Stavros D. Veresoglou

Suppression of fungal and nematode plant pathogens through arbuscular mycorrhizal fungi

Arbuscular mycorrhizal (AM) fungi represent ubiquitous mutualists of terrestrial plants. Through the symbiosis, plant hosts, among other benefits, receive protection from pathogens. A meta-analysis was conducted on 106 articles to determine whether, following pathogen infection of AM-colonized plants, the identity of the organisms involved (pathogens, AM fungi and host plants) had implications for the extent of the AM-induced pathogen suppression. Data on fungal and nematode pathogens were analysed separately. Although we found no differences in AM effectiveness with respect to the identity of the plant pathogen, the identity of the AM isolate had a dramatic effect on the level of pathogen protection. AM efficiency differences with respect to nematode pathogens were mainly limited to the number of AM isolates present; by contrast, modification of the ability to suppress fungal pathogens could occur even through changing the identity of the Glomeraceae isolate applied. N-fixing plants received more protection from fungal pathogens than non-N-fixing dicotyledons; this was attributed to the more intense AM colonization in N-fixing plants. Results have implications for understanding mycorrhizal ecology and agronomic applications.

Land use influences arbuscular mycorrhizal fungal communities in the farming–pastoral ecotone of northern China

We performed a landscape-scale investigation to compare the arbuscular mycorrhizal fungal (AMF) communities between grasslands and farmlands in the farming-pastoral ecotone of northern China. AMF richness and community composition were examined with 454 pyrosequencing. Structural equation modelling (SEM) and multivariate analyses were applied to disentangle the direct and indirect effects (mediated by multiple environmental factors) of land use on AMF. Land use conversion from grassland to farmland significantly reduced AMF richness and extraradical hyphal length density, and these land use types also differed significantly in AMF community composition. SEM showed that the effects of land use on AMF richness and hyphal length density in soil were primarily mediated by available phosphorus and soil structural quality. Soil texture was the strongest predictor of AMF community composition. Soil carbon, nitrogen and soil pH were also significantly correlated with AMF community composition, indicating that these abiotic variables could be responsible for some of the community composition differences among sites. Our study shows that land use has a partly predictable effect on AMF communities across this ecologically relevant area of China, and indicates that high soil phosphorus concentrations and poor soil structure are particularly detrimental to AMF in this fragile ecosystem.

Do arbuscular mycorrhizal fungi affect the allometric partition of host plant biomass to shoots and roots? A meta-analysis of studies from 1990 to 2010

Arbuscular mycorrhizas (AM) are ubiquitous root symbioses with often pervasive effects on the plant host, one of which may be above- and belowground biomass allocation. A meta-analysis was conducted on 516 trials that were described in 90 available articles to examine whether AM colonization could result in a modification of partitioning of plant biomass in shoots and roots. It was hypothesized that alleviating plant nutrient limitations could result in a decrease of root to shoot (R/S) ratio in AM plants or, alternatively, the direction of shifts in the R/S ratio would be determined by the changes in total dry biomass. In our analysis, we considered four types of stresses: drought stress, single heavy metal stress, multiple heavy metal stress, and other potential abiotic plant stress factors. When disregarding any factors that could regulate effects, including stress status and mode of propagation, the overall AM effect was a significant modification of biomass towards shoot growth. However, the responses of stressed and clonally propagated plants differed from those of seed-grown unstressed plants. Our meta-analysis detected a considerable decline in the R/S ratio when plants were grown from seeds in the absence of abiotic stresses. Moreover, we demonstrate that additional regulators of the AM-mediated impact on R/S ratio were presence of competition from other plants, plant growth outcome of the symbiosis, growth substrate volume, experimental duration, and the identities of both plant and AM fungus. Our results indicate that a prediction of AM effects on R/S allocation becomes more accurate when considering regulators, most notably propagation mode and stress. We discuss possible mechanisms through which stress and other regulators may operate.

Impact of inoculation with Azospirillum spp. on growth properties and seed yield of wheat: a meta-analysis of studies in the ISI Web of Science from 1981 to 2008

Azospirillum spp. represents one of the most studied plant growth promoting bacteria. A meta-analysis was conducted on 59 available articles to evaluate the extent to which Azospirillum may contribute to wheat growth properties. A mean increase of 8.9% in seed yield and 17.8% in aboveground dry weight was found to result from inoculation of wheat with Azospirillum. However, key determinants for the plant growth promoting effect were found to be the amount of N fertilization applied–maximum plant growth promoting effect was reported in the absence of N fertilization- and identities of wheat cultivar—Triticum aestivum was superior to Triticum durum-and Azospirillum isolate—Azospirillum lipoferum was more effective than Azospirillum brasilense. Co-inoculation with Azotobacter tended to further increase the growth promoting effect of Azospirillum on seed yield. A weak relationship between plant growth promoting effect on seed yield and aboveground biomass was detected. Inoculation with Azospirillum decreased the shoot:root ratio of wheat in field trials; but for pot trials, a key determinant of the shoot:root effect was the size of the pot used. The authors, thus, raise the scepticism of whether the growth parameters recorded in pot trials are representative of those under field conditions. Results highlight the efficiency of Azospirillum as an inoculant of wheat.

