Abstract
Retrotransposons are the most abundant group of transposable elements (TEs) in plants, providing an extraordinarily versatile source of genetic variation. Thlaspi arvense, a close relative of the model plant Arabidopsis thaliana with worldwide distribution, thrives from sea level to above 4,000 m elevation in the Qinghai-Tibet Plateau (QTP), China. Its strong adaptability renders it an ideal model system for studying plant adaptation in extreme environments. However, how the retrotransposons affect the T. arvense genome evolution and adaptation is largely unknown. We report a high-quality chromosome-scale genome assembly of T. arvense with a scaffold N50 of 59.10 Mb. Long terminal repeat retrotransposons (LTR-RTs) account for 56.94% of the genome assembly, and the Gypsy superfamily is the most abundant TEs. The amplification of LTR-RTs in the last six million years primarily contributed to the genome size expansion in T. arvense. We identified 351 retrogenes and 303 genes flanked by LTRs, respectively. A comparative analysis showed that orthogroups containing those retrogenes and genes flanked by LTRs have a higher percentage of significantly expanded orthogroups (SEOs), and these SEOs possess more recent tandem duplicated genes. All present results indicate that RNA-based gene duplication (retroduplication) accelerated the subsequent tandem duplication of homologous genes resulting in family expansions, and these expanded gene families were implicated in plant growth, development, and stress responses, which were one of the pivotal factors for T. arvense’s adaptation to the harsh environment in the QTP regions. In conclusion, the high-quality assembly of the T. arvense genome provides insights into the retroduplication mediated mechanism of plant adaptation to extreme environments.
Highlights
Thlaspi arvense is a member of the extended II lineage of Brassicaceae (Huang et al, 2016), which is closely related to Arabidopsis
The Benchmarking Universal Single-Copy Orthologs (BUSCO) analysis showed that 94.58% of 1,440 plant lineage single-copy orthologs were present in the T. arvense assembly indicating the high completeness of the gene regions of the final assembly (Supplementary Table 5)
We found that α whole-genome duplication (WGD) (Ks = 0.75) event was the most recent WGD event for T. arvense, and this WGD event was shared by T. arvense and three other members of Brassicaceae (Arabidopsis thaliana, Brassica rapa, and Eutrema salsugineum), except for B. rapa which experienced an addition of a whole-genome triplication (WGT) (Ks = 0.3) (Figure 1B; Wang et al, 2011)
Summary
Thlaspi arvense is a member of the extended II lineage of Brassicaceae (Huang et al, 2016), which is closely related to Arabidopsis. T. arvense is native to Eurasia and has a wide distribution in various temperate regions of the northern hemisphere (Warwick et al, 2002). T. arvense plants can survive in a wide altitude distribution from 0 to 4,000 m in the QinghaiTibet Plateau (QTP) region, the world’s highest plateau as a consequence of the continuous rising from the late Tertiary/midMiocene to the Quaternary, producing extensive genetic divergence and great species diversity (An et al, 2015; Zhang et al, 2019). Haplotypes of T. arvense unique to the QTP were recently recognized and collected. Based on a phylogeographic analysis, populations of T. arvense in China are a mixture of highly diverged ancestral subpopulations (An et al, 2015). T. arvense has been well recognized as a potential winter cover biofuel crop given its extreme cold tolerance and high seed oil content (Dorn et al, 2013, 2015; Sedbrook et al, 2014; Claver et al, 2017)
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