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. 2023 Nov 27;11(1):uhad244.

doi: 10.1093/hr/uhad244. eCollection 2024 Jan.

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PMID: 38225981 PMCID: PMC10788775 DOI: 10.1093/hr/uhad244

The haplotype-resolved telomere-to-telomere carnation (Dianthus caryophyllus) genome reveals the correlation between genome architecture and gene expression

Lan Lan et al. Hortic Res. 2023.

Abstract

Carnation (Dianthus caryophyllus) is one of the most valuable commercial flowers, due to its richness of color and form, and its excellent storage and vase life. The diverse demands of the market require faster breeding in carnations. A full understanding of carnations is therefore required to guide the direction of breeding. Hence, we assembled the haplotype-resolved gap-free carnation genome of the variety 'Baltico', which is the most common white standard variety worldwide. Based on high-depth HiFi, ultra-long nanopore, and Hi-C sequencing data, we assembled the telomere-to-telomere (T2T) genome to be 564 479 117 and 568 266 215 bp for the two haplotypes Hap1 and Hap2, respectively. This T2T genome exhibited great improvement in genome assembly and annotation results compared with the former version. The improvements were seen when different approaches to evaluation were used. Our T2T genome first informs the analysis of the telomere and centromere region, enabling us to speculate about specific centromere characteristics that cannot be identified by high-order repeats in carnations. We analyzed allele-specific expression in three tissues and the relationship between genome architecture and gene expression in the haplotypes. This demonstrated that the length of the genes, coding sequences, and introns, the exon numbers and the transposable element insertions correlate with gene expression ratios and levels. The insertions of transposable elements repress expression in gene regulatory networks in carnation. This gap-free finished T2T carnation genome provides a valuable resource to illustrate the genome characteristics and for functional genomics analysis in further studies and molecular breeding.

© The Author(s) 2024. Published by Oxford University Press on behalf of Nanjing Agricultural University.

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Figures

Figure 1 Figure 1

The phenotypes and gap-free genome assembly features of ‘Baltico’. A–D ‘Baltico’ plant (A) and its different tissues: (B) shoot, (C) flower bud, and (D) blooming flower. E, F Hi-C heat maps of Hap1 (E) and Hap2 (F). G, Hk-mer spectrum analysis plots generated by KAT for Hap1 (F) and Hap2 (H); the black region represents the proportion of k-mers present in the HiFi reads but missing in the assemblies.

Figure 2 Figure 2

Genome structure of each chromosome and structure of four centromeres in ‘Baltico’ gap-free genomes. A Genome features of each chromosome in ‘Baltico’ gap-free haplotypes and collinearity analysis between the haplotypes; bin sizes of different features were all set at 100 kb. B Sequence identity heat map of candidate centromere regions for Chr10 and Chr13 in two haplotypes. Cold colors indicate low identity between regions, while warm colors indicate high identity between regions.

Figure 3 Figure 3

Relationship between gene expression and genome architecture. A, D Expression ratio (A) and FPKM (D) of different lengths of CDSs, introns and genes among the two gap-free haplotype-resolved genomes. *P ≤ 0.05; **P ≤ 0.01, ***P ≤ 0.001; ****P ≤ 0.0001; ns, no significant difference. B, E Expression ratio (B) and FPKM (E) of different lengths of CDS, introns, and genes. Letters a–g refer to results of significant difference analysis. C, F Different expression ratio (C) and FPKM (F) of genes with specific intact TE insertions. The orbicular indicates the group exhibiting no significant difference from Total genes; the pentagram refers to the particular group that exhibited no significant difference from the None groups. ‘Total’ refers to total annotated genes in the genomes; ‘None’ means the genes did not have correlation with TE insertion; ‘n’ refers to the total number of the specific group. G Hap1 and Hap2 separated into seven clusters through GDA. H Location of the seven clusters classified by GDA among chromosomes of the Hap1.

Figure 4 Figure 4

Allele-specific expression characteristics. A Similarity of allele CDS between two haplotypes. B Statistics on the number of different types of ASE in flowers, roots, and leaves. C Venn diagram indicating the number of ASEs in three tissues. (D) Ka/Ks values for different classes of ASE in flowers. Dots represent outliers. Boxes represent 25–75% of the value. The upper and lower horizontal lines represent the range with 1.5 interquartile range. E Distribution of ASEs (class of ‘increased expression of one allele’) in two haplotypes in flowers. Expressions are presented as log10(FPKM + 1). *P ≤ 0.05; **P ≤ 0.01; ***P ≤ 0.001; ****P ≤ 0.0001 (t-test). F GO enrichment analysis of class of biallelic expression in flower. G GO enrichment analysis of class of unbalanced expression alleles in flower.

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