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Differences in transcription regulation of diurnal metabolic support to physiologically contrasting seasonal life-history states in migratory songbirds

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Abstract

We hypothesized that there were diurnal differences in metabolism, with major transcriptional changes occurring early during the day and/or night between migratory and non-migratory states of avian migrants. Present study investigated this in captive Black-headed Buntings (Emberiza melanocephala) exhibiting long-day stimulated vernal migratory and post-breeding non-migratory states, by using RNA-Seq and qPCR assays of liver samples collected at 1 h into day (hour 1) and 1 h into night (hour 17) of the 16-h photoperiod (16L:8D). There were differentially expressed genes (DEGs) both within (day vs. night) and between (vernal migratory vs. non-migratory) states. Within the state, 358 and 52 DEGs were identified in migratory and non-migratory states, respectively. In the migratory state, genes associated with oxidative phosphorylation (sdh) had higher expression, and genes associated with fat metabolism (acaca and elovl6) and ABC transporters (abcg5, abcg8) had lower expression at night, compared to the daytime. In the non-migratory state, among genes associated with fat metabolism and gluconeogenesis, ppara and hmgcl had higher while aacs had lower expression at night. Between states, 35 and 180 DEGs were identified in day and night, respectively, with highly expressed genes associated with fat metabolism (acsbg2, cetp) found in migratory, and those associated with cell death (casp7), gluconeogenesis (stat3) and circadian rhythm pathway (cry1) in the non-migratory state. These results demonstrate differentially activated hepatic molecular pathways during photostimulated vernal migratory and post-breeding non-migratory states of buntings and provide molecular insights into differential metabolic support to physiologically contrasting seasonal life-history states in migratory songbirds.

Zusammenfassung

Unterschiede in der Transkriptionsregulierung im Tagesgang des Stoffwechsels innerhalb der physiologisch und jahreszeitlich bedingten Lebensphasen ziehender Singvögel

Wir stellten die Hypothese auf, dass es zwischen Zugvögeln und Standvögeln tageszeitliche Stoffwechsel-Unterschiede gibt, bei denen größere Transkriptionsveränderungen früh am Tag und/oder in der Nacht auftreten. In der vorliegenden Studie wurde dies bei in Gefangenschaft gehaltenen Kappenammern (Emberiza melanocephala) in durch Langtage stimulierter Frühjahrszug-Aktivität und in der zugfreien Zeit nach dem Brüten untersucht. Dazu wurden RNA-Seq- und qPCR-Tests an Leberproben durchgeführt, die um 1 Uhr am Tag (Stunde 1) und um 1 Uhr in der Nacht (Stunde 17) während einer 16-stündigen Photoperiode (16L:8D) entnommen wurden. Es gab unterschiedlich exprimierte Gene (DEGs) sowohl innerhalb (Tag vs. Nacht) als auch zwischen einzelnen Phasen (Frühjahrszug vs. stationär). Innerhalb der jeweiligen Phase wurden 358 DEGs bei Ziehenden und 52 DEGs bei Nicht-Ziehenden identifiziert. Während des Ziehens hatten mit der oxidativen Phosphorylierung (sdh) verbundene Gene eine höhere Expression; Gene, die mit dem Fettstoffwechsel (acaca und elovl6) und den ABC-Transportern (abcg5, abcg8) zusammenhängen, zeigten nachts eine geringere Expression als am Tag. Außerhalb der Zugzeit hatten von denjenigen Genen, die mit dem Fettstoffwechsel und der Gluconeogenese in Verbindung stehen, ppara und hmgcl nachts eine höhere, aacs eine niedrigere Expression. Zwischen den jeweiligen Phasen wurden am Tag 35 und in der Nacht 180 DEGs identifiziert, wobei während des Ziehens hoch exprimierte Gene im Zusammenhang mit dem Fettstoffwechsel (acsbg2, cetp) gefunden wurden und zwischen den Zugzeiten solche, die mit dem Zelltod (casp7), der Gluconeogenese (stat3) und dem circadianen Rhythmus (cry1) in Verbindung stehen. Diese Ergebnisse zeigen, dass bei Ammern die molekularen Stoffwechselwege in der Leber während des photoperiodisch stimulierten Frühjahrszuges und in der Zeit nach dem Brüten unterschiedlich aktiviert werden. Sie geben ferner molekulare Einblicke in die unterschiedliche Stoffwechselunterstützung in den physiologisch unterschiedlichen, jahreszeitlich bedingten Lebensphasen ziehender Singvögel.

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Availability of data and materials

The RNA-Seq data are accessible from the NCBI Gene Expression Omnibus repository (#GSE104748). The Genbank accession numbers to access the gene sequences are given in Table S2.

Code availability

Not applicable.

Abbreviations

aacs :

Acetoacetyl-coA synthetase

acaca :

Acetyl-coA carboxylase 1

acot7 :

Acyl-coenzyme A thioesterase 7

acsbg2 :

Acyl-coA synthetase bubblegum family member 2

casp7 :

Caspase-7

cetp :

Cholesteryl ester transfer protein

cry1 :

Cryptochrome 1

cs :

Citrate synthase

elovl6 :

Elongation of long-chain fatty acids family member 6

gpx4 :

Glutathione peroxidase 4

hmgcl :

3-Hydroxy-3-methyl-glutaryl CoA lyase

nM:

Photorefractory (post-breeding) non-migratory state

pck1 :

Phosphoenolpyruvate carboxykinase 1

ppara :

Peroxisome proliferator-activated receptor alpha

sdh :

Succinate dehydrogenase

stat3 :

Signal transducer and activator of transcription 3

tmem :

Transmembrane protein

vM:

Photostimulated vernal (spring) migratory state

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Funding

The work was supported by the Department of Biotechnology [BT/PR4984/MED/30/752/2012], New Delhi, to VK; AS received a CSIR fellowship.

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Authors and Affiliations

  1. Department of Zoology, University of Delhi, Delhi, 110 007, India

    Aakansha Sharma, Subhajit Das, Devraj Singh & Vinod Kumar

  2. Department of Zoology, University of Lucknow, Lucknow, 226 007, India

    Sangeeta Rani

Authors
  1. Aakansha Sharma
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  2. Subhajit Das
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  3. Devraj Singh
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  4. Sangeeta Rani
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  5. Vinod Kumar
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Contributions

VK: conceived the idea; DS and SR: experiment—monitoring of activity behaviour and collecting liver samples; AS and SD: transcriptome analysis; AS: qPCR assays; AS and VK: Analyses and preparation of figures; VK and AS: Wrote the paper. VK: Resources including funding.

Corresponding author

Correspondence to Vinod Kumar.

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Ethical approval

This study was performed as per approval of the Institutional Animal Ethics Committee experiment of the Department of Zoology, University of Lucknow, Lucknow, India (LU/ZOOL/IRPHA/Protocol2.3/NOV07).

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Communicated by I. Moore.

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Sharma, A., Das, S., Singh, D. et al. Differences in transcription regulation of diurnal metabolic support to physiologically contrasting seasonal life-history states in migratory songbirds. J Ornithol 163, 199–212 (2022). https://doi.org/10.1007/s10336-021-01926-5

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