Epichloë endophytes are fungal symbionts of grasses that span a continuum including asexual mutualists that are vertically transmitted, obligately sexual pathogens that are horizontally transmitted, and mixed-strategy symbionts with both mutualistic and pathogenic capabilities. Here we show that processes of genome evolution differ markedly for the different symbiont types. Genetic and phylogenetic analysis was conducted of a broad taxonomic, ecological and geographical sample of sexual and asexual isolates, in which were identified and sequenced alleles of genes for beta-tubulin (tub2) and translation elongation factor 1-alpha (tef1), and microsatellite alleles were identified by length polymorphisms. The majority of asexual isolates had two or three alleles of most loci, but every sexual isolate had only single alleles for each locus. Phylogenetic analysis of tub2 and tef1 indicated that in all instances of multiple alleles in an isolate, the alleles were derived from different sexual species. It is concluded that, whereas horizontally transmissible species had haploid genomes and speciation occurred cladistically, most of the strictly seedborne mutualists were interspecific hybrids with heteroploid (aneuploid or polyploid) genomes. Furthermore, the phylogenetic evidence indicated that, in at least some instances, hybridization followed rather than caused evolution of the strictly seedborne habit. Therefore, the abundance of hybrid species among grass endophytes, and their prevalence in many host populations suggests a selective advantage of hybridization for the mutualistic endophytes.
Fungi (kingdom Mycota) and oomycetes (kingdom Stramenopila, phylum Oomycota) are crucially important in the nutrient cycles of the world. Their interactions with plants sometimes benefit and sometimes act to the detriment of humans. Many fungi establish ecologically vital mutualisms, such as in mycorrhizal fungi that enhance nutrient acquisition, and endophytes that combat insects and other herbivores. Other fungi and many oomycetes are plant pathogens that devastate natural and agricultural populations of plant species. Studies of fungal and oomycete evolution were extraordinarily difficult until the advent of molecular phylogenetics. Over the past decade, researchers applying these new tools to fungi and oomycetes have made astounding new discoveries, among which is the potential for interspecific hybridization. Consequences of hybridization among pathogens include adaptation to new niches such as new host species, and increased or decreased virulence. Hybrid mutualists may also be better adapted to new hosts and can provide greater or more diverse benefits to host plants.
Epichloe species are fungal symbionts (endophytes) of grasses, many of which are benign or mutual islic and have a balance of horizontal (contagious) and vertical (seed-borne) transmission, whereas others mainly transmit horizontally and are more antagonistic. Over the past eight years several Epichloe species have been describe! based largely on the biological species concept. We conducted a multi-gene phylogenetic analysis to evaluate these endophytes as phylogenet.c species, and thereby assess the relationship of phylogenetic and biological species. Variation mainly in nitrons of genes encoding ^-tubulin (tub2), translation elongation factor 1-a («e/7), and actin (act I) provided robust phylogenet.c signal distinguishing the described Epichloe species. Outgroup rooting split the genus into two major groups. One group included most species with balanced transmission strategy, and in this group the phylogenetic ami biological spec.es concepts corresponded well. In contrast, these species concepts poorly corresponded for the other group the Epichloe typhina complex, with predominantly antagonistic, horizontally transmitted endophytes. We suggest that the balance of vertical and horizontal transmission may promote ecological (host) specialization and subsequent genetic isolation as mechanisms promoting speciation; whereas strict horizontal transmission may select for broader host ranges, slow the development of genetically isolated species, and thereby increase lineage sorting effects that cause conflicts between phylogenetic and biological species.
Significant phylogenetic codivergence between plant or animal hosts (H) and their symbionts or parasites (P) indicates the importance of their interactions on evolutionary time scales. However, valid and realistic methods to test for codivergence are not fully developed. One of the systems where possible codivergence has been of interest involves the large subfamily of temperate grasses (Pooideae) and their endophytic fungi (epichloae). These widespread symbioses often help protect host plants from herbivory and stresses and affect species diversity and food web structures. Here we introduce the MRCALink (most-recent-common-ancestor link) method and use it to investigate the possibility of grass-epichloë codivergence. MRCALink applied to ultrametric H and P trees identifies all corresponding nodes for pairwise comparisons of MRCA ages. The result is compared to the space of random H and P tree pairs estimated by a Monte Carlo method. Compared to tree reconciliation, the method is less dependent on tree topologies (which often can be misleading), and it crucially improves on phylogeny-independent methods such as ParaFit or the Mantel test by eliminating an extreme (but previously unrecognized) distortion of node-pair sampling. Analysis of 26 grass species-epichloë species symbioses did not reject random association of H and P MRCA ages. However, when five obvious host jumps were removed, the analysis significantly rejected random association and supported grass-endophyte codivergence. Interestingly, early cladogenesis events in the Pooideae corresponded to early cladogenesis events in epichloae, suggesting concomitant origins of this grass subfamily and its remarkable group of symbionts. We also applied our method to the well-known gopher-louse data set.
This study was conducted to explore fungal endophyte communities inhabiting native switchgrass plants from the tallgrass prairie of northern Oklahoma. The primary focus was to isolate these endophytes in pure culture from surface-sterilized plant tissues and provide taxonomic identifications based on comparative analysis of ITS rDNA gene sequences. From these data, we evaluated the biodiversity of these potentially beneficial endosymbionts from this rapidly disappearing habitat of the Great Plains. While important from a strictly conservationist standpoint, this survey further allowed us to identify candidate endophytes for introduction into commercial switchgrass cultivars for biomass enhancement. A total of 210 whole plant samples were collected at early vegetative, full reproductive and senescence stages. Fungal endophytes were isolated, identified to species level when possible, and grouped into communities based on plant part, collection month and part of the prairie from which the plants were collected. Species diversity for each community was estimated by Shannon diversity index, and differences in diversity indices were compared using a t-test. The presence of fungal species representing at least 18 taxonomic orders suggests a high level of diversity in switchgrass endophyte communities. The fungal communities from shoot tissue had significantly higher species diversity than communities from the root tissue. The abundance of taxa assigned to the order Hypocreales (to which mutualistic, clavicipitaceous endophytes of coolseason grasses belong) found in shoot (64%) and root tissues (39%) throughout the growing season suggests great potential for utilizing these endophytes for enhancing biomass production and stress resistance of this important bioenergy crop.
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