SciCombinator

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Concept: Mycorrhiza

171

Very few principles have been unraveled that explain the relationship between soil properties and soil biota across large spatial scales and different land-use types. Here, we seek these general relationships using data from 52 differently managed grassland and forest soils in three study regions spanning a latitudinal gradient in Germany. We hypothesize that, after extraction of variation that is explained by location and land-use type, soil properties still explain significant proportions of variation in the abundance and diversity of soil biota. If the relationships between predictors and soil organisms were analyzed individually for each predictor group, soil properties explained the highest amount of variation in soil biota abundance and diversity, followed by land-use type and sampling location. After extraction of variation that originated from location or land-use, abiotic soil properties explained significant amounts of variation in fungal, meso- and macrofauna, but not in yeast or bacterial biomass or diversity. Nitrate or nitrogen concentration and fungal biomass were positively related, but nitrate concentration was negatively related to the abundances of Collembola and mites and to the myriapod species richness across a range of forest and grassland soils. The species richness of earthworms was positively correlated with clay content of soils independent of sample location and land-use type. Our study indicates that after accounting for heterogeneity resulting from large scale differences among sampling locations and land-use types, soil properties still explain significant proportions of variation in fungal and soil fauna abundance or diversity. However, soil biota was also related to processes that act at larger spatial scales and bacteria or soil yeasts only showed weak relationships to soil properties. We therefore argue that more general relationships between soil properties and soil biota can only be derived from future studies that consider larger spatial scales and different land-use types.

Concepts: Scientific method, Bacteria, Evolution, Yeast, Soil, Mycorrhiza, Humus, Soil life

170

This study aimed to evaluate the impact of genetically modified (GM) wheat with introduced pm3b mildew resistance transgene, on two types of root-colonizing microorganisms, namely pseudomonads and arbuscular mycorrhizal fungi (AMF). Our investigations were carried out in field trials over three field seasons and at two locations. Serial dilution in selective King’s B medium and microscopy were used to assess the abundance of cultivable pseudomonads and AMF, respectively. We developed a denaturing gradient gel electrophoresis (DGGE) method to characterize the diversity of the pqqC gene, which is involved in Pseudomonas phosphate solubilization. A major result was that in the first field season Pseudomonas abundances and diversity on roots of GM pm3b lines, but also on non-GM sister lines were different from those of the parental lines and conventional wheat cultivars. This indicates a strong effect of the procedures by which these plants were created, as GM and sister lines were generated via tissue cultures and propagated in the greenhouse. Moreover, Pseudomonas population sizes and DGGE profiles varied considerably between individual GM lines with different genomic locations of the pm3b transgene. At individual time points, differences in Pseudomonas and AMF accumulation between GM and control lines were detected, but they were not consistent and much less pronounced than differences detected between young and old plants, different conventional wheat cultivars or at different locations and field seasons. Thus, we conclude that impacts of GM wheat on plant-beneficial root-colonizing microorganisms are minor and not of ecological importance. The cultivation-independent pqqC-DGGE approach proved to be a useful tool for monitoring the dynamics of Pseudomonas populations in a wheat field and even sensitive enough for detecting population responses to altered plant physiology.

Concepts: Genetics, Bacteria, Biology, Plant, Fungus, Mycorrhiza, Glomeromycota, Arbuscular mycorrhiza

168

Fungal phospholipases are members of the fungal/bacterial group XIV secreted phospholipases A2 (sPLA2). TbSP1, the sPLA2 primarily addressed in this study, is upregulated by nutrient deprivation and is preferentially expressed in the symbiotic stage of the ectomycorrhizal fungus Tuber borchii. A peculiar feature of this phospholipase and of its ortholog from the black truffle T. melanosporum is the presence of a 54 amino acid sequence of unknown functional significance, interposed between the signal peptide and the start of the conserved catalytic core of the enzyme. X-ray diffraction analysis of a recombinant TbSP1 form corresponding to the secreted protein previously identified in T. borchii mycelia, revealed a structure comprising the five α-helices that form the phospholipase catalytic module, but lacking the N-terminal 54 amino acids. This finding led to a series of functional studies that showed that TbSP1, as well as its T. melanosporum ortholog, is a self-processing pro-phospholipase A2, whose phospholipase activity increases up to 80-fold following autoproteolytic removal of the N-terminal peptide. Proteolytic cleavage occurs within a serine-rich, intrinsically flexible region of TbSP1, does not involve the phospholipase active site, and proceeds via an intermolecular mechanism. Autoproteolytic activation, which also takes place at the surface of nutrient-starved, sPLA2 overexpressing hyphae, may strengthen and further control the effects of phospholipase upregulation in response to nutrient deprivation, also in the context of symbiosis establishment and mycorrhiza formation.

