Evolutionary history shapes patterns of mutualistic benefit in Acacia–rhizobial interactions

The ecological and evolutionary factors that drive the emergence and maintenance of variation in mutualistic benefit (i.e., the benefits provided by one partner to another) in mutualistic symbioses are not well understood. In this study, we evaluated the role that host and symbiont phylogeny might play in determining patterns of mutualistic benefit for interactions among nine species of Acacia and 31 strains of nitrogen‐fixing rhizobial bacteria. Using phylogenetic comparative methods we compared patterns of variation in mutualistic benefit (host response to inoculation) to rhizobial phylogenies constructed from housekeeping and symbiosis genes; and a multigene host phylogeny. We found widespread genotype‐by‐genotype variation in patterns of plant growth. A relatively large component of this variation (21–28%) was strongly influenced by the interacting evolutionary histories of both partners, such that phylogenetically similar host species had similar growth responses when inoculated with phylogenetically similar rhizobia. We also found a relatively large nonphylogenetic effect for the average mutualistic benefit provided by rhizobia to plants, such that phylogenetic relatedness did not predict the overall benefit provided by rhizobia across all hosts. We conclude that phylogenetic relatedness should frequently predict patterns of mutualistic benefit in acacia‐rhizobial mutualistic interactions; but that some mutualistic traits also evolve independently of the phylogenies.     

Molecular genetic mechanisms used by legumes to control early stages of mutually beneficial (mutualistic) symbiosis

Recent data on the plant control of early stages of mutually beneficial (mutualistic) symbioses of legumes, the mechanisms of perception and transmission of the microsymbiont’s molecular signals in the macrosymbiont’s cells, and induction of the genetic programs of the development of symbiotic compartments and organs of the plant are summarized. It is demonstrated that the genetic system of the plant controlling the development of nitrogen-fixing symbiosis of legumes (symbiotic root nodules), which emerged 70–80 Ma ago, has undoubtedly evolved on the basis of the genetic system controlling the development of the symbiosis with arbuscular mycorrhizal fungi (which emerged 400–500 Ma ago). Interactions between genes and between gene products, as well as exchange of molecular signals, form the basis of mutually beneficial (mutualistic) plant-bacterium interactions. Even in the case of a highly specific nitrogen-fixing symbiosis of legumes (symbiotic nodules), the receptors perceiving the signal from root-nodule bacteria may function in different ways. The development of arbuscular mycorrhiza and nitrogen-fixing symbiosis in legumes is a multistep process involving hundreds of genes of both the macro- and microsymbionts. For the symbioses to develop successfully, these genes should act in a coordinated way in the newly formed superorganismal system. Further studies are necessary to shed light onto the complexity of the plant genetic control of the development of mutualistic symbioses in legumes and provide information required for improving their functions in adaptive plant-breeding systems.     

Pathogenic and mutualistic plant-bacteria interactions: ever increasing similarities

Plant-interacting bacteria can establish either mutualistic or pathogenic interactions that cause beneficial or detrimental effects respectively, to their hosts. In spite of the completely different outcomes, accumulating evidence indicates that similar molecular bases underlie the establishment of these two contrasting plant-bacteria associations. Recent findings observed in the mutualistic nitrogen-fixing Rhizobium-legume symbiosis add new elements to the increasing list of similarities. Amongst these, in this review we describe the role of plant resistance proteins in determining host specificity in the Rhizobium-legume symbiosis that resemble the gene-for-gene resistance of plant-pathogen interactions, and the production of antimicrobial peptides by certain legumes to control rhizobial proliferation within nodules. Amongst common bacterial strategies, cyclic diguanylate (c-di-GMP) appears to be a second messenger used by both pathogenic and mutualistic bacteria to regulate key features for interaction with their plant hosts.     

Insights into the history of the legume‐betaproteobacterial symbiosis

The interaction between legumes and rhizobia has been well studied in the context of a mutualistic, nitrogen‐fixing symbiosis. The fitness of legumes, including important agricultural crops, is enhanced by the plants’ ability to develop symbiotic associations with certain soil bacteria that fix atmospheric nitrogen into a utilizable form, namely, ammonia, via a chemical reaction that only bacteria and archaea can perform. Of the bacteria, members of the alpha subclass of the protebacteria are the best‐known nitrogen‐fixing symbionts of legumes. Recently, members of the beta subclass of the proteobacteria that induce nitrogen‐fixing nodules on legume roots in a species‐specific manner have been identified. In this issue, Bontemps et al. reveal that not only are these newly identified rhizobia novel in shifting the paradigm of our understanding of legume symbiosis, but also, based on symbiotic gene phylogenies, have a history that is both ancient and stable. Expanding our understanding of novel plant growth promoting rhizobia will be a valuable resource for incorporating alternative strategies of nitrogen fixation for enhancing plant growth.     

