Polyploid plants obtain greater fitness benefits from a nutrient acquisition mutualism.

Polyploidy is a key driver of ecological and evolutionary processes in plants, yet little is known about its effects on biotic interactions. This gap in knowledge is especially profound for nutrient acquisition mutualisms, despite the fact that they regulate global nutrient cycles and structure ecosystems. Generalism in mutualistic interactions depends on the range of potential partners (niche breadth), the benefits obtained and ability to maintain benefits across a variety of partners (fitness plasticity). Here, we determine how each of these is influenced by polyploidy in the legume-rhizobium mutualism. We inoculated a broad geographic sample of natural diploid and autotetraploid alfalfa (Medicago sativa) lineages with a diverse panel of Sinorhizobium bacterial symbionts. To analyze the extent and mechanism of generalism, we measured host growth benefits and functional traits. Autotetraploid plants obtained greater fitness enhancement from mutualistic interactions and were better able to maintain this across diverse rhizobial partners (i.e. low plasticity in fitness) relative to diploids. These benefits were not attributed to increases in niche breadth, but instead reflect increased rewards from investment in the mutualism. Polyploid plants displayed greater generalization in bacterial mutualisms relative to diploids, illustrating another axis of advantage for polyploids over diploids.

Autopolyploidy alters nodule-level interactions in the legume-rhizobium mutualism.

PREMISE: Polyploidy is a major genetic driver of ecological and evolutionary processes in plants, yet its effects on plant interactions with mutualistic microbes remain unresolved. The legume-rhizobium symbiosis regulates global nutrient cycles and plays a role in the diversification of legume species. In this mutualism, rhizobia bacteria fix nitrogen in exchange for carbon provided by legume hosts. This exchange occurs inside root nodules, which house bacterial cells and represent the interface of legume-rhizobium interactions. Although polyploidy may directly impact the legume-rhizobium mutualism, no studies have explored how it alters the internal structure of nodules. METHODS: We created synthetic autotetraploids using Medicago sativa subsp. caerulea. Neotetraploid plants and their diploid progenitors were singly inoculated with two strains of rhizobia, Sinorhizobium meliloti and S. medicae. Confocal microscopy was used to quantify internal traits of nodules produced by diploid and neotetraploid plants. RESULTS: Autotetraploid plants produced larger nodules with larger nitrogen fixation zones than diploids for both strains of rhizobia, although the significance of these differences was limited by power. Neotetraploid M. sativa subsp. caerulea plants also produced symbiosomes that were significantly larger, nearly twice the size, than those present in diploids. CONCLUSIONS: This study sheds light on how polyploidy directly affects a plant-bacterium mutualism and uncovers novel mechanisms. Changes in plant-microbe interactions that directly result from polyploidy likely contribute to the increased ability of polyploid legumes to establish in diverse environments.

Gazing into the anthosphere: considering how microbes influence floral evolution.

The flower is the hallmark of angiosperms and its evolution is key to their diversification. As knowledge of ecological interactions between flowers and their microbial communities (the anthosphere) expands, it becomes increasingly important to consider the evolutionary impacts of these associations and their potential eco-evolutionary dynamics. In this Viewpoint we synthesize current knowledge of the anthosphere within a multilevel selection framework and illustrate the potential for the extended floral phenotype (the phenotype expressed from the genes of the plant and its associated flower microbes) to evolve. We argue that flower microbes are an important, but understudied, axis of variation that shape floral trait evolution and angiosperm reproductive ecology. We highlight knowledge gaps and discuss approaches that are critical for gaining a deeper understanding of the role microbes play in mediating plant reproduction, ecology, and evolution.

The direct effects of plant polyploidy on the legume-rhizobia mutualism.

