Photoperiodically driven transcriptome-wide changes in the hypothalamus reveal transcriptional differences between physiologically contrasting seasonal life-history states in migratory songbirds

Abstract

We investigated time course of photoperiodically driven transcriptional responses in physiologically contrasting seasonal life-history states in migratory blackheaded buntings. Birds exhibiting unstimulated winter phenotype (photosensitive state; responsive to photostimulation) under 6-h short days, and regressed summer phenotype (photorefractory state; unresponsiveness to photostimulation) under 16-h long days, were released into an extended light period up to 22 h of the day. Increased tshβ and dio2, and decreased dio3 mRNA levels in hypothalamus, and low prdx4 and high il1β mRNA levels in blood confirmed photoperiodic induction by hour 18 in photosensitive birds. Further, at hours 10, 14, 18 and 22 of light exposure, the comparison of hypothalamus RNA-Seq results revealed transcriptional differences within and between states. Particularly, we found reduced expression at hour 14 of transthyretin and proopiomelanocortin receptor, and increased expression at hour 18 of apolipoprotein A1 and carbon metabolism related genes in the photosensitive state. Similarly, valine, leucine and isoleucine degradation pathway genes and superoxide dismutase 1 were upregulated, and cocaine- and amphetamine-regulated transcript and gastrin-releasing peptide were downregulated in the photosensitive state. These results show life-history-dependent activation of hypothalamic molecular pathways involved in initiation and maintenance of key biological processes as early as on the first long day.

Genetic Control of Avian Migration: Insights from Studies in Latitudinal Passerine Migrants

“…A study on redheaded buntings reported a significant increase after exposure to a single long day in mRNA levels of Pax6 (paired box 6) involved in the activation of Eya3 (Eye absent 3, important for photoperiodic induction), Tshβ , Dio2 and Rhodopsin genes [ 64 ]. A similar significant increase in the mRNA expression of Tshβ and Dio2 and a decrease in Dio3 level was found by hour 18 of the first long day in migratory blackheaded bunting ( Figure 2 , [ 65 ]). Interestingly, the peak mRNA expression of Tshβ and Dio2 occurred during hour 14–16 of the day, consistent with the circadian rhythm in photo-inducibility of the photoperiodic response system in buntings [ 66 ].…”

The DNA methylation status of the serotonin metabolic pathway associated with reproductive inactivation induced by long-light exposure in Magang geese

“…At the expression level, Photoperiodism impacted gene expression levels in the hypothalamus [ 4 , 5 , 48 ]. Gene expression in the hypothalamus was associated with increased TSHβ and dio2 mRNA levels and decreased dio3 mRNA levels under long light conditions [ 48 ].…”

“…At the expression level, Photoperiodism impacted gene expression levels in the hypothalamus [ 4 , 5 , 48 ]. Gene expression in the hypothalamus was associated with increased TSHβ and dio2 mRNA levels and decreased dio3 mRNA levels under long light conditions [ 48 ]. As expected, the expression level of dio2 observed a significant increase in RD after long light exposure in the hypothalamus of Magang geese.…”

The DNA methylation status of the vitamin A signaling associated with testicular degeneration induced by long-day photoperiods in Magang geese

“…A long-day photoperiod caused a profound change in the architecture and function of the testes of Magang geese. Although transcriptome responses to photoperiod effects on the testis have been extensively studied in avians ( Sun et al, 2020 ; Sharma, et al, 2021 ), relatively little is known about the epigenetic impact of testicular regression during long-day photoperiods. Current knowledge is primarily based on genetic analyses of candidate genes associated with endocrine regulation of the HPG axis ( Leska, et al, 2012 ; Gumułka, et al, 2023 ).…”