Extinction risk of soil biota

Belowground soil biota play key roles in maintaining proper ecosystem functioning, but studies on their extinction ecology are sparse. Here, Veresoglou et al. review the risks to soil biota posed by global change, and highlight the technical challenges involved in identifying extinction events.

Do closely related plants host similar arbuscular mycorrhizal fungal communities? A meta-analysis

AimsThe arbuscular mycorrhizal symbiosis is a widespread symbiosis in terrestrial biomes with functional implications for the ecology of both plants and soil organisms. We here asked whether phylogenetic host specificity (PHS) in arbuscular mycorrhizal (AM) fungal communities exists.MethodsData were retrieved from the online database MaarjAM and AM fungal sequences were clustered into taxa to allow us to compute community similarity indices. The phylogenetic reconstruction of the plant hosts allowed us to obtain an objective index of host relatedness. PHS was assessed through mixed effects linear models with community similarity as dependent variable, host relatedness as independent variable and with ecosystem type as covariate.ResultsTo our surprise not only did we not find evidence of PHS, but we detected evidence that more closely related plants hosted more dissimilar AM fungal communities. Results differed for different ecosystems.ConclusionsWe highlight the importance of ecosystem type when assessing PHS. Moreover, we argue for potential causes of the unique PHS patterns that are detected in the AM association.

Arbuscular mycorrhizal fungi – short‐term liability but long‐term benefits for soil carbon storage?

The interaction between plants and mycorrhizal fungi represents a major link between atmospheric and soil-contained carbon (C). In order to estimate the fate of atmospheric CO2 under the projected increases in the upcoming century, ranging from an increase of 20% to > 200% compared with current concentrations (Pachauri & Reisinger, 2007), it is crucial to understand how plants and mycorrhizal fungi either buffer or exacerbate atmospheric CO2 rises through their effects on soil C sequestration. Indirect evidence suggests that arbuscular mycorrhizal fungi (AMF) generally stimulate soil carbon pools (Wilson et al., 2009), and experience enhanced growth under elevated CO2 (eCO2) (Antoninka et al., 2011), leading to the assumption that they will buffer atmospheric CO2 increases. However, long-term experiments under eCO2 show both increased carbon storage (Iversen et al., 2012) and accelerated decomposition (negating the effect of the increase of soil carbon inputs; Phillips et al., 2012), leaving the question as to whether soils will buffer against CO2 increases wide open.While there is a dearth of direct empirical evidence regarding the involvement of AMF in soil C storage processes under conditions of global change, there is uncertainty about how component processes leading to soil C storage will be affected. Recently, Cheng et al. (2012) presented a compelling body of evidence to suggest that AMF may diminish rather than enhance soil C pools in the topsoil. Their findings are based on the observation that, in the presence of AMF, fresh above-ground plant litter decomposes faster, in particular at eCO2 and increased nitrogen (N) concentrations (Cheng et al., 2012). This observation suggests that AMF can accelerate decomposition and can even lead to a loss of soil C pools, at least in the short term. However, we feel that other parts of the soil C equation will need to be resolved in order to fully understand how AMF affect long-term soil C-sequestration potential. This is because short-term experiments do not account for potential increases in organic matter (OM) of plant or microbial origin triggered by increased decomposition; long-term (decadal scale) effects of soil biota such as AMF can be qualitatively different from short-term effects; and pulse increases of CO2 and N affect soils in a way that may not represent a system where CO2 and N are at consistently higher concentrations. Soil C sequestration is the net build-up of C in the entire soil profile through accumulation ofOM from plant, fungal (and other microbial) and animal origins. Decomposition of OM is an ongoing process, and snapshot rate assessments must therefore be interpreted with caution. If a particular nutrient (e.g. C or N) is elevated, this may lead to accelerated decomposition, but conclusions about soil C gain or loss can only be drawn if the effect of biomass increases of all biota is also incorporated into the equation (Fig. 1a). This becomes apparent in a simplemodel where AMF are allowed to produce recalcitrant compounds (such as various polysaccharides (K€ogel-Knabner, 2002) and glomalin, in line with experimental observations; Rillig, 2004) that contribute to the future OM fraction (see Fig. 1b). In the short term, an AMFmediated increase in decomposition of labile plant littermay lead to a reduction of soil C. However, the C balance is offset by a longterm gain in recalcitrant compounds (Fig. 1a). Contributions of AMF are likely to be further amplified through physically protecting OM from decomposition by means of soil aggregation (Rillig, 2004) and via a general increase in plant productivity and hence significantly higher litter input (Hoeksema et al., 2010). The principal mechanism by which AMF are proposed to stimulate soil C efflux is through priming of decomposers, which is a commonly observed soil-biotic response to increased (labile) OM deposition (de Graaff et al., 2010). However, whether this stimulation of soil saprobes is a permanent effect will require further study: C pulses and the resulting soil fungal community responses are a well-appreciated side-effect of sudden-onset CO2 exposure designs, which disappearwhenCO2 is gradually increased (Klironomos et al., 2005). Such sudden increases in atmospheric CO2 concentration are unlikely to happen in the near future. By contrast, other parameters will likely change under permanently altered amounts of resources, for instance litter quality. Decomposability of plant litter is known to decrease following plant exposure to eCO2 (Norby et al., 2001), and has the potential to buffer soil C concentrations against effects predicted from shortterm experiments. Thus the magnitude of priming effects through AMF under permanent eCO2 (as opposed to pulse elevation) must be scaled against indirect effects on litter quality to fully appreciate the contribution of AMF to plant-derived soil C concentrations. A way in which short-term experimental studies could control for some of these effects is to include additional treatments where soil and OM (thus controlling for factors such as soil aggregation and quantity and quality of litter) have been preconditioned, to the extent feasible, according to experimental treatments of interest (e.g. ambient vs eCO2; low vs high N; + vs AMF) in a factorial manner. Another highly useful addition might be a treatment where plant roots but not AMF can access plant litter generated under ambient vs eCO2 concentrations (a true nonAMF treatment). Even though these approaches do not resolve all fundamental issues arising from predicting long-term processes with short-term experiments, decomposition in the eCO2 and AMF treatments can be compared between ‘uniform’ and ‘preconditioned’ (according to treatment) plant and soil material. This way

