Type IV pili are involved in plant–microbe and fungus–microbe interactions

Adherence of bacteria to eukaryotic cells is essential for the initiation of infection in many animal and human pathogens, e.g. Neisseria gonorrhoeae and Pseudomonas aeruginosa . Adhesion-mediating type IV pili, filamentous surface appendages formed by pilin subunits, are crucial virulence factors. Here, we report that type IV pilus-dependent adhesion is also involved in plant–bacteria and fungus–bacteria interactions. Nitrogen-fixing, endophytic bacteria, Azoarcus sp., can infect the roots of rice and spread systemically into the shoot without causing symptoms of plant disease. Formation of pili on solid media was dependent on the pilAB locus. PilA encodes an unusually short (6.4 kDa) putative pilin precursor showing 100% homology to the conserved N-terminus of the Pseudomonas aeruginosa type IV pilin. PilB encodes for a 14.2 kDa polypeptide showing similarity to FimF, a component of type I fimbriae of Escherichia coli . It was found to be extruded beyond the cell surface by immunofluorescence studies, and it may, therefore, be part of a pilus assembly complex or the pilus itself. Both genes are involved in the establishment of bacteria on the root surface of rice seedlings, as detected by fluorescence microscopy. Moreover, both genes are necessary for bacterial adhesion to the mycelium of an ascomycete, which was isolated from the same rhizosphere as the bacteria. In co-culture with the fungus, Azoarcus sp. forms complex intracytoplasmic membranes, diazosomes, which are related to efficient nitrogen fixation. Adhesion to the mycelium appears to be crucial for this process, as diazosomes were absent and nitrogen fixation rates were decreased in pilAB mutants in co-culture.     

From plant–microbe interactions to symbiogenetics: a universal paradigm for the interspecies genetic integration

Beneficial plant–microbe symbioses are based on the integration of genetic material from diverse organisms resulting in formation of superorganism genetic systems. Analysis of their functions and evolution requires the establishment of a new biological discipline, proposed to be called symbiogenetics, which provides a basis for fundamental and applied research of the genetic control over different (symbiotic and biocenotic) biotic interactions. In ecology and agrobiology, the approaches of symbiogenetics are indispensable for optimising the interactions between the plants and the beneficial microbes to be used in ecosystem management and in sustainable crop production in which hazardous fertilisers and pesticides should be replaced by environmentally friendly microbial inoculants.     

The functional consequences of diversity in plant–pollinator interactions

The role of biological diversity in maintaining ecosystem functioning is a central issue in ecology. Most studies on diversity–functioning relationships have focused on ecosystem and community levels, leaving the extension of those relationships to other organization levels, such as populations, as a challenging and unsolved issue. Empirical studies have shown links between pollinator diversity and plant fecundity, suggesting that a diversity–functioning relationship at the population level may occur in pollination systems. We theoretically explored the effect of pollinator diversity on plant reproduction. We found that low pollinator diversity is beneficial when the most abundant pollinators are the most effective. In contrast, when the most effective pollinators are not the most abundant, we found an optimal value of pollinator diversity at which plant fecundity is maximized. When we parametrized our model with real data, we obtained that an increase in pollinator diversity was beneficial for the reproduction of some plants whereas it was harmful for other plants, the outcome depending exclusively on the differences in effectiveness among pollinators. Consequently, our theoretical approach suggests that in pollination systems the diversity–function relationship may be explained as the consequence of the interaction between among-pollinator differences in effectiveness and frequency of interaction, without the need to invoke additional ecological mechanisms.     

Refuge-mediated apparent competition in plant–consumer interactions

At the intersection of consumer behaviour and plant competition is the concept of refuge-mediated apparent competition: an indirect interaction whereby plants provide a refuge for a shared consumer, subsequently increasing consumer pressure on another plant species. Here, we use a simple model and empirical examples to develop and illustrate the concept of refuge-mediated apparent competition. We find that the likelihood that an inferior competitor will succeed via refuge-mediated apparent competition is greater when competitors have similar resource requirements and when consumers exhibit a strong response to the refuge and high attack rates on the superior competitor. Refuge-mediated apparent competition may create an emergent Allee effect, such that a species invades only if it is sufficiently abundant to alter consumer impact on resident species. This indirect interaction may help explain unresolved patterns observed in biological invasion, such as the different physical structure of invasive exotic plants, the lag phase, and the failure of restoration efforts. Given the ubiquity of refuge-seeking behaviour by consumers and the ability of consumers to alter the outcome of direct competition among plants, refuge-mediated apparent competition may be an underappreciated mechanism affecting the composition and diversity of plant communities.
Ecology Letters (2010) 13: 11–20     

