Comparative Analysis of Syntenic Genes in Grass Genomes Reveals Accelerated Rates of Gene Structure and Coding Sequence Evolution in Polyploid Wheat

Eduard D Akhunov,Yaqin Ma,Gaganpreet Kaur,Bikram S Gill,Sunish Sehgal,Hanquan Liang,Mingcheng Luo,Alina R Akhunova,Shichen Wang,Matthew J Hayden,Jaroslav Doležel,Kerrie L Forrest,Justin D Faris,Wanlong Li,Deven See,Hana Šimková

doi:10.1104/pp.112.205161

Abstract

Cycles of whole-genome duplication (WGD) and diploidization are hallmarks of eukaryotic genome evolution and speciation. Polyploid wheat (Triticum aestivum) has had a massive increase in genome size largely due to recent WGDs. How these processes may impact the dynamics of gene evolution was studied by comparing the patterns of gene structure changes, alternative splicing (AS), and codon substitution rates among wheat and model grass genomes. In orthologous gene sets, significantly more acquired and lost exonic sequences were detected in wheat than in model grasses. In wheat, 35% of these gene structure rearrangements resulted in frame-shift mutations and premature termination codons. An increased codon mutation rate in the wheat lineage compared with Brachypodium distachyon was found for 17% of orthologs. The discovery of premature termination codons in 38% of expressed genes was consistent with ongoing pseudogenization of the wheat genome. The rates of AS within the individual wheat subgenomes (21%-25%) were similar to diploid plants. However, we uncovered a high level of AS pattern divergence between the duplicated homeologous copies of genes. Our results are consistent with the accelerated accumulation of AS isoforms, nonsynonymous mutations, and gene structure rearrangements in the wheat lineage, likely due to genetic redundancy created by WGDs. Whereas these processes mostly contribute to the degeneration of a duplicated genome and its diploidization, they have the potential to facilitate the origin of new functional variations, which, upon selection in the evolutionary lineage, may play an important role in the origin of novel traits.

Highlights

Cycles of whole-genome duplication (WGD) and diploidization are hallmarks of eukaryotic genome evolution and speciation
The remaining 32% of reads were not included in the assembly due to having only partial overlap with contigs (588 Mb), absence of overlap with any other reads (335 Mb), high copy number (715 Mb), and/or artifacts such as chimeric sequences (842 Mb)
Using paired-end sequence reads, nearly 60% (195 Mb) of large contigs (LC) were assembled into 38,036 scaffolds with an N50 size of 6,013 bp (Table I) and a total gap length of 17 Mb

Summary

Introduction

Cycles of whole-genome duplication (WGD) and diploidization are hallmarks of eukaryotic genome evolution and speciation. Comparative analysis of model grass genomes (International Rice Genome Sequencing Project, 2005; Paterson et al, 2009; Schnable et al, 2009; International Brachypodium Initiative, 2010) revealed a more detailed picture of wheat genome structure evolution involving segmental duplications, chromosome inversions, translocations, and small-scale structural rearrangements (Akhunov et al, 2003; Gu et al, 2004, 2006; Salse et al, 2008; Choulet et al, 2010; Devos, 2010; Mayer et al, 2011; Wicker et al., 2011). Only a limited number of genes have been characterized for AS events (Båga et al, 1999; Terashima and Takumi, 2009), and the impact of WGD on AS patterns on a genome-wide scale remains unknown

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