A reconciliation analysis of host switching in plant-fungal symbioses

Plant-fungal symbioses include many familiar antagonistic and mutualistic associations and some model cases of coevolution. The relationship between coevolution at the different evolutionary scales has remained an open question. Widespread host specificity and documented host switches offer conflicting indications of what to expect from comparisons of plant and fungal phylogenies. This study sought to establish the role of plant phylogeny in determining fungal phylogeny and the relative contributions of codivergence and host switching by comparing tree topologies for 15 plant-fungal symbioses. Second it attempted to characterize the relationship between phylogenetic congruence and switching. Trees were estimated from published sequences and reconciliation analysis was applied in the form of cophylogeny mapping using "jungles". This provided an exhaustive account of all possible switches capable of reconciling two associated phylogenies. A continuum of cophylogenetic dynamics was identified, ranging from mostly codivergence (e.g., Exobasidium) to mostly switching, (e.g., Erysiphe). Surprisingly, congruent solutions do not necessarily have fewer switches when using cophylogeny mapping, but a significant negative relationship between congruence and the distance of switches proved to be a useful indicator. According to reconciliation analysis, the contribution of host phylogeny varies widely across plant-fungal symbioses, making host specificity and coadaptation poor indicators of macroevolutionary trends because they are necessary, but not sufficient, conditions.     

Are common symbiosis genes required for endophytic rice-rhizobial interactions?

Legume plants are able to establish root nodule symbioses with nitrogen-fixing bacteria, called rhizobia. Recent studies revealed that the root nodule symbiosis has co-opted the signaling pathway that mediates the ancestral mycorrhizal symbiosis that occurs in most land plants. Despite being unable to induce nodulation, rhizobia have been shown to be able to infect and colonize the roots of non-legumes such as rice. One fascinating question is whether establishment of such associations requires the common symbiosis (Sym) genes that are essential for infection of plant cells by mycorrhizal fungi and rhizobia in legumes. Here, we demonstrated that the common Sym genes are not required for endophytic colonization of rice roots by nitrogen-fixing rhizobia.     

Themes from variation: probing the commonalities of symbiotic associations

Research on symbiosis (including antagonistic and mutualistic associations) wrestles, directly or indirectly, with the paradox: why are symbiotic associations so prevalent in the biosphere in the face of ubiquitous immune or antibiotic defenses among organisms? The symposium "Living Together: the Dynamics of Symbiotic Interactions" considered several questions: 1. How do symbiotic species partners come together? Do symbioses share similar patterns of signal recognition and response? 2. What roles do nutrients and metabolites play in symbiotic interactions, and how are metabolic exchanges affected by environmental changes? 3. In what ways do the dynamics of multispecies symbioses differ from two-species associations? 4. How do antagonistic (parasitic, pathogenic) symbioses differ from mutualistic ones? In what ways do changes in the biotic and physical environment affect the evolutionary balance of symbiotic associations? 5. What are the coevolutionary patterns of symbiotic associations? 6. Which research techniques, and strategies of experimental design, might be useful across a broad range of symbiotic associations?Two themes emerged from the symposium. First, all the participants have incorporated multiple techniques and perspectives into their work, approaches which facilitate the understanding of symbiotic dynamics at several levels of biological organization. Secondly, many of the papers addressed genetic and environmental variation in symbiotic interactions. Such approaches are useful tools for analysis of the mechanics of interspecies interactions and for characterization of the most important factors which influence them. They provide us with the tools to evaluate symbioses in a world of complexity, variation and change.     

Mutualism and parasitism: the yin and yang of plant symbioses

Plants are solar-powered sugar factories that feed a multitude of other organisms. Many of these organisms associate directly with host plants to gain access to the plant's photosynthates. Such symbioses encompass a wide collection of styles ranging from mutualistic to commensal and parasitic. Among these, the mutualistic arbuscular mycorrhizal (AM) symbiosis is one of the evolutionarily oldest symbioses of plants, relying on the formation of an intimate relationship between fungi of the Glomeromycota and roots of the majority of vascular flowering plants. In this symbiosis, the fungus intracellularly colonizes living root cells, implying the existence of an extreme form of compatibility. Interestingly, molecular events that happen in the plant in response to mycorrhizal colonization also occur in other beneficial and, as recently shown, even antagonistic plant symbioses. Thus, basic 'compatibility modules' appear to be partially conserved between mutualism and parasitism.     

