Background

Specialized interactions help structure communities, but persistence of specialized organisms is puzzling because a generalist can occupy more environments and partake in more beneficial interactions. The "Jack-of-all-trades is a master of none" hypothesis asserts that specialists persist because the fitness of a generalist utilizing a particular habitat is lower than that of a specialist adapted to that habitat. Yet, there are many reasons to expect that mutualists will generalize on partners.Plant-soil feedbacks help to structure plant and microbial communities, but how frequently are soil-based symbiotic mutualistic interactions sufficiently specialized to influence species distributions and community composition? To address this question, we quantified realized partner richness and phylogenetic breadth of four wild-grown native legumes (Lupinus bicolor, L. arboreus, Acmispon strigosus and A. heermannii) and performed inoculation trials to test the ability of two hosts (L. bicolor and A. strigosus) to nodulate (fundamental partner richness), benefit from (response specificity), and provide benefit to (effect specificity) 31 Bradyrhizobium genotypes.

Results

In the wild, each Lupinus species hosted a broader genetic range of Bradyrhizobium than did either Acmispon species, suggesting that Acmispon species are more specialized. In the greenhouse, however, L. bicolor and A. strigosus did not differ in fundamental association specificity: all inoculated genotypes nodulated both hosts. Nevertheless, A. strigosus exhibited more specificity, i.e., greater variation in its response to, and effect on, Bradyrhizobium genotypes. Lupinus bicolor benefited from a broader range of genotypes but averaged less benefit from each. Both hosts obtained more fitness benefit from symbionts isolated from conspecific hosts; those symbionts in turn gained greater fitness benefit from hosts of the same species from which they were isolated.

Conclusions

This study affirmed two important tenets of evolutionary theory. First, as predicted by the Jack-of-all-trades is a master of none hypothesis, specialist A. strigosus obtained greater benefit from its beneficial symbionts than did generalist L. bicolor. Second, as predicted by coevolutionary theory, each test species performed better with partner genotypes isolated from conspecifics. Finally, positive fitness feedback between the tested hosts and symbionts suggests that positive plant-soil feedback could contribute to their patchy distributions in this system.

α-Gliadins are a major group of gluten proteins in wheat flour that contribute to the end-use properties for food processing and contain major immunogenic epitopes that can cause serious health-related issues including celiac disease (CD). α-Gliadins are also the youngest group of gluten proteins and are encoded by a large gene family. The majority of the gene family members evolved independently in the A, B, and D genomes of different wheat species after their separation from a common ancestral species. To gain insights into the origin and evolution of these complex genes, the genomic regions of the Gli-2 loci encoding α-gliadins were characterized from the tetraploid wild emmer, a progenitor of hexaploid bread wheat that contributed the AABB genomes. Genomic sequences of Gli-2 locus regions for the wild emmer A and B genomes were first reconstructed using the genome sequence scaffolds along with optical genome maps. A total of 24 and 16 α-gliadin genes were identified for the A and B genome regions, respectively. α-Gliadin pseudogene frequencies of 86% for the A genome and 69% for the B genome were primarily caused by C to T substitutions in the highly abundant glutamine codons, resulting in the generation of premature stop codons. Comparison with the homologous regions from the hexaploid wheat cv. Chinese Spring indicated considerable sequence divergence of the two A genomes at the genomic level. In comparison, conserved regions between the two B genomes were identified that included α-gliadin pseudogenes containing shared nested TE insertions. Analyses of the genomic organization and phylogenetic tree reconstruction indicate that although orthologous gene pairs derived from speciation were present, large portions of α-gliadin genes were likely derived from differential gene duplications or deletions after the separation of the homologous wheat genomes ~ 0.5 MYA. The higher number of full-length intact α-gliadin genes in hexaploid wheat than that in wild emmer suggests that human selection through domestication might have an impact on α-gliadin evolution. Our study provides insights into the rapid and dynamic evolution of genomic regions harboring the α-gliadin genes in wheat.

Wheat Gli-2 loci encode complex groups of α-gliadin prolamins that are important for breadmaking, but also major triggers of celiac disease (CD). Elucidation of α-gliadin evolution provides knowledge to produce wheat with better end-use properties and reduced immunogenic potential. The Gli-2 loci contain a large number of tandemly duplicated genes and highly repetitive DNA, making sequence assembly of their genomic regions challenging. Here, we constructed high-quality sequences spanning the three wheat homeologous α-gliadin loci by aligning PacBio-based sequence contigs with BioNano genome maps. A total of 47 α-gliadin genes were identified with only 26 encoding intact full-length protein products. Analyses of α-gliadin loci and phylogenetic tree reconstruction indicate significant duplications of α-gliadin genes in the last ~2.5 million years after the divergence of the A, B and D genomes, supporting its rapid lineage-independent expansion in different Triticeae genomes. We showed that dramatic divergence in expression of α-gliadin genes could not be attributed to sequence variations in the promoter regions. The study also provided insights into the evolution of CD epitopes and identified a single indel event in the hexaploid wheat D genome that likely resulted in the generation of the highly toxic 33-mer CD epitope.

Improving end-use quality and disease resistance are important goals in wheat breeding. The genetic loci controlling these traits are highly complex, consisting of large families of prolamin and resistance genes with members present in all three homeologous A, B, and D genomes in hexaploid bread wheat. Here, orthologous regions harboring both prolamin and resistance gene loci were reconstructed and compared to understand gene duplication and evolution in different wheat genomes. Comparison of the two orthologous D regions from the hexaploid wheat Chinese Spring and the diploid progenitor Aegilops tauschii revealed their considerable difference due to the presence of five large structural variations with sizes ranging from 100 kb to 2 Mb. As a result, 44% of the Ae. tauschii and 71% of the Chinese Spring sequences in the analyzed regions, including 79 genes, are not shared. Gene rearrangement events, including differential gene duplication and deletion in the A, B, and D regions, have resulted in considerable erosion of gene collinearity in the analyzed regions, suggesting rapid evolution of prolamin and resistance gene families after the separation of the three wheat genomes. We hypothesize that this fast evolution is attributed to the co-evolution of the two gene families dispersed within a high recombination region. The identification of a full set of prolamin genes facilitated transcriptome profiling and revealed that the A genome contributes the least to prolamin expression because of its smaller number of expressed intact genes and their low expression levels, while the B and D genomes contribute similarly.