Comparative Genomics Suggests That an Ancestral Polyploidy Event Leads to Enhanced Root Nodule Symbiosis in the Papilionoideae

Qi-Gang Li, Li Zhang, Chun Li, Jim M. Dunwell, Yuan-Ming Zhang
2013 Molecular biology and evolution  
Comparative genomics suggests that an ancestral polyploidy event leads to enhanced root nodule symbiosis in the Papilionoideae. Molecular Biology and Evolution, 30 (12). pp. 26022611. ISSN 15371719 doi: Available at Abstract Root nodule symbiosis (RNS) is one of the most efficient biological systems for nitrogen fixation and it occurs in 90% of genera in the Papilionoideae, the largest subfamily of legumes. Most papilionoid species show evidence of a
more » ... idy event occurred approximately 58 million years ago. Although polyploidy is considered to be an important evolutionary force in plants, the role of this papilionoid polyploidy event, especially its association with RNS, is not understood. In this study, we explored this role using an integrated comparative genomic approach and conducted gene expression comparisons and gene ontology enrichment analyses. The results show the following: (1) approximately a quarter of the papilionoid-polyploidy-derived duplicate genes are retained; (2) there is a striking divergence in the level of expression of gene duplicate pairs derived from the polyploidy event; and (3) the retained duplicates are frequently involved in the processes crucial for RNS establishment, such as symbiotic signalling, nodule organogenesis, rhizobial infection and nutrient exchange and transport. Thus, we conclude that the papilionoid polyploidy event might have further refined RNS and induced a more robust and enhanced symbiotic system. This conclusion partly explains the widespread occurrence of the Papilionoideae. Downloaded from 4 applied a phylogenetic strategy to scan the genes in the cytokinin phosphorelay pathway and found that two papilionoid-WGD-derived type-A cytokinin response regulators, MtRR9 and MtRR11, in M. truncatula are recruited during nodulation. In addition, Young et al. (2011) indicated that the papilionoid polyploidy event might have facilitated the emergence of critical components of Nod factor signalling and contributed to the complexity of rhizobial nodulation found in the Papilionoideae. Although these previous studies have suggested the important roles of this polyploidy event, most of them are based on studies of single genes, pathways or genomes, and very little insight has been gained from genome-wide and cross-species comparative studies. Recently, the increasing number of completely sequenced legume and non-legume genomes has provided a rich opportunity for a comparative genomics study. The first step for a comparative genomics analysis of the papilionoid WGD event is to identify gene duplicates derived from this event. Currently, there are two widely used approaches for comparative genomics studies: a synteny-based method and a phylogenetic approach (Dehal and Boore 2005; Thomas et al. 2006; Vilella et al. 2009; Young et al. 2011; Wang et al. 2012; Li and Zhang 2013). Of these two methods, the synteny method can give a view of genome structure variation, and the phylogenetic approach provides not only a group of homologies but also their phylogenetic relationships. However, the identification of interesting lineages in the phylogenetic approach can be affected by incorrect topologies in the structure of gene trees. Therefore, it would be beneficial to integrate the two aforementioned approaches. In this study, we utilized an integrated comparative genomics approach using the completely sequenced genomes of four papilionoid species and two non-legume species to identify the papilionoid WGD-derived gene lineages. We also investigated the retention patterns of these lineages. Gene expression comparison and GO enrichment analysis were conducted to identify the papilionoid WGD-enhanced biological processes and/or pathways likely associated with the evolution of RNS in Papilionoideae. Based on these results, we were able to infer the potential roles of the papilionoid polyploidy event in the evolution of RNS.
doi:10.1093/molbev/mst152 pmid:24008584 fatcat:svgkasvdffezretdc335x5w3ci