Phylogenetic analysis of host–symbiont specificity and codivergence in bioluminescent symbioses

Several groups of marine fishes and squids form mutualistic bioluminescent symbioses with luminous bacteria. The dependence of the animal on its symbiont for light production, the animal's specialized anatomical adaptations for harboring bacteria and controlling light emission, and the host family bacterial species specificity characteristic of these associations suggest that bioluminescent symbioses are tightly coupled associations that might involve coevolutionary interactions. Consistent with this possibility, evidence of parallel cladogenesis has been reported for squid–bacterial associations. However, genetic adaptations in the bacteria necessary for and specific to symbiosis have not been identified, and unlike obligate endosymbiotic associations in which the bacteria are transferred vertically, bacterially bioluminescent hosts acquire their light‐organ symbionts from the environment with each new host generation. These contrasting observations led us to test the hypotheses of species specificity and codivergence in bioluminescent symbioses, using an extensive sampling of naturally formed associations. Thirty‐five species of fish in seven teleost families (Chlorophthalmidae, Macrouridae, Moridae, Trachichthyidae, Monocentridae, Acropomatidae, Leiognathidae) and their light‐organ bacteria were examined. Phylogenetic analysis of a taxonomically broad sampling of associations was based on mitochondrial 16S rRNA and cytochrome oxidase I gene sequences for the fish and on recA, gyrB and luxA sequences for bacteria isolated from the light organs of these specimens. In a fine‐scale test focused on Leiognathidae, phylogenetic analysis was based also on histone H3 subunit and 28S rRNA gene sequences for the fish and on gyrB, luxA, luxB, luxF and luxE sequences for the bacteria. Deep divergences were revealed among the fishes, and clear resolution was obtained between clades of the bacteria. In several associations, bacterial species identities contradicted strict host family bacterial species specificity. Furthermore, the fish and bacterial phylogenies exhibited no meaningful topological congruence; evolutionary divergence of host fishes was not matched by a similar pattern of diversification in the symbiotic bacteria. Re‐analysis of data reported for squids and their luminous bacteria also revealed no convincing evidence of codivergence. These results refute the hypothesis of strict host family bacterial species specificity and the hypothesis of codivergence in bioluminescent symbioses. © The Willi Hennig Society 2007.     

Water Stress Strengthens Mutualism Among Ants,Trees, and Scale Insects

Abiotic environmental variables strongly affect the outcomes of species interactions. For example, mutualistic interactions between species are often stronger when resources are limited. The effect might be indirect: water stress on plants can lead to carbon stress, which could alter carbon-mediated plant mutualisms. In mutualistic ant–plant symbioses, plants host ant colonies that defend them against herbivores. Here we show that the partners'' investments in a widespread ant–plant symbiosis increase with water stress across 26 sites along a Mesoamerican precipitation gradient. At lower precipitation levels, Cordia alliodora trees invest more carbon in Azteca ants via phloem-feeding scale insects that provide the ants with sugars, and the ants provide better defense of the carbon-producing leaves. Under water stress, the trees have smaller carbon pools. A model of the carbon trade-offs for the mutualistic partners shows that the observed strategies can arise from the carbon costs of rare but extreme events of herbivory in the rainy season. Thus, water limitation, together with the risk of herbivory, increases the strength of a carbon-based mutualism.     

The role of epiphytism in architecture and evolutionary constraint within mycorrhizal networks of tropical orchids

Characterizing the architecture of bipartite networks is increasingly used as a framework to study biotic interactions within their ecological context and to assess the extent to which evolutionary constraint shape them. Orchid mycorrhizal symbioses are particularly interesting as they are viewed as more beneficial for plants than for fungi, a situation expected to result in an asymmetry of biological constraint. This study addressed the architecture and phylogenetic constraint in these associations in tropical context. We identified a bipartite network including 73 orchid species and 95 taxonomic units of mycorrhizal fungi across the natural habitats of Reunion Island. Unlike some recent evidence for nestedness in mycorrhizal symbioses, we found a highly modular architecture that largely reflected an ecological barrier between epiphytic and terrestrial subnetworks. By testing for phylogenetic signal, the overall signal was stronger for both partners in the epiphytic subnetwork. Moreover, in the subnetwork of epiphytic angraecoid orchids, the signal in orchid phylogeny was stronger than the signal in fungal phylogeny. Epiphytic associations are therefore more conservative and may co‐evolve more than terrestrial ones. We suggest that such tighter phylogenetic specialization may have been driven by stressful life conditions in the epiphytic niches. In addition to paralleling recent insights into mycorrhizal networks, this study furthermore provides support for epiphytism as a major factor affecting ecological assemblage and evolutionary constraint in tropical mycorrhizal symbioses.     