Background: Polyploidy is known to significantly alter plant genomes, phenotypes and interactions with the abiotic environment, yet the impacts of polyploidy on plant-biotic interactions are less well known. A particularly important plant-biotic interaction is the legume-rhizobia mutualism, in which rhizobia fix atmospheric nitrogen in exchange for carbon provided by legume hosts. This mutualism regulates nutrient cycles in natural ecosystems and provides nitrogen to agricultural environments. Despite the ecological, evolutionary and agricultural importance of plant polyploidy and the legume-rhizobia mutualism, it is not yet fully understood whether plant polyploidy directly alters mutualism traits or the consequences on plant growth. Scope: The aim was to propose a conceptual framework to understand how polyploidy might directly enhance the quantity and quality of rhizobial symbionts hosted by legume plants, resulting in increased host access to fixed nitrogen (N). Mechanistic hypotheses have been devised to examine how polyploidy can directly alter traits that impact the quantity (e.g. nodule number, nodule size, terminal bacteroid differentiation) and quality of symbionts (e.g. nodule environment, partner choice, host sanctions). To evaluate these hypotheses, an exhaustive review of studies testing the effects of plant polyploidy on the mutualism was conducted. In doing so, overall trends were synthesized, highlighting the limited understanding of the mechanisms that underlie variation in results achieved thus far, revealing striking gaps in knowledge and uncovering areas ripe for future research. Conclusions: Plant polyploidy can immediately alter nodule size, N fixation rate and the identity of rhizobial symbionts hosted by polyploid legumes, but many of the mechanistic hypotheses proposed here, such as bacteroid number and enhancements of the nodule environment, remain unexplored. Although current evidence supports a role of plant polyploidy in enhancing key aspects of the legume-rhizobia mutualism, the underlying mechanisms and effects on host benefit from the mutualism remain unresolved.

Effect of the anther-smut fungus Microbotryum on the juvenile growth of its host Silene latifolia.

PREMISE OF THE STUDY: Plant pathogens that form persistent systemic infections within plants have the potential to affect multiple plant life history traits, yet we tend to focus only on visible symptoms. Anther smut of Silene latifolia caused by the fungus Microbotryum lychnidis-dioicae induces the anthers of its host to support fungal spore production instead of pollen, and the pathogen is primarily transmitted among flowering plants by pollinators. Nevertheless, most of its life cycle is spent in the asymptomatic vegetative phase, and spores falling on seedlings or nonflowering plants can also infect the host. The purpose of this study was to ask whether the fungus also had an effect on its host plant in the juvenile vegetative phase before flowering as this is important for the disease dynamics in species where infection of seedlings is commonplace. METHODS: Leaf length and leaf number of inoculated and uninoculated juvenile plants were compared in greenhouse experiments, and in one experiment, disease status of the plants at flowering was determined. KEY RESULTS: Inoculated plants had shorter but more leaves, and reduced root mass at the early juvenile (preflowering) stage. Some of these effects were detectable in plants that were inoculated but showed no disease symptoms at flowering. CONCLUSIONS: These results show that pathogenic fungi can have endophyte-like effects even in the total absence of their typical and more charismatic symptoms, and conversely that the assessment of endophyte effects on the fitness of their hosts should include all stages of the host life cycle.

A recurring syndrome of accelerated plastid genome evolution in the angiosperm tribe Sileneae (Caryophyllaceae).

In flowering plants, plastid genomes are generally conserved, exhibiting slower rates of sequence evolution than the nucleus and little or no change in structural organization. However, accelerated plastid genome evolution has occurred in scattered angiosperm lineages. For example, some species within the genus Silene have experienced a suite of recent changes to their plastid genomes, including inversions, shifts in inverted repeat boundaries, large indels, intron losses, and rapid rates of amino acid sequence evolution in a subset of protein genes, with the most extreme divergence occurring in the protease gene clpP. To investigate the relationship between the rates of sequence and structural evolution, we sequenced complete plastid genomes from three species (Silene conoidea, S. paradoxa, and Lychnis chalcedonica), representing independent lineages within the tribe Sileneae that were previously shown to have accelerated rates of clpP evolution. We found a high degree of parallel evolution. Elevated rates of amino acid substitution have occurred repeatedly in the same subset of plastid genes and have been accompanied by a recurring pattern of structural change, including cases of identical inversions and intron loss. This "syndrome" of changes was not observed in the closely related outgroup Agrostemma githago or in the more slowly evolving Silene species that were sequenced previously. Although no single mechanism has yet been identified to explain the correlated suite of changes in plastid genome sequence and structure that has occurred repeatedly in angiosperm evolution, we discuss a possible mixture of adaptive and non-adaptive forces that may be responsible.