Concepts: Protein, Protein structure, Amino acid, Plant, Fungus, Mycorrhiza, Mycelium, Ascomycota

167

Arbuscular mycorrhizal fungi (AMF) and their bioprotective aspects are of great interest in the context of sustainable agriculture. Combining the benefits of AMF with the utilisation of plant species diversity shows great promise for the management of plant diseases in environmentally compatible agriculture. In the present study, AMF were tested against Fusarium oxysporum f. sp. lycopersici with tomato intercropped with either leek, cucumber, basil, fennel or tomato itself. Arbuscular mycorrhizal (AM) root colonisation of tomato was clearly affected by its intercropping partners. Tomato intercropped with leek showed even a 20 % higher AM colonisation rate than tomato intercropped with tomato. Positive effects of AMF expressed as an increase of tomato biomass compared to the untreated control treatment could be observed in root as well as in shoot weights. A compensation of negative effects of F. oxysporum f. sp. lycopersici on tomato biomass by AMF was observed in the tomato/leek combination. The intercropping partners leek, cucumber, basil and tomato had no effect on F. oxysporum f. sp. lycopersici disease incidence or disease severity indicating no allelopathic suppression; however, tomato co-cultivated with tomato clearly showed a negative effect on one plant/pot with regard to biomass and disease severity of F. oxysporum f. sp. lycopersici. Nonetheless, bioprotective effects of AMF resulting in the decrease of F. oxysporum f. sp. lycopersici disease severity were evident in treatments with AMF and F. oxysporum f. sp. lycopersici co-inoculation. However, these bioprotective effects depended on the intercropping partner since these effects were only observed in the tomato/leek and tomato/basil combination and for the better developed plant of tomato/tomato. In conclusion, the effects of the intercropping partner on AMF colonisation of tomato are of great interest for crop plant communities and for the influences on each other. The outcome of the bioprotective effects of AMF resulting in the decrease on F. oxysporum f. sp. lycopersici disease severity and/or compensation of plant biomass does not depend on the degree of AM colonisation but more on the intercropping partner.

Concepts: Plant, Fungus, Mycorrhiza, Glomeromycota, Arbuscular mycorrhiza, Fusarium oxysporum, Fruit, Ascomycota

70

Colonization of land by plants was a major transition on Earth, but the developmental and genetic innovations required for this transition remain unknown. Physiological studies and the fossil record strongly suggest that the ability of the first land plants to form symbiotic associations with beneficial fungi was one of these critical innovations. In angiosperms, genes required for the perception and transduction of diffusible fungal signals for root colonization and for nutrient exchange have been characterized. However, the origin of these genes and their potential correlation with land colonization remain elusive. A comprehensive phylogenetic analysis of 259 transcriptomes and 10 green algal and basal land plant genomes, coupled with the characterization of the evolutionary path leading to the appearance of a key regulator, a calcium- and calmodulin-dependent protein kinase, showed that the symbiotic signaling pathway predated the first land plants. In contrast, downstream genes required for root colonization and their specific expression pattern probably appeared subsequent to the colonization of land. We conclude that the most recent common ancestor of extant land plants and green algae was preadapted for symbiotic associations. Subsequent improvement of this precursor stage in early land plants through rounds of gene duplication led to the acquisition of additional pathways and the ability to form a fully functional arbuscular mycorrhizal symbiosis.

Concepts: Algae, DNA, Evolution, Eukaryote, Plant, Fungus, Symbiosis, Mycorrhiza

43

The roots of most land plants are colonised by mycorrhizal fungi that provide mineral nutrients in exchange for carbon. Here, we show that mycorrhizal mycelia can also act as a conduit for signalling between plants, acting as an early warning system for herbivore attack. Insect herbivory causes systemic changes in the production of plant volatiles, particularly methyl salicylate, making bean plants, Vicia faba, repellent to aphids but attractive to aphid enemies such as parasitoids. We demonstrate that these effects can also occur in aphid-free plants but only when they are connected to aphid-infested plants via a common mycorrhizal mycelial network. This underground messaging system allows neighbouring plants to invoke herbivore defences before attack. Our findings demonstrate that common mycorrhizal mycelial networks can determine the outcome of multitrophic interactions by communicating information on herbivore attack between plants, thereby influencing the behaviour of both herbivores and their natural enemies.

Concepts: Plant, Fungus, Predation, Animal, Mycorrhiza, Mycelium, Herbivore, Warning system

28

Arbuscular mycorrhizal fungi (AMF) have been implicated in non-native plant invasion success and persistence. However, few studies have identified the AMF species associating directly with plant invaders, or how these associations differ from those of native plant species. Identifying changes to the AMF community due to plant invasion could yield key plant-AMF interactions necessary for the restoration of native plant communities. This research compared AMF associating with coexisting Bromus tectorum, an invasive annual grass, and Artemisia tridentata, the dominant native shrub in western North America. At three sites, soil and root samples from Bromus and Artemisia were collected. Sporulation was induced using trap cultures, and spores were identified using morphological characteristics. DNA was extracted from root and soil subsamples and amplified. Sequences obtained were aligned and analyzed to compare diversity, composition, and phylogenetic distance between hosts and sites. Richness of AMF species associated with Artemisia in cultures was higher than AMF species associated with Bromus. Gamma diversity was similar and beta diversity was higher in AMF associated with Bromus compared to Artemisia. AMF community composition differed between hosts in both cultures and roots. Two AMF species (Archaeospora trappei and Viscospora viscosum) associated more frequently with Artemisia than Bromus across multiple sites. AMF communities in Bromus roots were more phylogenetically dispersed than in Artemisia roots, indicating a greater competition for resources within the invasive grass. Bromus associated with an AMF community that differed from Artemisia in a number of ways, and these changes could restrict native plant establishment.

