High-quality genome assembly and comparative genomic profiling of yellowhorn (Xanthoceras sorbifolia) revealed environmental adaptation footprints and seed oil contents variations.

Yellowhorn (Xanthoceras sorbifolia) is a species of deciduous tree that is native to Northern and Central China, including Loess Plateau. The yellowhorn tree is a hardy plant, tolerating a wide range of growing conditions, and is often grown for ornamental purposes in parks, gardens, and other landscaped areas. The seeds of yellowhorn are edible and contain rich oil and fatty acid contents, making it an ideal plant for oil production. However, the mechanism of its ability to adapt to extreme environments and the genetic basis of oil synthesis remains to be elucidated. In this study, we reported a high-quality and near gap-less yellowhorn genome assembly, containing the highest genome continuity with a contig N50 of 32.5 Mb. Comparative genomics analysis showed that 1,237 and 231 gene families under expansion and the yellowhorn-specific gene family NB-ARC were enriched in photosynthesis and root cap development, which may contribute to the environmental adaption and abiotic stress resistance of yellowhorn. A 3-ketoacyl-CoA thiolase (KAT) gene (Xso_LG02_00600) was identified under positive selection, which may be associated with variations of seed oil content among different yellowhorn cultivars. This study provided insights into environmental adaptation and seed oil content variations of yellowhorn to accelerate its genetic improvement.

Metabolomics analysis reveals amelioration effects of yellowhorn tea extract on hyperlipidemia, inflammation, and oxidative stress in high-fat diet-fed mice.

Yellowhorn tea (YT) is traditionally used as a lipid-lowering beverage in Mongolian minorities. However, the pharmacological effects of YT extract and its specific metabolic changes in hyperlipidemia models are not fully understood. The aim of this study was to identify biomarkers using untargeted metabolomics techniques and to investigate the mechanisms underlying the changes in metabolic pathways associated with lipid lowering, anti-inflammation and anti-oxidant in hyperlipidemic mice. A high-fat diet (HFD)-induced hyperlipidemic mouse model was established. YT extract was administered as oral gavage at 0.15, 0.3, and 0.6 g/kg doses for 10 weeks. HFD-induced hyperlipidemia and the therapeutic effect of YT extract were evaluated based on histopathology and by assessing blood lipid levels. Liver inflammatory factors and oxidative stress indices were determined using enzyme-linked immunosorbent assays. Liver metabolites were evaluated using untargeted metabolomics. Biochemical and histological examinations showed that YT extract significantly reduced body-weight gain (p < 0.01) and fat deposition in tissues. YT extract significantly reduced the levels of serum and liver triglyceride and total cholesterol; inflammatory factors [interleukin (IL)-6, IL-1ß, and tumor necrosis factor-α]; malondialdehyde; and leptin (p < 0.05) in hyperlipidemic mice. YT extract also significantly increased the levels of oxidative stress indicators (superoxide dismutase, catalase, and glutathione peroxidase) and adiponectin. Metabolomics studies revealed several endogenous molecules were altered by the high-fat diet and recovery following intervention with YT extract. The metabolites that were significantly different in the liver after YT intake included citicoline, acetylcholine, pyridoxine, and NAD. Pathway analysis indicated that YT extract ameliorated HFD-induced hyperlipidemia in mice via three major metabolic pathways, namely, glycerophospholipid metabolism, vitamin B6 metabolism, and nicotinate and nicotinamide metabolism. This study demonstrates YT extract has profound effects on the alleviation of HFD-induced hyperlipidemia, inflammation and oxidative stress.

Differential gene expression and potential regulatory network of fatty acid biosynthesis during fruit and leaf development in yellowhorn (Xanthoceras sorbifolium), an oil-producing tree with significant deployment values.

Xanthoceras sorbifolium (yellowhorn) is a woody oil plant with super stress resistance and excellent oil characteristics. The yellowhorn oil can be used as biofuel and edible oil with high nutritional and medicinal value. However, genetic studies on yellowhorn are just in the beginning, and fundamental biological questions regarding its very long-chain fatty acid (VLCFA) biosynthesis pathway remain largely unknown. In this study, we reconstructed the VLCFA biosynthesis pathway and annotated 137 genes encoding relevant enzymes. We identified four oleosin genes that package triacylglycerols (TAGs) and are specifically expressed in fruits, likely playing key roles in yellowhorn oil production. Especially, by examining time-ordered gene co-expression network (TO-GCN) constructed from fruit and leaf developments, we identified key enzymatic genes and potential regulatory transcription factors involved in VLCFA synthesis. In fruits, we further inferred a hierarchical regulatory network with MYB-related (XS03G0296800) and B3 (XS02G0057600) transcription factors as top-tier regulators, providing clues into factors controlling carbon flux into fatty acids. Our results offer new insights into key genes and transcriptional regulators governing fatty acid production in yellowhorn, laying the foundation for efforts to optimize oil content and fatty acid composition. Moreover, the gene expression patterns and putative regulatory relationships identified here will inform metabolic engineering and molecular breeding approaches tailored to meet biofuel and bioproduct demands.

