Deep Homology and Evolutionary Tinkering in the Origins of Nodulation

[摘要] Nodulation is the mutualistic symbiosis in which plants house nitrogen-fixing bacteria in specialized root nodule organs, and exchange plant photosynthate for bacteria fixed nitrogen. This symbiosis occurs only in the Nitrogen-Fixing Clade (NFC) of rosids – the Fagales, Fabales, Cucurbitales and Rosales. Within the NFC, nodulation evolved multiple times independently, and different nodulating lineages show substantial differences in nodule morphology and development, as well as bacterial symbiont and infection mechanism. Despite the apparent nonhomology of nodulation, each examined instance of its evolution involved the recruitment of the same homologous genes, meaning that nodulation is deeply homologous. The nodulation pathway evolved by the recruitment of genes from a variety of pathways, in an example of evolutionary tinkering. This dissertation examines the precise pattern of gene recruitment that created nodules in different lineages, with a focus on the subtilase gene family. A phylogenetic analysis of the subtilase gene family reveals that the subtilase ortholog recruited for nodulation in the legumes is paralogous to the one recruited in the Fagales, and that these two lineages diverged before the origin of the NFC. A synteny analysis of symbiotic subtilases in the legumes shows that a lineage of subtilases mediating arbuscular mycorrhization originated by whole genome duplication, followed by lineage-specific tandem duplication. A transcriptomic study of nodulation in Elaeagnus umbellata, a nodulating actinorhizal shrub in the Elaeagnaceae for which the genetic basis of nodulation is poorly understood, assembled 13 genes homologous with those involved in nodulation in other lineages, showing deep homology. 12 of these 13 genes were orthologous, showing congruence with the species tree in phylogenetic analysis, but our assembled E. umbellata subtilase was paralogous with those mediating nodulation in the actinorhizal Fagales and orthologous with those mediating nodulation in rhizobial legumes. In showing differential recruitment of subtilases in the independent origins of nodulation, this dissertation provides further evidence of the nonhomology of nodulation, and presents nodulation as a fertile system to examine the ortholog conjecture, deep homology, and evolutionary tinkering in the origin of a complex and important symbiotic organ.

[发布机构] University of Michigan

[效力级别] Actinorhiza

[关键词] Deep Homology;Actinorhiza;Nodulation;Elaeagnus umbellata;Subtilase;Ecology and Evolutionary Biology;Science;Ecology and Evolutionary Biology