A roadmap of plant membrane transporters in arbuscular mycorrhizal and legume–rhizobium symbioses

Most land plants live in close contact with beneficial soil microbes: the majority of land plant species establish symbiosis with arbuscular mycorrhizal fungi, while most legumes, the third largest plant family, can form a symbiosis with nitrogen-fixing rhizobia. These microbes contribute to plant nutrition via endosymbiotic processes that require modulating the expression and function of plant transporter systems. The efficient contribution of these symbionts involves precisely controlled integration of transport, which is enabled by the adaptability and plasticity of their transporters. Advances in our understanding of these systems, driven by functional genomics research, are rapidly filling the gap in knowledge about plant membrane transport involved in these plant–microbe interactions. In this review, we synthesize recent findings associated with different stages of these symbioses, from the pre-symbiotic stage to nutrient exchange, and describe the role of host transport systems in both mycorrhizal and legume–rhizobia symbioses.

The membrane transport system functions in establishing and maintaining arbuscular mycorrhiza and legume–rhizobium symbioses.     

MycoRed: Betalain pigments enable in vivo real-time visualisation of arbuscular mycorrhizal colonisation

Arbuscular mycorrhiza (AM) are mutualistic interactions formed between soil fungi and plant roots. AM symbiosis is a fundamental and widespread trait in plants with the potential to sustainably enhance future crop yields. However, improving AM fungal association in crop species requires a fundamental understanding of host colonisation dynamics across varying agronomic and ecological contexts. To this end, we demonstrate the use of betalain pigments as in vivo visual markers for the occurrence and distribution of AM fungal colonisation by Rhizophagus irregularis in Medicago truncatula and Nicotiana benthamiana roots. Using established and novel AM-responsive promoters, we assembled multigene reporter constructs that enable the AM-controlled expression of the core betalain synthesis genes. We show that betalain colouration is specifically induced in root tissues and cells where fungal colonisation has occurred. In a rhizotron setup, we also demonstrate that betalain staining allows for the noninvasive tracing of fungal colonisation along the root system over time. We present MycoRed, a useful innovative method that will expand and complement currently used fungal visualisation techniques to advance knowledge in the field of AM symbiosis.

Arbuscular mycorrhiza are mutualistic interactions formed between soil fungi and plant roots. This study presents the MycoRed system, which uses red plant pigments derived from beetroot to reveal how fungi establish symbiosis with living legume and wild tobacco roots.     

Quantification of symbiotic contributions to lower termite lignocellulose digestion using antimicrobial treatments

Animal-microbe co-evolution and symbiosis are broadly distributed across the animal kingdom. Insects form a myriad of associations with microbes ranging from vectoring of pathogens to intracellular, mutualistic relationships. Lower termites are key models for insect-microbe symbiosis because of the diversity, complexity and functionality of their unique tripartite symbiosis. This collaboration allows termites to live on a diet of nitrogen-poor lignocellulose. Recent functional investigations of lignocellulose digestion in lower termites have primarily focused on the contributions of the eukaryotic members of the termite holobiont (termite and protist). Here, using multiple antimicrobial treatments, we induced differing degrees of dysbiosis in the termite gut, leading to variably altered symbiont abundance and diversity, and lignocellulolytic capacity. Although protists are clearly affected by antimicrobial treatments, our findings provide novel evidence that the removal of distinct groups of bacteria partially reduces, but does not abolish, the saccharolytic potential of the termite gut holobiont. This is specifically manifested by reductions of 23–47% and 30–52% in glucose and xylose yields respectively from complex lignocellulose. Thus, all members of the lower termite holobiont (termite, protist and prokaryotes) are involved in the process of efficient, sustained lignocellulase activity. This unprecedented quantification of the relative importance of prokaryotes in this system emphasizes the collaborative nature of the termite holobiont, and the relevance of lower termites as models for inter-domain symbioses.     

Can the tight co-speciation between reed beetles (Col., Chrysomelidae,Donaciinae) and their bacterial endosymbionts,which provide cocoon material,clarify the deeper phylogeny of the hosts?

In most mutualistic symbioses of insects and intracellular bacteria, the endosymbionts provide additional nutrients to a host that feeds on an unbalanced diet. A strictly vertical transmission leads to co-speciation between the two partners. We have investigated an insect-bacteria relationship with a non-nutritional basis. The reed beetles (Donaciinae) harbor bacteria that produce a secretion used by the larvae for building a cocoon for pupation in mud underwater. The 16S rRNA of the bacteria and the cytochrome c oxidase I and elongation factor 1alpha of the beetles have been partially sequenced. The bacterial and the host phylogeny were highly congruent. Larger taxonomic units (genera) and host species groups/pairs have been recovered in the bacterial phylogeny. The symbiont data still cannot clarify the hitherto unresolved deeper phylogeny of the hosts, which is interpreted as a sign of rapid adaptive radiation of the reed beetles soon after their origin. The rate of sequence evolution among/within host species is discussed.     

