Zanthoxylum-specific whole genome duplication and recent activity of transposable elements in the highly repetitive paleotetraploid Z. bungeanum genome

Shijing Feng,Huifeng Jiang,Min Liu,Gang Wang,Anzhi Wei,Yulin Liu,He Dai,Lu Tian,Tuxi Yang,Yonghong Liu,Zhenshan Liu,Zujun Yang,Jisen Zhang,Jian Cheng,Zihe Li,Qing Zhang

doi:10.1038/s41438-021-00665-1

Abstract

Zanthoxylum bungeanum is an important spice and medicinal plant that is unique for its accumulation of abundant secondary metabolites, which create a characteristic aroma and tingling sensation in the mouth. Owing to the high proportion of repetitive sequences, high heterozygosity, and increased chromosome number of Z. bungeanum, the assembly of its chromosomal pseudomolecules is extremely challenging. Here, we present a genome sequence for Z. bungeanum, with a dramatically expanded size of 4.23 Gb, assembled into 68 chromosomes. This genome is approximately tenfold larger than that of its close relative Citrus sinensis. After the divergence of Zanthoxylum and Citrus, the lineage-specific whole-genome duplication event η-WGD approximately 26.8 million years ago (MYA) and the recent transposable element (TE) burst ~6.41 MYA account for the substantial genome expansion in Z. bungeanum. The independent Zanthoxylum-specific WGD event was followed by numerous fusion/fission events that shaped the genomic architecture. Integrative genomic and transcriptomic analyses suggested that prominent species-specific gene family expansions and changes in gene expression have shaped the biosynthesis of sanshools, terpenoids, and anthocyanins, which contribute to the special flavor and appearance of Z. bungeanum. In summary, the reference genome provides a valuable model for studying the impact of WGDs with recent TE activity on gene gain and loss and genome reconstruction and provides resources to accelerate Zanthoxylum improvement.

Highlights

Introduction As close relatives ofCitrus in the Rutaceae family, plants of the genus Zanthoxylum generate strong tingling and numbing sensations in the mouth, which together with the pungent taste of hot chili form the spicy-hot flavor of Asian cuisine
The evolution of gene families was analyzed by comparing the Z. bungeanum genome with that of 16 other plant species, including Amborella trichopoda, Piper nigrum, Zea mays, Oryza sativa, Papaver somniferum, Vitis vinifera, Dimocarpus longan, Arabidopsis thaliana, Brassica napus, Gossypium hirsutum, Arachis hypogaea, Cucumis sativus, Sesamum indicum, Capsicum annuum, Citrus sinensis, and Nicotiana tabacum
The distributions of synonymous substitutions per synonymous site (KS) of paralogous genes in the Z. bungeanum genome showed a single peak at approximately 0.21, but no similar peak was identified in C. sinensis (Fig. 2B), suggesting the occurrence of a recent whole-genome duplication (WGD) event experienced by Zanthoxylum that was not shared among other Rutaceae members

Summary

Introduction

Introduction As close relatives ofCitrus in the Rutaceae family, plants of the genus Zanthoxylum generate strong tingling and numbing sensations in the mouth, which together with the pungent taste of hot chili form the spicy-hot flavor of Asian cuisine. The distributions of synonymous substitutions per synonymous site (KS) of paralogous genes in the Z. bungeanum genome showed a single peak at approximately 0.21, but no similar peak was identified in C. sinensis (Fig. 2B), suggesting the occurrence of a recent WGD event experienced by Zanthoxylum (ηWGD) that was not shared among other Rutaceae members. These results combined with the phylogenetic analysis (Fig. 2A) indicated that the η-WGD of Z. bungeanum occurred after the divergence of Citrus and Zanthoxylum.

Results

Conclusion