Spatio-temporal transcriptome dynamics coordinate rapid transition of core crop functions in 'lactating' pigeon.
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ABSTRACT:
SUBMITTER: Wang Y
PROVIDER: S-EPMC10249823 | biostudies-literature | 2023 Jun
REPOSITORIES: biostudies-literature
Publications
Spatio-temporal transcriptome dynamics coordinate rapid transition of core crop functions in 'lactating' pigeon.
Wang Yujie Y Wang Xun X Luo Yi Y Zhang Jiaman J Lin Yu Y Wu Jie J Zeng Bo B Liu Lei L Yan Peiqi P Liang Jiyuan J Guo Hongrui H Jin Long L Tang Qianzi Q Long Keren K Li Mingzhou M
PLoS genetics 20230608 6
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 bree ...[more]
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Project description:<p>Pigeons (Columba livia) are widely kept as domesticated pets worldwide, and may have adapted to captivity through the evolutionarily specialized ability to produce ‘milk’ in the crops of both male and female parents via rapid proliferation and shedding of lipid- and protein-enriched epithelial cells. Given the implications for understanding evolution in atricial species, a comprehensive transcriptomic perspective of the pigeon crop spanning the complete breeding cycle is warranted. 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 cycle. This multi-omics analysis identified a set of ‘lactation’-related genes involved in lipid and protein metabolism that are highly expressed in the crop. Spatial transcriptomics analysis revealed extensive reorganization of long-range 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. This study thus illustrates the preferential de novo synthesis of ‘milk’ lipids and proteins in the crop epithelium prior to shedding from the lumen, and provides candidate enhancer loci for further investigation of the regulatory elements controlling pigeon ‘lactation’. Furthermore, these comprehensive datasets provide a foundational resource for avian and evolutionary biology research, especially relevant to atricial reproductive biology.</p>
2023-02-13 | MTBLS5195 | MetaboLights
Project description:BACKGROUND: Both male and female pigeons have the ability to produce a nutrient solution in their crop for the nourishment of their young. The production of the nutrient solution has been likened to lactation in mammals, and hence the product has been called pigeon 'milk'. It has been shown that pigeon 'milk' is essential for growth and development of the pigeon squab, and without it they fail to thrive. Studies have investigated the nutritional value of pigeon 'milk' but very little else is known about what it is or how it is produced. This study aimed to gain insight into the process by studying gene expression in the 'lactating' crop. RESULTS: Macroscopic comparison of 'lactating' and non-'lactating' crop reveals that the 'lactating' crop is enlarged and thickened with two very obvious lateral lobes that contain discrete rice-shaped pellets of pigeon 'milk'. This was characterised histologically by an increase in the number and depth of rete pegs extending from the basal layer of the epithelium to the lamina propria, and extensive proliferation and folding of the germinal layer into the superficial epithelium. A global gene expression profile comparison between 'lactating' crop and non-'lactating' crop showed that 542 genes are up-regulated in the 'lactating' crop, and 639 genes are down-regulated. Pathway analysis revealed that genes up-regulated in 'lactating' crop were involved in the proliferation of melanocytes, extracellular matrix-receptor interaction, the adherens junction and the wingless (wnt) signalling pathway. Gene ontology analysis showed that antioxidant response and microtubule transport were enriched in 'lactating' crop. CONCLUSIONS: There is a hyperplastic response in the pigeon crop epithelium during 'lactation' that leads to localised cellular stress and expression of antioxidant protein-encoding genes. The differentiated, cornified cells that form the pigeon 'milk' are of keratinocyte lineage and contain triglycerides that are likely endocytosed as very low density lipoprotein (VLDL) and repackaged as triglyceride in vesicles that are transported intracellularly by microtubules. This mechanism is an interesting example of the evolution of a system with analogies to mammalian lactation, as pigeon 'milk' fulfils a similar function to mammalian milk, but is produced by a different mechanism.
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Finally, we present associations between specific SNPs and gene expression levels in different brain regions across development. The dataset presented here provides research opportunities and a wealth of information not previously available to the scientific community. Here we report the generation and analysis of genome-wide exon-level transcriptome data from 16 brain regions comprising the cerebellar cortex, mediodorsal nucleus of the thalamus, striatum, amygdala, hippocampus, and 11 areas of the neocortex. The dataset was generated from 1,340 samples collected from both hemispheres of 57 postmortem human brains, spanning from embryonic development to late adulthood and representing males and females of multiple ethnicities. We also performed genome-wide genotyping of 2.5 million single nucleotide polymorphisms (SNPs) and assessed copy number variations for all donors. 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