of most female plants. Female plants were sensitive to changes in soil fertility and adjusted the extent of their root colonization by arbuscular mycorrhizal fungi accordingly. Overall, the different resource demands on male and female plants seem to modulate the interactions of C. papaya with arbuscular mycorrhizal fungi.     

Variable mycorrhizal benefits on the reproductive output of Geranium sylvaticum,with special emphasis on the intermediate phenotype

In several gynodioecious species, intermediate sex between female and hermaphrodite has been reported, but few studies have investigated fitness parameters of this intermediate phenotype. Here, we examined the interactions between plant sex and arbuscular mycorrhizal (AM) fungal species affecting the reproductive output of Geranium sylvaticum, a sexually polymorphic plant species with frequent intermediate sexes between females and hermaphrodites, using a common garden experiment. Flowering phenology, AM colonisation levels and several plant vegetative and reproductive parameters, including seed and pollen production, were measured. Differences among sexes were detected in flowering, fruit set, pollen production and floral size. The two AM species used in the present work had different effects on plant fitness parameters. One AM species increased female fitness through increasing seed number and seed mass, while the other species reduced seed mass in all sexes investigated. AM fungi did not affect intermediate and hermaphrodite pollen content in anthers. The three sexes in G. sylvaticum did not differ in their reproductive output in terms of total seed production, but hermaphrodites had potentially larger fathering ability than intermediates due to higher anther number. The ultimate female function – seed production – did not differ among the sexes, but one of the AM fungi used potentially decreased host plant fitness. In addition, in the intermediate sex, mycorrhizal symbiosis functioned similarly in females as in hermaphrodites.     

Effects of inoculation with native arbuscular mycorrhizal fungi on clonal growth of Potentilla reptans and Fragaria moschata (Rosaceae)

Many clonal plants live in symbiosis with ubiquitous arbuscular mycorrhizal (AM) fungi, however, little is known about their interaction with respect to clonal reproduction and resource acquisition. The effects of arbuscular mycorrhiza on the growth and intraclonal integration between ramets of two stoloniferous species were studied experimentally in a nutritionally homogenous soil environment. Two species coexisting at the same field site, Potentilla reptans and Fragaria moschata, were selected as model plants for the study. Pairs of their ramets were grown in neighbouring pots with each ramet rooted separately. Four inoculation treatments were established: (1) both mother and daughter ramets remained non-inoculated, (2) both ramets were inoculated with a mixture of three native AM fungi from the site of plant origin, (3) only mother or (4) daughter ramet was inoculated. The stolons connecting the ramets were either left intact or were disrupted. Despite the consistent increase in phosphorus concentrations in inoculated plants, a negative growth response of both plant species to inoculation with AM fungi was observed and inoculated ramets produced fewer stolons and fewer offspring ramets and had lower total shoot dry weights as compared to non-inoculated ones. A difference in the extent of the negative mycorrhizal growth response was recorded between mother and daughter ramets of P. reptans, with daughter ramets being more susceptible. Due to AM effect on ramet performance, and thereby on the source-sink relationship, inoculation also significantly influenced biomass allocation within clonal fragments. Physiological integration between mother and daughter ramets was observed when their root systems were heterogeneous in terms of AM colonization. These results hence indicate the potential of mycorrhizal fungi to impact clonal growth traits of stoloniferous plant species, with possible consequences for their population dynamics.     

Strigolactones, signals for parasitic plants and arbuscular mycorrhizal fungi

Although strigolactones play a critical role as rhizospheric signaling molecules for the establishment of arbuscular mycorrhizal (AM) symbiosis and for seed germination of parasitic weeds, scarce data are available about interactions between AM fungi and strigolactones. In the present work, we present background data on strigolactones from studies on their seed germination activity on the parasitic weeds Orobanche and Striga, the importance of nitrogen and phosphorus for this seed germination activity, and what this could mean for AM fungi. We also present results on the susceptibility of plants to AM fungi and the possible involvement of strigolactones in this AM susceptibility and discuss the role of strigolactones for the formation and the regulation of the AM symbiosis as well as the possible implication of these compounds as plant signals in other soil-borne plant–microbe interactions.     

Effects of arbuscular mycorrhizal infection on the growth and reproduction of the annual legumeKummerowia striata growing in a nutrient-poor alluvial soil

A culture experiment was conducted to examine the effects of arbuscular mycorrhizal (AM) fungi on the growth and reproduction ofKummerowia striata, a common annual legume of river floodplains of Japan. The plants were grown from seeds in pots with nutrient-poor sandy soil collected from a fluvial bar. Arbuscular mycorrhizal infection increased the aboveground biomass, nodule weight, leaf nitrogen concentration and seed production. However, flowering occurred earlier in plants without AM fungi. These effects of AM fungi were insignificant in plants supplied with phosphate. These results suggest that AM fungi may influence the establishment ofK. striata in nutrient-poor, disturbed habitats.     