Medium-term fertilization of grassland plant communities masks plant species-linked effects on soil microbial community structure

According to the singular hypothesis of plant diversity, different plant species are expected to make unique contributions to ecosystem functioning. Hence, individual species would support distinct microbial communities. It was hypothesized that microbial community dynamics in the respective rhizospheres of, two floristically divergent species, Agrostis capillaris and Prunella vulgaris that were dominant in a temperate, upland grassland in northern Greece, would support distinct microbial communities, in agreement to the singular hypothesis. Phospholipid lipid fatty acid (PLFA) profiles of the rhizosphere soil microbial community were obtained from the grassland which had been subjected to factorial nitrogen (N) and phosphorus (P) fertilization over five plant growth seasons. The soil cores analyzed were centered on stands of the two co-occurring target plant species, sampled from five blocks in all four factorial N and P fertilization combinations. Distinct PLFA clustering patterns following principle component analysis of PLFA concentrations revealed that, in the absence of P fertilization, soils under the two plant species supported divergent microbial communities. In the P fertilized plots, however, no such distinction could be observed. Results reveal that nutrient fertilization may mask the ability of plant species to shape their own rhizosphere microbial community.

Glomus intraradices and Gigaspora margarita arbuscular mycorrhizal associations differentially affect nitrogen and potassium nutrition of Plantago lanceolata in a low fertility dune soil

Two controlled microcosm experiments aimed at a critical re-assessment of the contributions of divergent arbuscular mycorrhizal (AM) fungi to plant mineral nutrition were established that specifically targeted Plantago lanceolata–Glomus intraradices (B.B/E) and –Gigaspora margarita (BEG 34) symbioses developed in a native, nutrient limited, coastal dune soil. Plant tissue nitrogen (N), phosphorus (P) and potassium (K) status as well as plant growth parameters and levels of mycorrhizal colonization were assessed at harvest. In addition to the general well-established mycorrhizal facilitation of P uptake, the study was able to demonstrate a G. intraradices-specific contribution to improved plant nitrogen and potassium nutrition. In the two respective experiments, G. intraradices-inoculated plants had 27.8% and 40.8% more total N and 55.8% and 23.3% more total K when compared to Gi. margarita inoculated counterparts. Dissimilar overall contribution of the two isolates to plant nutrition was identified in AM-genus specific differences in plant tissue N:P:K ratios. G. intraradices inoculated and non-mycorrhizal plants generally exhibited N:P:K ratios indicative of P limitation whereas for Gi. margarita mycorrhizal plants, corresponding ratios strongly implied either N or K limitation. The study provides further evidence highlighting AM functional biodiversity in respect to plant nutrient limitation experienced by mycorrhizal P. lanceolata in an ecologically relevant soil system.

Modelling the environmental and soil factors that shape the niches of two common arbuscular mycorrhizal fungal families

AimsArbuscular mycorrhizal (AM) fungi, a group of obligate symbionts of terrestrial plants, have a global distribution range. Yet, we lack concrete synthetic and empirical evidence that could reveal whether distinct ecological niches are distributed across Glomeromycota through determining linkages between environmental factors and the distribution of these taxa.MethodsWe have modelled the probability of occurrence of Gigasporaceae and Acaulosporaceae as a function of candidate environmental factors. These families are among the most common but non-ubiquitous taxa in AM-driven ecosystems. We have constructed our database using studies with a global scope and carried out our analysis through a logistic regression approach.ResultsThe probability of occurrence of Acaulosporacae increased in acidic environments and soils with high bulk density. By contrast, a key factor that affected probability of occurrence of Gigasporaceae was precipitation.ConclusionsThrough the analysis of an unprecedentedly large amount of data we could infer that niche processes mediate occurrence of a group of fungi at scales broader than the local scale of the individual studies gathered in the analysed dataset. Knowledge of well-supported niche features could enhance discovery of new taxa of AM fungi, and would facilitate development of study designs with greater ecological realism.