Population genomic analysis uncovers complex breeding history of celery

Celery, a key vegetable in the Apiaceae family, is widely valued for its nutrition and medicinal uses. It is commonly categorized into three varieties: A. graveolens var. dulce (common celery) with thick and solid petioles; A. graveolens var. rapaceum (celeriac) characterized by a round, enlarged hypocotyl; and A. graveolens var. secalinum (smallage or leaf celery) with slender, aromatic petioles. However, current research predominantly focuses on common celery, leaving the other two varieties understudied, thus limiting insights into their evolutionary history and genetic diversity.

Researchers from the Wuhan Botanical Garden of the Chinese Academy of Sciences achieved the first high-quality chromosomal-level genome assembly of celeriac using whole-genome sequencing. They also constructed a comprehensive genomic variation map by resequencing 177 celery samples. This study was published in Plant Biotechnology Journal.

Through phylogenetic, population structure, and genetic diversity analyses, the researchers discovered that Mediterranean smallage is the earliest cultivated celery type, providing evidence for its origin in the Mediterranean region.

"After initial domestication in this region, celery was artificially selected for two distinct purposes," said Prof. Gao Lei, the corresponding author of the study. "One selection led to celeriac with enlarged hypocotyls, while the other targeted common and Chinese leaf celery, focusing on petiole structure and flavor improvement."

Common celery petioles are solid and succulent, while those of celeriac and smallage are characteristically slender and hollow. Cross-sectional observations confirmed that hollow cavities develop progressively during petiole growth.

Using transcriptome analysis alongside SNP (single nucleotide polymorphisms)-GWAS (genome-wide association studies), and SV(structure variant)-GWAS, the researchers identified that the hollow/solid petiole trait in celery is linked to the presence or absence of a NAC gene, Agrc04g007090.

Population variation analysis revealed that this gene is present in all hollow celery and absent in solid petiole samples. Functional validation in Arabidopsis confirmed that Agrc04g007090 regulates hollow petiole formation by promoting programmed cell death in petiole pith cells.

These findings shed light on the cultivation and domestication history of celery while uncovering the molecular mechanisms underlying its key agronomic traits. They offer valuable genetic resources for the improvement and conservation of celery varieties.