Land-use change impact on mycorrhizal symbiosis in female and male plants of wild <Emphasis Type="Italic">Carica papaya</Emphasis> (Caricaceae)

It has been acknowledged that land-use change has negative effects on genetic diversity and sex ratio in dioecious species, but less attention has been paid on the influence that land-use change has on the biotic interactions, especially between dioecious species and arbuscular mycorrhizal (AM) fungi. AM mutualism involves reciprocal transfer of carbohydrates and mineral nutrients between the host plant’s roots and these fungi. Here, we report spatial and temporal variation in AM colonization in dioecious wild Carica papaya plants growing in sites with different land use intensity. We tagged, recorded the basal stem circumference and collected roots of reproductive female and male Carica papaya plants in three wild sites during dry and rainy seasons of western Mexico. We also collected soil samples in each site to conduct soil chemical analyses. The sexes of C. papaya did not show significant differences in the frequency (percentage of root colonized by intraradical fungal structures) and abundance (length of intraradical hyphae) of AM fungi but the higher AM colonization was observed during the dry season, and in the site with the lowest disturbance. There was no relationship between soil chemistry and AM colonization. Overall, our findings suggest that land-use intensity has a negative effect on AM colonization and we discuss the consequences of habitat loss for the reproductive female and male plants, the implications of decreasing AM colonization for wild Carica papaya plants an important species that provides a source of genetic variation for the C. papaya varieties.     

Effect of arbuscular mycorrhizal fungi inoculation on root traits and root volatile organic compound emissions of Sorghum bicolor

Volatile organic compounds (VOCs) emitted by plant roots have important functions that can influence the rhizospheric environment. The aim of this study was to examine the effects of arbuscular mycorrhizal (AM) fungi on the profile of root VOCs. Sorghum (Sorghum bicolor) plants were grown in pots inoculated with either Glomus mosseae or Glomus intraradices, which formed mycorrhiza with the roots. Control plants were grown in pots inoculated with sterile inoculum and did not form mycorrhiza. Forty-four VOCs were determined using headspace solid-phase microextraction (HS-SPME) and gas chromatography–mass spectrometry (GC-MS). Alkanes were the most abundant type of VOCs emitted by both mycorrhizal and non-mycorrhizal plants. Both the quantity and type of volatiles were dramatically altered by the presence of AM fungi, and these changes had species specificity. Compared with non-mycorrhizal plants, mycorrhizal plants emitted more alcohols, alkenes, ethers and acids but fewer linear-alkanes. The AM fungi also influenced the morphological traits of the host roots. The total root length and specific root length of mycorrhizal plants were significantly greater than those of non-mycorrhizal plants; however, both the incidence and length of root-hair were dramatically decreased. Our findings confirm that AM fungi can alter the profile of VOCs emitted by roots as well as the root morphology of sorghum plants, indicating that AM fungi have the potential to help plants adapt to and alter soil environments.     

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.     

The arbuscular mycorrhizal fungus Rhizophagus intraradices and other microbial groups affect plant species in a copper-contaminated post-mining soil

Background and aimArbuscular mycorrhizal fungi (AMF) have an important role in plant-microbe interactions. But, there are few studies in which the combined effect of AMF with a stress factor, such as the presence of a metal, on plant species were assessed. This study investigated the effect of arbuscular mycorrhizal (AM) fungus Rhizophagus intraradices and other soil microbial groups in the presence of copper on three plant species in a microcosm experiment.MethodsTwo grass species Poa compressa and Festuca rubra and one herb species Centaurea jacea were selected as model plants in a pot-design test in which soils were artificially contaminated with copper. Treatments were bacteria (control), saprophytic fungi, protists, and a combined treatment of saprophytic fungi and protists, all in the presence or absence of the AM fungal species. After sixty days, plants were harvested and the biomass of grass and herb species and microbial respiration were measured.ResultsThe results showed almost equal above- and belowground plant biomass and microbial respiration in the treatments in the presence or absence of R. intraradices. The herb species C. jecea responded significantly to the soil inoculation with AM fungus, while grass species showed inconsistent patterns. Significant effect of AMF and copper and their interactions was observed on plant biomass when comparing contaminated vs. non-contaminated soils.ConclusionStrong effect of AMF on the biomass of herb species and slight changes in plant growth with the presence of this fungal species in copper-spiked test soils indicates the importance of mycorrhizal fungi compared to other soil microorganisms in our experimental microcosms.     

