Circadian timing in central and peripheral tissues in a migratory songbird: dependence on annual life‐history states

Abstract

Predictable seasonal change in photoperiod triggers a sequential change in the daily activity-rest pattern, adaptive for migration in several bird species. The night-migratory black-headed bunting (Emberiza melanocephala) is day active under short photoperiods (8 h light:16 h dark, short day sensitive). Under long photoperiods (16 h light:8 h dark), the buntings are initially day active (long day premigratory) but subsequently become intensely night active (long day migratory) and after few weeks again return to a day active pattern (long day refractory). However, it is unclear how the daily expression of circadian genes changes during photoperiod-induced seasonal life-history states (LHSs). We measured period 2 (Per2), cryptochrome 1 (Cry1), brain and muscle arnt-like protein 1 (Bmal1), and circadian locomotor output cycles kaput (Clock) mRNA expressions in various neural and peripheral tissues of buntings in different LHSs and discovered differences of ∼2 to 6 h in the phase and 2- to 4-fold in amplitude of circadian oscillations of Per2, Cry1, and Bmal1 between photoperiod-induced LHSs. Phase relationship in mRNA oscillations was altered between oscillator components in the circadian pacemaker system (retina, pineal, hypothalamus) as well as in the peripheral (liver, muscle) tissues. These results show for the first time altered waveforms of clock gene expressions in all tissues in parallel with behavioral shifts and suggest the involvement of circadian system in photoperiod induction of seasonal LHSs in a migratory species.

Hypothalamic and liver transcriptome from two crucial life‐history stages in a migratory songbird

“…birds fatten and gain weight, develop nocturnal Zugunruhe and show elevated plasma corticosterone, testosterone and luteinizing hormone (LH) concentrations and gonadal recrudescence (Jain & Kumar, ; Mishra et al., ; Misra et al., ; Rani et al., ). Hypothalamus and liver mRNA levels of the circadian clock and light‐ and thyroid hormone‐responsive genes and of genes involved in carbohydrate and fat metabolism and oxidative phosphorylation show changes with alteration in the seasonal state (Mishra et al., ; Singh et al., ; Trivedi et al., ; Trivedi, Malik, Rani, & Kumar, ). We predicted transcriptome‐wide changes in the hypothalamus and liver with photostimulation of the spring migratory state in black‐headed buntings.…”

Proteus: a random forest classifier to predict disorder-to-order transitioning binding regions in intrinsically disordered proteins

“…Indeed, serine-rich proteins in bacterial enzymes like kinases [50] and eukaryotic splicing factors [51] have been reported to be part of intrinsically disordered proteins. The other polar (Thr, Asn, Gln) and charged (Asp, Glu, Lys, Arg) amino acids were found to have similar or slightly higher propensities in disordered compared to ordered sequences, which agrees well with the earlier observations [47, 48].…”

Transcriptome‐wide changes in testes reveal molecular differences in photoperiod‐induced seasonal reproductive life‐history states in migratory songbirds

“…All procedures were approved by the Institutional Animal Ethics Committee of the Department of Zoology, University of Lucknow (protocol no: LU/ZOOL/IRPHA/Protocol2.3/NOV07), where the experiment was done. We used testes from the experiment, as earlier described (Mishra, Singh, & Kumar, ; D. Singh, Trivedi, Rani, Panda, & Kumar, ). Briefly, adult male black‐headed buntings were maintained until the beginning (for about 40 weeks) of the experiment under short days (SD; 8L:16D, winter‐like photoperiod) in which they were unstimulated and photosensitive SDSE, or exposed to long days (LD, 16L:8D, summer‐like photoperiod) in which following testicular maturation cycle they were photorefractory, LDRF (similar to post‐breeding condition; D. Singh et al, ).…”

“…We used testes from the experiment, as earlier described (Mishra, Singh, & Kumar, ; D. Singh, Trivedi, Rani, Panda, & Kumar, ). Briefly, adult male black‐headed buntings were maintained until the beginning (for about 40 weeks) of the experiment under short days (SD; 8L:16D, winter‐like photoperiod) in which they were unstimulated and photosensitive SDSE, or exposed to long days (LD, 16L:8D, summer‐like photoperiod) in which following testicular maturation cycle they were photorefractory, LDRF (similar to post‐breeding condition; D. Singh et al, ). Using three groups of photosensitive and one group of photorefractory birds, we reproduced all four critical testicular LHSs as follows (Figure a).…”

“…Thereafter, gene‐specific primers (Table ) were used for measurement of mRNA expression using SYBR green chemistry on Applied Biosystems StepOne Plus thermal cycler (Applied Biosystems, Foster City, CA). Both target and reference genes ( β‐actin ) were run in duplicates and relative mRNA expression levels were calculated by method (Livak & Schmittgen, ) as routinely done in our laboratory (Mishra, Singh, et al, Mishra, Bharadhwaj, et al, ; D. Singh et al, ). We first calculated Δ C t value as a difference between the threshold cycles ( C t ) of target and reference gene ( C t [target] − C t [reference] ).…”