Genome and transcriptome analyses reveal parallel altitude adaptation in Chenopodium

Elucidating how crops adapt to heterogeneous environments requires integrative analyses of genome-wide variation, regulatory architecture, and evolutionary processes. Chenopodium quinoa, a globally important pseudocereal, shows strong ecological differentiation between highland and lowland ecotypes, yet the genetic and regulatory bases of environmental adaptation across the genus remain incompletely understood.

We generate a comprehensive genomic and transcriptomic resource consisting of whole-genome resequencing of 558 accessions from 20 Chenopodium species and transcriptomes from 295 accessions. Population genomic analyses reveal extensive genetic diversity, asymmetric evolution of the A and B subgenomes, and widespread interspecific introgression. Notably, Chenopodium berlandieri contributes adaptive variation to cultivated quinoa, particularly in genes related to stress response and immunity. Comparative analyses identify signatures of parallel adaptation to altitude in both quinoa and its wild relative Chenopodium berlandieri, including shared targets of selection such as PTR2, involved in nutrient transport, and CONSTANS, a key regulator of photoperiodic flowering. By genome-wide eQTL mapping, we identify 2,659 cis- and 407,628 trans-eQTLs regulating more than 11,000 genes. A major cis-eQTL controlling ELF3 expression is associated with large upstream deletions enriched in highland quinoa populations and correlated with reduced gene expression and elongated hypocotyls, implicating regulatory structural variation in altitude adaptation.

Our integrative analyses demonstrate how coding variation, regulatory divergence, and introgression jointly drive parallel environmental adaptation across wild and cultivated Chenopodium, providing insights into polyploid crop evolution and resources for breeding climate-resilient quinoa.