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

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’.

Assembly and annotation of 2 high-quality columbid reference genomes from sequencing of a Columba livia × Columba guinea F1 hybrid

“…The Cliv_3 and Cgui_1 assemblies have contig N50s of 6.97 and 7.61 Mb, respectively. Therefore, the overall contiguity of the Cliv_3 assembly shows significant improvement over Cliv_2.1, which has a contig N50 of only 26 kb ( Table 1 ), and compares favorably to a recent C. livia PacBio-based assembly that has a slightly higher contig N50 of 7.8 Mb, but a larger number of contigs (1,949) ( Wang et al . 2023 ).…”

“…2018 ). However, updated sequencing technology has paved the way for substantial improvements in contiguity and completeness, as seen in a recently released C. livia assembly ( Wang et al . 2023 ).…”

Comprehensive Transcriptomic and Metabolomic Analysis Revealed the Functional Differences in Pigeon Lactation between Male and Female during the Reproductive Cycle

“…Growing evidence shows the synthesis of crop milk is controlled by prolactin- and insulin-activated pathways [ 20 , 21 , 22 , 23 ], which have an effect on the protein synthesis and apoptosis of crop epidermal cells [ 24 ]. Recently, a multiomics analysis identified some transcriptional regulatory elements that play key roles in the formation mechanisms of pigeon crop milk [ 25 ]. However, little literature is available on the chemical composition of pigeon crop milk and the underlying mechanism affecting its production between male and female pigeons.…”