Competitive interactions are mediated in a sex‐specific manner by arbuscular mycorrhiza in Antennaria dioica

• Plants usually interact with other plants, and the outcome of such interaction ranges from facilitation to competition depending on the identity of the plants, including their sexual expression. Arbuscular mycorrhizal (AM) fungi have been shown to modify competitive interactions in plants. However, few studies have evaluated how AM fungi influence plant intraspecific and interspecific interactions in dioecious species.
• The competitive abilities of female and male plants of Antennaria dioica were examined in a greenhouse experiment. Females and males were grown in the following competitive settings: (i) without competition, (ii) with intrasexual competition, (iii) with intersexual competition, and (iv) with interspecific competition by Hieracium pilosella – a plant with similar characteristics to A. dioica. Half of the pots were grown with Claroideoglomus claroideum, an AM fungus isolated from the same habitat as the plant material. We evaluated plant survival, growth, flowering phenology, and production of AM fungal structures.
• Plant survival was unaffected by competition or AM fungi. Competition and the presence of AM fungi reduced plant biomass. However, the sexes responded differently to the interaction between fungal and competition treatments. Both intra‐ and interspecific competition results were sex‐specific, and in general, female performance was reduced by AM colonization. Plant competition or sex did not affect the intraradical structures, extraradical hyphae, or spore production of the AM fungus.
• These findings suggest that plant sexual differences affect fundamental processes such as competitive ability and symbiotic relationships with AM fungi.

     

Effects of the soil microbiome on the demography of two annual prairie plants

1. Both mutualistic and pathogenic soil microbes are known to play important roles in shaping the fitness of plants, likely affecting plants at different life cycle stages.
2. In order to investigate the differential effects of native soil mutualists and pathogens on plant fitness, we compared survival and reproduction of two annual tallgrass prairie plant species (Chamaecrista fasciculata and Coreopsis tinctoria) in a field study using 3 soil inocula treatments containing different compositions of microbes. The soil inocula types included fresh native whole soil taken from a remnant prairie containing both native mutualists and pathogens, soil enhanced with arbuscular mycorrhizal (AM) fungi derived from remnant prairies, and uninoculated controls.
3. For both species, plants inoculated with native prairie AM fungi performed much better than those in uninoculated soil for all parts of the life cycle. Plants in the native whole prairie soil were either generally similar to plants in the uninoculated soil or had slightly higher survival or reproduction.
4. Overall, these results suggest that native prairie AM fungi can have important positive effects on the fitness of early successional plants. As inclusion of prairie AM fungi and pathogens decreased plant fitness relative to prairie AM fungi alone, we expect that native pathogens also can have large effects on fitness of these annuals. Our findings support the use of AM fungi to enhance plant establishment in prairie restorations.

     

Symbiotic interactions between arbuscular mycorrhizal (AM) fungi and male papaya plants: Its status,role and implications

Experiments were conducted to study the arbuscular mycorrhizal (AM) status and its role in P-uptake through assay of root phosphatases activities in four varieties of male Carica papaya L. viz. CO-1, CO-2, Honey Dew and Washington during flowering stages. In the present study, mean total root colonization of AM fungi recorded peak increase in flowering stage-II while mean root phosphatase (acid and alkaline) activities recorded peak increase in flowering stage-I. Unlike root colonization and root phosphatase activities, spore density did not exhibit any definite patterns and recorded a narrow range of fluctuation during different flowering stages of male C. papaya. The study brought out the fact that root colonization and spore density of AM fungi along with root phosphatase activities varied significantly within the four varieties of male C. papaya plants during each flowering stage. The study also recorded consistently higher acid root phosphatase activity than alkaline root phosphatase activity under P-deficient, acidic soil conditions during all flowering stages of male C. papaya plants. Studies revealed that the root colonization of AM fungi influenced root phosphatase activities (acid and alkaline) positively and significantly during all flowering stages of male C. papaya plants. A total of twelve species of AM fungi belonging to five genera viz. Acaulospora, Dentiscutata, Gigaspora, Glomus, and Racocetra were recovered from the rhizosphere of male C. papaya plants.     

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.     