Concepts: Species, Plant, Fungus, Soil, Mycorrhiza, Glomeromycota, Arbuscular mycorrhiza, Plants

28

The outcome of a compatible mycorrhizal interaction is different from that in a compatible plant-pathogen interaction; however, it is not clear what mechanisms are used to evade or suppress the host defence. The aim of this work is to reveal differences between the interaction of Norway spruce roots to the pathogen Ceratocystis polonica and the ectomycorrhizal Laccaria bicolor, examine if L. bicolor is able to evade inducing host defence responses typically induced by pathogens, and test if prior inoculation with the ectomycorrhizal fungus affects the outcome of a later challenge with the pathogen. The pathogen was able to invade the roots and caused extensive necrosis, leading to seedling death, with or without prior inoculation with L. bicolor. The ectomycorrhizal L. bicolor colonised primary roots of the Norway spruce seedlings by partly covering, displacing and convoluting the cells of the outer root cortex, leaving the seedlings healthy. We detected increased total peroxidase activity, and staining indicating increased lignification in roots as a response to C. polonica. In L. bicolor inoculated roots there was no increase in total peroxidase activity, but an additional highly acidic peroxidase isoform appeared that was not present in healthy roots, or in roots invaded by the pathogen. Increased protease activity was detected in roots colonised by C. polonica, but little protease activity was detected in L. bicolor inoculated roots. These results suggest that the pathogen efficiently invades the roots despite the induced host defence responses, while L. bicolor suppresses or evades inducing such host responses in this experimental system.

Concepts: Plant, Fungus, Mycorrhiza, Glomeromycota, Arbuscular mycorrhiza, Root, Mycelium, Ascomycota

28

Mycorrhizal symbiosis is common among land plants including pteridophytes (monilophytes and lycophytes). In pteridophytes with diplohaplontic life cycle, mycorrhizal formations were mostly reported for sporophytes, but very few for gametophytes. To clarify the mycorrhizal association of photosynthetic gametophytes, field-collected gametophytes of Angiopteris lygodiifolia (Marattiaceae, n = 52) and Osmunda japonica (Osmundaceae, n = 45) were examined using microscopic and molecular techniques. Collected gametophytes were mostly cut into two pieces. One piece was used for light and scanning microscopic observations, and the other for molecular identification of plant species (chloroplast rbcL sequences) and mycorrhizal fungi (small subunit rDNA sequences). Microscopic observations showed that 96 % (50/52) of Angiopteris and 95 % (41/43) of Osmunda gametophytes contained intracellular hyphae with arbuscules and/or vesicles and fungal colonization was limited to the inner tissue of the thick midribs (cushion). Fungal DNA analyses showed that 92 % (48/52) of Angiopteris and 92 % (35/38) of Osmunda have sequences of arbuscular mycorrhizal fungi, which were highly divergent but all belonged to Glomus group A. These results suggest that A. lygodiifolia and O. japonica gametophytes consistently form arbuscular mycorrhizae. Mycorrhizal formation in wild fern gametophytes, based on large-scale sampling with molecular identification of host plant species, was demonstrated for the first time.

Concepts: Plant, Fungus, Symbiosis, Mycorrhiza, Glomeromycota, Arbuscular mycorrhiza, Fern, Mycelium

28

Due to their complementary roles in meeting plant nutritional needs, arbuscular mycorrhizal fungi (AMF) and nitrogen-fixing bacteria (N(2)-fixers) may have synergistic effects on plant communities. Using greenhouse microcosms, we tested the effects of AMF, N(2)-fixers (symbiotic: rhizobia, and associative: Azospirillum brasilense), and their potential interactions on the productivity, diversity, and species composition of diverse tallgrass prairie communities and on the productivity of Panicum virgatum in monoculture. Our results demonstrate the importance of AMF and N(2)-fixers as drivers of plant community structure and function. In the communities, we found a positive effect of AMF on diversity and productivity, but a negative effect of N(2)-fixers on productivity. Both AMF and N(2)-fixers affected relative abundances of species. AMF shifted the communities from dominance by Elymus canadensis to Sorghastrum nutans, and seven other species increased in abundance with AMF, accounting for the increased diversity. N(2)-fixers led to increases in Astragalus canadensis and Desmanthus illinoense, two legumes that likely benefited from the presence of the appropriate rhizobia symbionts. Sorghastrum nutans declined 44 % in the presence of N(2)-fixers, with the most likely explanation being increased competition from legumes. Panicum monocultures were more productive with AMF, but showed no response to N(2)-fixers, although inference was constrained by low Azospirillum treatment effectivity. We did not find interactions between AMF and N(2)-fixers in communities or Panicum monocultures, indicating that short-term effects of these microbial functional groups are additive.

Concepts: Plant, Fungus, Symbiosis, Mycorrhiza, Glomeromycota, Arbuscular mycorrhiza, Nitrogen, Rhizobia