Centromere-Specific Retrotransposons and Very-Long-Chain Fatty Acid Biosynthesis in the Genome of Yellowhorn (Xanthoceras sorbifolium, Sapindaceae), an Oil-Producing Tree With Significant Drought Resistance.

In-depth genome characterization is still lacking for most of biofuel crops, especially for centromeres, which play a fundamental role during nuclear division and in the maintenance of genome stability. This study applied long-read sequencing technologies to assemble a highly contiguous genome for yellowhorn (Xanthoceras sorbifolium), an oil-producing tree, and conducted extensive comparative analyses to understand centromere structure and evolution, and fatty acid biosynthesis. We produced a reference-level genome of yellowhorn, ∼470 Mb in length with ∼95% of contigs anchored onto 15 chromosomes. Genome annotation identified 22,049 protein-coding genes and 65.7% of the genome sequence as repetitive elements. Long terminal repeat retrotransposons (LTR-RTs) account for ∼30% of the yellowhorn genome, which is maintained by a moderate birth rate and a low removal rate. We identified the centromeric regions on each chromosome and found enrichment of centromere-specific retrotransposons of LINE1 and Gypsy in these regions, which have evolved recently (∼0.7 MYA). We compared the genomes of three cultivars and found frequent inversions. We analyzed the transcriptomes from different tissues and identified the candidate genes involved in very-long-chain fatty acid biosynthesis and their expression profiles. Collinear block analysis showed that yellowhorn shared the gamma (γ) hexaploidy event with Vitis vinifera but did not undergo any further whole-genome duplication. This study provides excellent genomic resources for understanding centromere structure and evolution and for functional studies in this important oil-producing plant.

Yellowhorn drought-induced transcription factor XsWRKY20 acts as a positive regulator in drought stress through ROS homeostasis and ABA signaling pathway.

Yellowhorn (Xanthoceras sorbifolium) is a peculiar woody edible oil-bearing tree in China. WRKY transcription factors have specific roles in plant multiple abiotic stress responses. However, it is still not clear that the molecular mechanisms of WRKYs involve in drought tolerance in yellowhorn. In this study, we isolated a drought-induced group I WRKY gene from yellowhorn, designated as XsWRKY20. Expression of XsWRKY20 was strongly induced by PEG6000, NaCl, ABA and SA. Virus-induced gene silencing (VIGS) of XsWRKY20 reduced tolerance to drought stress in yellowhorn, as determined through physiological analyses of POD activity, SOD activity and proline content. This susceptibility was coupled with decreased expression of stress-related genes. In contrast, overexpression of XsWRKY20 in tobacco notably improved drought tolerance. Compared with the WT plants, the XsWRKY20-transgenic lines exhibited lower ROS and MDA content and higher antioxidant enzyme activity and proline content after drought treatment. Moreover, overexpression of XsWRKY20 enhanced the expression of several genes associated with encoding these antioxidant enzymes, proline biosynthesis and ABA signaling pathway. Taken together, XsWRKY20 functions as a positive regulator contributing to drought stress tolerance through either ROS homeostasis by antioxidant systems or ABA-dependent/independent gene expression pathway.

Pseudomolecule-level assembly of the Chinese oil tree yellowhorn (Xanthoceras sorbifolium) genome.

BACKGROUND: Yellowhorn (Xanthoceras sorbifolium) is a species of the Sapindaceae family native to China and is an oil tree that can withstand cold and drought conditions. A pseudomolecule-level genome assembly for this species will not only contribute to understanding the evolution of its genes and chromosomes but also bring yellowhorn breeding into the genomic era. FINDINGS: Here, we generated 15 pseudomolecules of yellowhorn chromosomes, on which 97.04% of scaffolds were anchored, using the combined Illumina HiSeq, Pacific Biosciences Sequel, and Hi-C technologies. The length of the final yellowhorn genome assembly was 504.2 Mb with a contig N50 size of 1.04 Mb and a scaffold N50 size of 32.17 Mb. Genome annotation revealed that 68.67% of the yellowhorn genome was composed of repetitive elements. Gene modelling predicted 24,672 protein-coding genes. By comparing orthologous genes, the divergence time of yellowhorn and its close sister species longan (Dimocarpus longan) was estimated at ∼33.07 million years ago. Gene cluster and chromosome synteny analysis demonstrated that the yellowhorn genome shared a conserved genome structure with its ancestor in some chromosomes. CONCLUSIONS: This genome assembly represents a high-quality reference genome for yellowhorn. Integrated genome annotations provide a valuable dataset for genetic and molecular research in this species. We did not detect whole-genome duplication in the genome. The yellowhorn genome carries syntenic blocks from ancient chromosomes. These data sources will enable this genome to serve as an initial platform for breeding better yellowhorn cultivars.