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Rapid Genome Evolution and Adaptation of Thlaspi arvense Mediated by Recurrent RNA-Based and Tandem Gene Duplications.

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.

SUBMITTER: Hu Y

PROVIDER: S-EPMC8764390 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundUnderstanding how organisms evolve and adapt to extreme habitats is of crucial importance in evolutionary ecology. Altitude gradients are an important determinant of the distribution pattern and range of organisms due to distinct climate conditions at different altitudes. High-altitude regions often provide extreme environments including low temperature and oxygen concentration, poor soil, and strong levels of ultraviolet radiation, leading to very few plant species being able to populate elevation ranges greater than 4000 m. Field pennycress (Thlaspi arvense) is a valuable oilseed crop and emerging model plant distributed across an elevation range of nearly 4500 m. Here, we generate an improved genome assembly to understand how this species adapts to such different environments.ResultsWe sequenced and assembled de novo the chromosome-level pennycress genome of 527.3 Mb encoding 31,596 genes. Phylogenomic analyses based on 2495 single-copy genes revealed that pennycress is closely related to Eutrema salsugineum (estimated divergence 14.32-18.58 Mya), and both species form a sister clade to Schrenkiella parvula and genus Brassica. Field pennycress contains the highest percentage (70.19%) of transposable elements in all reported genomes of Brassicaceae, with the retrotransposon proliferation in the Middle Pleistocene being likely responsible for the expansion of genome size. Moreover, our analysis of 40 field pennycress samples in two high- and two low-elevation populations detected 1,256,971 high-quality single nucleotide polymorphisms. Using three complementary selection tests, we detected 130 candidate naturally selected genes in the Qinghai-Tibet Plateau (QTP) populations, some of which are involved in DNA repair and the ubiquitin system and potential candidates involved in high-altitude adaptation. Notably, we detected a single base mutation causing loss-of-function of the FLOWERING LOCUS C protein, responsible for the transition to early flowering in high-elevation populations.ConclusionsOur results provide a genome-wide perspective of how plants adapt to distinct environmental conditions across extreme elevation differences and the potential for further follow-up research with extensive data from additional populations and species.

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Rapid Genome Evolution and Adaptation of Thlaspi arvense Mediated by Recurrent RNA-Based and Tandem Gene Duplications.

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