Exotic cheatgrass and loss of soil biota decrease the performance of a native grass

Soil disturbances can alter microbial communities including arbuscular mycorrhizal (AM) fungi, which may in turn, affect plant community structure and the abundance of exotic species. We hypothesized that altered soil microbial populations owing to disturbance would contribute to invasion by cheatgrass (Bromus tectorum), an exotic annual grass, at the expense of the native perennial grass, squirreltail (Elymus elymoides). Using a greenhouse experiment, we compared the responses of conspecific and heterospecific pairs of cheatgrass and squirreltail inoculated with soil (including live AM spores and other organisms) collected from fuel treatments with high, intermediate and no disturbance (pile burns, mastication, and intact woodlands) and a sterile control. Cheatgrass growth was unaffected by type of soil inoculum, whereas squirreltail growth, reproduction and nutrient uptake were higher in plants inoculated with soil from mastication and undisturbed treatments compared to pile burns and sterile controls. Squirreltail shoot biomass was positively correlated with AM colonization when inoculated with mastication and undisturbed soils, but not when inoculated with pile burn soils. In contrast, cheatgrass shoot biomass was negatively correlated with AM colonization, but this effect was less pronounced with pile burn inoculum. Cheatgrass had higher foliar N and P when grown with squirreltail compared to a conspecific, while squirreltail had lower foliar P, AM colonization and flower production when grown with cheatgrass. These results indicate that changes in AM communities resulting from high disturbance may favor exotic plant species that do not depend on mycorrhizal fungi, over native species that depend on particular taxa of AM fungi for growth and reproduction.     

Evidence for specificity to Glomus group Ab in two Asian mycoheterotrophic Burmannia species

Nonphotosynthetic mycorrhizal plants, so‐called mycoheterotrophic plants, have long attracted the curiosity of botanists and mycologists. Recent advances in molecular methods based on fungal‐specific PCR amplification have dramatically enhanced the identification of their host mycorrhizal fungi. However, studies investigating the fungal hosts of arbuscular mycorrhizae‐forming mycoheterotrophs are still limited in Asia, which is known as one of the diversity hot spots of mycoheterotrophs that parasitize arbuscular mycorrhizae (AM). Therefore, we aimed to reveal the mycorrhizal associations of two Asian, fully mycoheterotrophic Burmannia species by molecular identification. Sequences of the small subunit ribosomal DNA showed that both Burmannia species are associated with several distinct lineages of Glomus group Ab. Because Glomus group Ab fungi have been confirmed as fungal hosts of various mycoheterotrophic plants in Africa and South America, we suggest they are widely exploited by AM‐forming mycoheterotrophs globally.     

Different growth response of five co-existing stoloniferous plant species to inoculation with native arbuscular mycorrhizal fungi

Five species of stoloniferous plants originating from the same field site (Galeobdolon montanum, Glechoma hederacea, Potentilla anserina, Ranunculus repens and Trifolium repens) were studied with respect to their interaction with arbuscular mycorrhizal (AM) fungi. More specifically, the question was addressed whether mycorrhizal growth response of host plant species could be related to their vegetative mobility. The roots of all the species examined were colonised with AM fungi in the field, with the percentage of colonisation varying among species from approximately 40% to 90%. In a subsequent pot experiment, plants of all the species were either left non-inoculated or were inoculated with a mixture of three native AM fungi isolated from the site of plant origin (Glomus mosseae, G. intraradices and G. microaggregatum). AM fungi increased phosphorus uptake in all the plant species; however, plant growth response to inoculation varied widely from negative to positive. In addition to the biomass response, AM inoculation led to a change in clonal growth traits such as stolon number and length or ramet number in some species. Possible causes of the observed differences in mycorrhizal growth response of various stoloniferous plants are discussed.     

Sex-Related Responses of Populus cathayana Shoots and Roots to AM Fungi and Drought Stress

We investigated the impact of drought and arbuscular mycorrhizal (AM) fungi on the morphological structure and physiological function of shoots and roots of male and female seedlings of the dioecious plant Populus cathayana Rehder. Pot-grown seedlings were subjected to well watered or water-limiting conditions (drought) and were grown in soil that was either inoculated or not inoculated with the AM fungus Rhizophagus intraradices. No significant differences were found in the infection rates between the two sexes. Drought decreased root and shoot growth, biomass and root morphological characteristics, whereas superoxide radical (O₂–) and hydrogen peroxide content, peroxidase (POD) activity, malondialdehyde (MDA) concentration and proline content were significantly enhanced in both sexes. Male plants that formed an AM fungal symbiosis showed a significant increase in shoot and root morphological growth, increased proline content of leaves and roots, and increased POD activity in roots under both watering regimes; however, MDA concentration in the roots decreased. By contrast, AM fungi either had no effect or a slight negative effect on the shoot and root growth of female plants, with lower root biomass, total biomass and root/shoot ration under drought. In females, MDA concentration increased in leaves and roots under both watering regimes, and the proline content and POD activity of roots increased under drought conditions; however, POD activity significantly decreased under well-watered conditions. These findings suggest that AM fungi enhanced the tolerance of male plants to drought by improving shoot and root growth, biomass and the antioxidant system. Further investigation is needed to unravel the complex effects of AM fungi on the growth and antioxidant system of female plants.