Factors Influencing Gene Family Size Variation Among Related Species in a Plant Family, Solanaceae

Abstract

Gene duplication and loss contribute to gene content differences as well as phenotypic divergence across species. However, the extent to which gene content varies among closely related plant species and the factors responsible for such variation remain unclear. Here, using the Solanaceae family as a model and Pfam domain families as a proxy for gene families, we investigated variation in gene family sizes across species and the likely factors contributing to the variation. We found that genes in highly variable families have high turnover rates and tend to be involved in processes that have diverged between Solanaceae species, whereas genes in low-variability families tend to have housekeeping roles. In addition, genes in high- and low-variability gene families tend to be duplicated by tandem and whole genome duplication, respectively. This finding together with the observation that genes duplicated by different mechanisms experience different selection pressures suggest that duplication mechanism impacts gene family turnover. We explored using pseudogene number as a proxy for gene loss but discovered that a substantial number of pseudogenes are actually products of pseudogene duplication, contrary to the expectation that most plant pseudogenes are remnants of once-functional duplicates. Our findings reveal complex relationships between variation in gene family size, gene functions, duplication mechanism, and evolutionary rate. The patterns of lineage-specific gene family expansion within the Solanaceae provide the foundation for a better understanding of the genetic basis underlying phenotypic diversity in this economically important family.

Evolution of a plant gene cluster in Solanaceae and emergence of metabolic diversity

“…To hypothesize the evolutionary history of genes in the acylsugar gene cluster, putative pseudogenes, which are homologs to protein-coding genes but with predicted premature stops/frameshifts and/or protein sequence truncation, were also identified for each species as described ( Wang et al, 2018 ). Protein sequences from Arabidopsis thaliana , Oryza sativa , and S. lycopersicum were used as queries in the searches against the genomic regions of target species using TBLASTN ( Altschul et al, 1990 ).…”

“…Genome-wide syntenic analysis was conducted using annotated protein-coding genes and putative pseudogenes from all the species with MCScanX-transposed (Wang et al, 2013) as described (Wang et al, 2018). The MCScanX-based analysis did not lead to a syntenic block of acylsugar gene cluster on chromosome 7 of S. melongena r2.5.1, which can be due to true absence, issues with genome assembly, or lack of coverage.…”

Genome-wide identification and expression analysis of AP2/ERF transcription factors in sugarcane (Saccharum spontaneum L.)

“…Multiple studies indicated that gene families evolved due to genome-wide duplication, segmental duplication or tandem duplication, and gene diversification occurred after these duplication events [32]. To explore SsAP2/ ERF genes evolution, we studied tandem and segmental duplication events of these genes using chromosomal information for S. spontaneum (Additional file 8).…”

Mechanistic insights into the evolution of DUF26-containing proteins in land plants

“…The young gene families initially expand through tandem duplications and therefore experience more relaxed selection 63 . This is supported by the fact that the tandem genes function in processes that require fast responses such as adaptation to environment, pathogen responses and secondary metabolism 2,64 , and that these gene families show high variation across species and have high kn/ks rates 5 . In tandems, main evolutionary forces are unequal crossover and concerted evolution through gene conversion, but over time the genes evolve into their specific functions.…”

“…The prevailing explanation for the phenomenon is dosage balance; in complex regulatory networks and protein complexes the stoichiometric balance between the different components needs to be preserved, and therefore selection acts against losses after WGMs and against duplications in SSDs 4 . In terms of sizes, the families retained after WGMs are stable across different species whereas highly variable families evolve through SSDs 5 , suggesting high turnover rates. However, these results have been obtained by analyzing the two extremes, the top families displaying pure WGM retention or SSD characteristics 3 while most of the gene families likely evolve in an intermediate manner.…”