Preference,specificity and cheating in the arbuscular mycorrhizal symbiosis

Arbuscular mycorrhizal symbioses are mutualistic interactions between fungi and most plants. There is considerable interest in this symbiosis because of the strong nutritional benefits conferred to plants and its influence on plant diversity. Until recently, the symbiosis was assumed to be unspecific. However, two studies have now revealed that although it can be largely unspecific with the fungal community composition changing seasonally, in certain ecosystems it can also be highly specific and might potentially allow plants to cheat the arbuscular mycorrhizal network that connects plants below ground.     

Phylogenetic analysis of local-scale tree soil associations in a lowland moist tropical forest

Background

Local plant-soil associations are commonly studied at the species-level, while associations at the level of nodes within a phylogeny have been less well explored. Understanding associations within a phylogenetic context, however, can improve our ability to make predictions across systems and can advance our understanding of the role of evolutionary history in structuring communities.

Methodology/Principal Findings

Here we quantified evolutionary signal in plant-soil associations using a DNA sequence-based community phylogeny and several soil variables (e.g., extractable phosphorus, aluminum and manganese, pH, and slope as a proxy for soil water). We used published plant distributional data from the 50-ha plot on Barro Colorado Island (BCI), Republic of Panamá. Our results suggest some groups of closely related species do share similar soil associations. Most notably, the node shared by Myrtaceae and Vochysiaceae was associated with high levels of aluminum, a potentially toxic element. The node shared by Apocynaceae was associated with high extractable phosphorus, a nutrient that could be limiting on a taxon specific level. The node shared by the large group of Laurales and Magnoliales was associated with both low extractable phosphorus and with steeper slope. Despite significant node-specific associations, this study detected little to no phylogeny-wide signal. We consider the majority of the ‘traits’ (i.e., soil variables) evaluated to fall within the category of ecological traits. We suggest that, given this category of traits, phylogeny-wide signal might not be expected while node-specific signals can still indicate phylogenetic structure with respect to the variable of interest.

Conclusions

Within the BCI forest dynamics plot, distributions of some plant taxa are associated with local-scale differences in soil variables when evaluated at individual nodes within the phylogenetic tree, but they are not detectable by phylogeny-wide signal. Trends highlighted in this analysis suggest how plant-soil associations may drive plant distributions and diversity at the local-scale.     

The Roles of Auxins and Cytokinins in Mycorrhizal Symbioses

Abstract Most land plant species that have been examined exist naturally with a higher fungus living in and around their roots in a symbiotic partnership called a mycorrhiza. Several types of mycorrhizal symbiosis exist, defined by the host/partner combination and the morphology of the symbiotic structures. The arbuscular mycorrhiza (AM) is ancient and may have co-evolved with land plants. Emerging results from gene expression studies have suggested that subsets of AM genes were co-opted during the evolution of other biotrophic symbioses. Here we compare the roles of phytohormones in AM symbiosis and ectomycorrhizas (EC), a more recent symbiosis. To date, there is little evidence of physiologic overlap between the two symbioses with respect to phytohormone involvement. Research on AM has shown that cytokinin (CK) accumulation is specifically enhanced by symbiosis throughout the plant. We propose a pathway of events linking enhanced CK to development of the AM. Additional and proposed involvement of other phytohormones are also described. The role of auxin in EC symbiosis and recent research advances on the topic are reviewed. We have reflected the literature bias in reporting individual growth regulator effects. However, we consider that gradients and ratios of these molecules are more likely to be the causal agents of morphologic changes resulting from fungal associations. We expect that once the individual roles of these compounds are explained, the subtleties of their function will be more clearly addressed.     

The diversity of reproductive parasites among arthropods: <Emphasis Type="Italic">Wolbachia</Emphasis>do not walk alone

Background  

Inherited bacteria have come to be recognised as important components of arthropod biology. In addition to mutualistic symbioses, a range of other inherited bacteria are known to act either as reproductive parasites or as secondary symbionts. Whilst the incidence of the α-proteobacterium Wolbachia is relatively well established, the current knowledge of other inherited bacteria is much weaker. Here, we tested 136 arthropod species for a range of inherited bacteria known to demonstrate reproductive parasitism, sampling each species more intensively than in past surveys.