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

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'. Author summary: The provision of food by parents is essential for offspring survival in some species. Unlike most birds, pigeons produce a 'milk' in their crops to feed hatched squabs. Here, using a multi-omics strategy, we conducted an integrated behavioral, genomic, transcriptomic, and chromatin interactome analysis of 'milk' production in the crop during the pigeon breeding stages. We generated a chromosome-level pigeon genome and annotated 18,660 high confidence protein-coding genes. Examination of spatio-temporal transcriptomic profiles revealed that lipid and protein synthesis-related genes are expressed at high levels in 'lactating' crops, suggesting that lipids and proteins used for 'milk' are preferentially synthesized de novo in the crop. We also identified the cis-regulatory elements of these 'lactation'-related genes and found that their expression is modulated by variation in promoter-enhancer chromatin-level interactions. Our data indicate that lipid- and protein-loaded crop epithelial cells proliferate rapidly and slough off during the 'lactation' stage to form pigeon 'milk'. This study provides an informative reference for further investigation of the transcriptional regulation underlying pigeon 'lactation'. [ABSTRACT FROM AUTHOR]