Spatio-temporal transcriptome dynamics coordinate rapid transition of core crop functions in 'lactating' pigeon

PLoS Genet. 2023 Jun 8;19(6):e1010746. doi: 10.1371/journal.pgen.1010746. eCollection 2023 Jun.

Abstract

Pigeons (Columba livia) are among a select few avian species that have developed a specialized reproductive mode wherein the parents produce a 'milk' in their crop to feed newborn squabs. Nonetheless, the transcriptomic dynamics and role in the rapid transition of core crop functions during 'lactation' remain largely unexplored. Here, we generated a de novo pigeon genome assembly to construct a high resolution spatio-temporal transcriptomic landscape of the crop epithelium across the entire breeding stage. This multi-omics analysis identified a set of 'lactation'-related genes involved in lipid and protein metabolism, which contribute to the rapid functional transitions in the crop. Analysis of in situ high-throughput chromatin conformation capture (Hi-C) sequencing revealed extensive reorganization of promoter-enhancer interactions linked to the dynamic expression of these 'lactation'-related genes between stages. Moreover, their expression is spatially localized in specific epithelial layers, and can be correlated with phenotypic changes in the crop. These results illustrate the preferential de novo synthesis of 'milk' lipids and proteins in the crop, and provides candidate enhancer loci for further investigation of the regulatory elements controlling pigeon 'lactation'.

MeSH terms

  • Animals
  • Columbidae* / genetics
  • Columbidae* / metabolism
  • Female
  • Gene Expression Profiling
  • Lactation
  • Milk
  • Transcriptome* / genetics

Grants and funding

This work was supported by the National Key R & D Program of China (2022YFF1000100 to Q.T.), the National Natural Science Foundation of China (32225046 to M.L.), the Sichuan Science and Technology Program (2022NSFSC0068 to X.W, 2021YFYZ0009 to M.L., and 2022JDJQ0054 to L.J.), and the Ya’an Science and Technology Program (21SXHZ0022 to L.J.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.