Nature sub-journal: Genome evolution of allium crops and the formation mechanism of special spicy flavors

Allium is the world's second largest vegetable cash crop after tomatoes, and because it is rich in unique spicy flavors, it is often used in vegetables, condiments or medicinal plants and is widely cultivated
worldwide.
For a long time, due to the characteristics of large genomes, its functional genes, genomic biology and molecular breeding research have been limited, especially its genetic and kinship are not clear, genomic evolution and the molecular metabolic basis of special flavor formation have not been resolved
.
Recently, the team of Professor Yu Jingquan/Zhang Mingfang/Zhou Yanhong of the College of Agronomy of Zhejiang University was published in the well-known nature sub-journal Nature Communications "Chromosome-level genome assembly of bunching onion illuminates genome evolution and flavor formation in Allium crops
".

The study used allium plant resources from China, Japan, South Korea, the United States, Europe, Russia, Central Asia and West Asia and other geographical sources to assemble the genome at the chromosome level of allium from scratch for the first time, and revealed the genomic basis of genomic evolution, chromosomal homology, family expansion of key genes and the formation of special spicy flavor of allium plants through population genetics, molecular evolution and comparative genome research, combined with multi-omics methods, and clarified that China is the origin and domestication center of allium onion
。 This achievement provides important scientific theoretical guidance
for the research of evolutionary biology, genome breeding and molecular improvement of allium plants.

Using integrated techniques such as PacBio, Bionano and HiC, the study assembled the highest quality chromosome-level genome
to date.
Comparative genomic studies have found that onions and onions diverged about 7 million years ago, while garlic diverged with the common ancestor of onions and onions about 16 million years ago, similar to garlic.
Three genome-wide replication events also occurred before Allium species diverged from each other, and collinear analysis showed that the genome chromosomes of the three Allium crops were highly homologous and evolutionarily close
to each other.
The study found that gene families associated with the biosynthesis of sulfur compounds associated with particular flavors expanded significantly in three allium plants with long terminal repeats LTR (especially Gypsy The accumulation of Allium was the main reason for the genome expansion of Allium plants, and the uneven expansion of different LTR branches led to the diversity of Allium genome components.
Widespread scattered repeat (DSD) events are responsible for
gene amplification and differentiation in the onion genome.
At the same time, two key gene families for the synthesis and metabolism of cysteine, sulfoxide (ACSO), the key substances for the formation of allium flavor were found - allinase, ALL and tear factor synthetase LFS has undergone a large expansion in the Allium genome (Figure 1a, d), and it presents unique expansion patterns and expression patterns in different Allium plants (Figure 1b) , the flavor substances of onion and onion seeds are mainly isoallicin, while garlic is mainly allicin (Figure 2c); It was found that the LFS and ALL family genes related to the formation of special flavor in allium crops underwent significant expansion, functional differentiation and redundancy in the process of evolution
.

Figure 1: Massive replication and differentiation of sulfide metabolism-related genes in Allium plants

Research has also revealed the origin and domestication pathways of onions
.
For a long time, the morphology, chromosome number and karyotype similarity of allium plants have led to unclear taxonomic status, and there are a large number of conspecifics and heterogeneous phenomena
.
This study uses genomics and population genetics to analyze the history of population differentiation and domestication of allium plants, corrects the academic thesis that Altai onion is the ancestor species of allium for a long time, and clarifies that Altai onion is evolutionarily closer to Chinese shallot
.
The plant onion resources of different geographical origin can be divided into 2 populations and 5 subgroups (Figure 2a, b), and it is found and verified that cultivated onions mainly originated in northwest China, and it is proposed that the land spread of green onions from western China to Central Asia and the domestication of cultivated onions in China and then from the southern region of China to Japan, Europe, and the Maritime migration paths
for spread in the Americas.

Fig.
2: Population genetic structure and domestication transmission pathway of Allium spp

Professor Yu Jingquan, Professor Zhang Mingfang and Professor Zhou Yanhong of the College of Agronomy of Zhejiang University are the corresponding authors of the paper, and Dr.
Liao Nanjiao, Associate Professor Hu Zhongyuan, Professor Miao Jinshan of Weifang University of Science and Technology, and Dr.
Hu Xiaodi of Nuohe Zhiyuan Institute of Bioinformatics are the co-first authors
of the paper.
The research was supported by the Modern Agricultural Industry Technology System of the Ministry of Agriculture (CARS-24-B-01) and the Special Fund for Basic Scientific Research of Central Universities (+226?2022-00100).

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