Invariant properties in coevolutionary networks of plant–animal interactions

Plant–animal mutualistic networks are interaction webs consisting of two sets of entities, plant and animal species, whose evolutionary dynamics are deeply influenced by the outcomes of the interactions, yielding a diverse array of coevolutionary processes. These networks are two‐mode networks sharing many common properties with others such as food webs, social, and abiotic networks. Here we describe generalized patterns in the topology of 29 plant–pollinator and 24 plant–frugivore networks in natural communities. Scale‐free properties have been described for a number of biological, social, and abiotic networks; in contrast, most of the plant–animal mutualistic networks (65.6%) show species connectivity distributions (number of links per species) with a power‐law regime but decaying as a marked cut‐off, i.e. truncated power‐law or broad‐scale networks and few (22.2%) show scale‐invariance. We hypothesize that plant–animal mutualistic networks follow a build‐up process similar to complex abiotic nets, based on the preferential attachment of species. However, constraints in the addition of links such as morphological mismatching or phenological uncoupling between mutualistic partners, restrict the number of interactions established, causing deviations from scale‐invariance. This reveals generalized topological patterns characteristic of self‐organized complex systems. Relative to scale‐invariant networks, such constraints may confer higher robustness to the loss of keystone species that are the backbone of these webs.     

Conditional outcomes in plant–herbivore interactions: neighbours matter

Spatial distribution of palatable and unpalatable plants can influence the foraging behaviour of herbivores, thereby changing plant‐damage probabilities. Moreover, the immediate proximity to certain plants can benefit other plants that grow below them, where toxicity or spines act as a physical barrier or concealment against herbivores. This paper presents the results of a multi‐scale experiment performed to test the effect of shrubs as protectors of tree saplings against herbivores and the mechanism involved in Mediterranean ecosystems. We performed a factorial design in two mountain ranges, similar in physiognomy and vegetation, planting saplings of a palatable tree, the maple (Acer opalus subsp. granatense), and an unpalatable tree, the black pine (Pinus nigra), under three different types of shrubs. We considered four experimental microhabitats: highly palatable shrub (Amelanchier ovalis), palatable but spiny shrub (Crataegus monogyna or Prunus ramburii), unpalatable spiny shrub (Berberis vulgaris subsp. australis) and control (gaps of bare soil without shrubs). Three main factors were found to determine the probability of sapling attack: sapling palatability, experimental microhabitat and plot. Palatable saplings (maples) were browsed much more than unpalatable ones (pines). The degree of protection provided by the shrub proved greater as its palatability decreased with respect to sapling palatability, the unpalatable spiny shrub being the safest microhabitat for palatable saplings and bare soil for unpalatable ones. The differences found in number of attacked saplings between plots may be attributable to differences in herbivore pressure. The community context in which interaction takes place, namely the characteristics of the neighbours and the intensity of herbivore pressure, are determining factors for understanding and predicting the damage undergone by a target plant species. The mechanism that best explains these results is associational avoidance of saplings that grow near to unpalatable shrubs. It is necessary to introduce this neighbour effect in theoretical models and food‐web approaches that analyse the plant–herbivore relationships, since it can strongly determine not only the intensity of the interaction, but also the spatial distribution and diversity of the plant community.     

Integrating plant–soil interactions into global carbon cycle models

1.  Plant–soil interactions play a central role in the biogeochemical carbon (C), nitrogen (N) and hydrological cycles. In the context of global environmental change, they are important both in modulating the impact of climate change and in regulating the feedback of greenhouse gas emissions (CO₂, CH₄ and N₂O) to the climate system.
2.  Dynamic global vegetation models (DGVMs) represent the most advanced tools available to predict the impacts of global change on terrestrial ecosystem functions and to examine their feedbacks to climate change. The accurate representation of plant–soil interactions in these models is crucial to improving predictions of the effects of climate change on a global scale.
3.  In this paper, we describe the general structure of DGVMs that use plant functional types (PFTs) classifications as a means to integrate plant–soil interactions and illustrate how models have been developed to improve the simulation of: (a) soil carbon dynamics, (b) nitrogen cycling, (c) drought impacts and (d) vegetation dynamics. For each of these, we discuss some recent advances and identify knowledge gaps.
4.  We identify three ongoing challenges, requiring collaboration between the global modelling community and process ecologists. First, the need for a critical evaluation of the representation of plant–soil processes in global models; second, the need to supply and integrate knowledge into global models; third, the testing of global model simulations against large-scale multifactor experiments and data from observatory gradients.
5.   Synthesis . This paper reviews how plant–soil interactions are represented in DGVMs that use PFTs and illustrates some model developments. We also identify areas of ecological understanding and experimentation needed to reduce uncertainty in future carbon coupled climate change predictions.     

