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Upgraded durian genome reveals the role of chromosome reshuffling during ancestral karyotype evolution, lignin biosynthesis regulation, and stress tolerance

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Abstract

Durian (Durio zibethinus) is a tropical fruit that has a unique flavor and aroma. It occupies a significant phylogenetic position within the Malvaceae family. Extant core-eudicot plants are reported to share seven ancestral karyotypes that have undergone reshuffling, resulting in an abundant genomic diversity. However, the ancestral karyotypes of the Malvaceae family, as well as the evolution trajectory leading to the 28 chromosomes in durian, remain poorly understood. Here, we report the high-quality assembly of the durian genome with comprehensive comparative genomic analyses. By analyzing the collinear blocks between cacao and durian, we inferred 11 Malvaceae ancestral karyotypes. These blocks were present in a single-copy form in cacao and mainly in triplicates in durian, possibly resulting from a recent whole genome triplication (WGT) event that led to hexaploidization of the durian genome around 20 (17–24) million years ago. A large proportion of the duplicated genes in durian, such as those involved in the lignin biosynthesis module for phenylpropane biosynthesis, are derived directly from whole genome duplication, which makes it an important force in reshaping its genomic architecture. Transcriptome studies have revealed that genes involved in feruloyl-CoA formations were highly preferentially expressed in fruit peels, indicating that the thorns produced on durian fruit may comprise guaiacyl and syringyl lignins. Among all the analyzed transcription factors (TFs), members of the heat shock factor family (HSF) were the most significantly upregulated under heat stress. All subfamilies of genes encoding heat shock proteins (HSPs) in the durian genome appear to have undergone expansion. The potential interactions between HSF Dzi05.397 and HSPs were examined and experimentally verified. Our study provides a high-quality durian genome and reveals the reshuffling mechanism of ancestral Malvaceae chromosomes to produce the durian genome. We also provide insights into the mechanism underlying lignin biosynthesis and heat stress tolerance.

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Data availability

The Nanopore ultralong, PacBio, Hi-C, next-generation reads, and RNA-seq datasets generated in this study have been deposited in the China National Center for Bioinformation (https://www.cncb.ac.cn/?lang=en) under accession number PRJCA023599. The genome sequence and annotation files are available at Figshare under the link (https://figshare.com/articles/dataset/Durian_genome_annotation/25237591).

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Acknowledgement

This work was supported by Shaanxi Normal University Academician Expert Workstation Foundation (1110010375) and the National Key Laboratory of Protein and Plant Gene Research Open Project (ZD2021058). We would like to express our special gratitude to Professor Fan Hongyan from the Institute of Tropical Fruit Tree of Hainan Academy of Agricultural Sciences for her valuable contribution to durian materials.

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Correspondence to Jianing Yu or Yuxian Zhu.

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11427_2024_2580_MOESM1_ESM.docx

Upgraded durian genome reveals ancestral karyotype, chromosome reshuffling plus mechanisms of lignin biosynthesis and stress tolerance

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Upgraded durian genome reveals ancestral karyotype, chromosome reshuffling plus mechanisms of lignin biosynthesis and stress tolerance

Table S16

A set of 135 single-copy genes from 14 species used to build the phylogenetic tree.

Table S17

FPKM of 15,072 genes that exhibited a 1:3 ratio.

Table S19

Genes exhibited Ka/Ks >0.7 in durian genome.

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Li, W., Chen, X., Yu, J. et al. Upgraded durian genome reveals the role of chromosome reshuffling during ancestral karyotype evolution, lignin biosynthesis regulation, and stress tolerance. Sci. China Life Sci. 67, 1266–1279 (2024). https://doi.org/10.1007/s11427-024-2580-3

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