Soil community composition drives aboveground plant–herbivore–parasitoid interactions

Soil organisms can influence higher trophic level aboveground organisms, but only very few studies have considered such effects. We manipulated soil community composition of model grassland ecosystems by introducing nematode communities, microorganisms, neither or both groups. Above ground, aphids ( Rhopalosiphum padi ) and parasitoids ( Aphidius colemani ) were introduced, and we measured individual performance and population dynamics of plants, aphids and parasitoids. In microcosms with nematode inoculations either with or without microorganism inoculation, aphids offspring production was significantly reduced by 31%. Aphid populations on both host plants Agrostis capillaris and Anthoxanthum odoratum were lowest in microcosms with combined nematode and microorganism inoculations. Opposite results were found for parasitoids. While the number of emerged parasitoids did not differ between treatments, parasitoid mortality and the proportion of males were significantly lower in microcosms with nematode and microorganism inoculations. Parasitized aphids were significantly larger in microcosms with nematodes inoculated. Plant biomass did not differ, but in the preferred host plant A. odoratum , foliar phenolic content was reduced in the presence of nematodes, and also the concentration of amino acids in the phloem. This study shows that the composition of the soil community matters for aboveground multitrophic interactions.     

Effects of mycorrhizal symbiosis on tallgrass prairie plant–herbivore interactions

Complex relationships occur among plants, mycorrhizal fungi, and herbivores. By altering plant nutrient status, mycorrhizas may alter herbivory or plant tolerance to herbivory via compensatory regrowth. We examined these interactions by assessing grasshopper preference and plant growth and fungal colonization responses to herbivory under mycorrhizal and non‐mycorrhizal conditions within tallgrass prairie microcosms. Mycorrhizal symbiosis increased plant regrowth following defoliation, and some strongly mycotrophic plant species showed overcompensation in response to herbivory when they were mycorrhizal. Although grasshoppers spent more time on mycorrhizal plants, herbivory intensity did not differ between mycorrhizal and non‐mycorrhizal plants. Aboveground herbivory by grasshoppers significantly increased mycorrhizal fungal colonization of plant roots. Thus mycorrhizas may greatly benefit plants subjected to herbivory by stimulating compensatory growth, and herbivores, in turn, may increase the development of the symbiosis. Our results also indicate strong interspecific differences among tallgrass prairie plant species in their responses to the interaction of aboveground herbivores and mycorrhizal symbionts.     

Mutualism versus pathogenesis: the give-and-take in plant–bacteria interactions

Pathogenic bacteria and mutualistic rhizobia are able to invade and establish chronic infections within their host plants. The success of these plant–bacteria interactions requires evasion of the plant innate immunity by either avoiding recognition or by suppressing host defences. The primary plant innate immunity is triggered upon recognition of common microbe-associated molecular patterns. Different studies reveal striking similarities between the molecular bases underlying the perception of rhizobial nodulation factors and microbe-associated molecular patterns from plant pathogens. However, in contrast to general elicitors, nodulation factors can control plant defences when recognized by their cognate legumes. Nevertheless, in response to rhizobial infection, legumes show transient or local defence-like responses suggesting that Rhizobium is perceived as an intruder although the plant immunity is controlled. Whether these responses are involved in limiting the number of infections or whether they are required for the progression of the interaction is not yet clear. Further similarities in both plant–pathogen and Rhizobium –legume associations are factors such as surface polysaccharides, quorum sensing signals and secreted proteins, which play important roles in modulating plant defence responses and determining the outcome of the interactions.     

Latitudinal variation in plant–herbivore interactions in European salt marshes

Ecological interactions often vary geographically. Work in salt marshes on the Atlantic Coast of the United States has documented community-wide latitudinal gradients in plant palatability and plant traits that may be driven in part by greater herbivore pressure at low latitudes. To determine if similar patterns exist elsewhere, we studied six taxa of saltmarsh plants ( Atriplex , Juncus , Limonium , Salicornia , Spartina and Suaeda ) at European sites at high (Germany and the Netherlands) and low (Portugal and Spain) latitudes. We conducted feeding assays using both native and non-native consumers, and documented patterns of herbivore damage in the field. As in the United States, high-latitude plants tended to be more palatable than low-latitude plants when offered to consumers in paired feeding assays in the laboratory, although assays with grasshopper consumers were less consistent than those with crab consumers, and plants in the field at low-latitude sites tended to experience greater levels of herbivore pressure than plants at high-latitude sites. Similarly, high-latitude leaf litter was more palatable than litter from low-latitude plants when offered to consumers in paired feeding assays in the laboratory. Latitudinal gradients in plant palatability and herbivore pressure may be a general phenomenon, and may contribute to latitudinal gradients in decomposition processes.     

First insights into the genes that control plant–bacterial interactions

The events leading up to the cloning of the first bacterial avirulence gene, avrA , from Pseudomonas syringae pv. glycinea are described. The cloning of this gene marked the beginning of the molecular analyses of bacterial effectors and has paved the way for determining of the role of bacterial effectors in pathogen virulence and the triggering of plant innate immunity.