Photoperiodic induction of pre-migratory phenotype in a migratory songbird: identification of metabolic proteins in flight muscles

Abstract

Migratory birds need to undergo physiological changes during their preparation for migration. The current study characterized those changes in photoperiodic migratory black-headed buntings (Emberiza melanocephala), which initiate their northward spring migration in response to increasing day lengths. We measured differences in body mass, testis size and triglycerides levels in buntings between groups exposed to short (8 h light:16 h darkness, 8L:16D; SD) and long (16L:8D; LD) days, and identified proteins that showed significant differences between SD and LD in the flight muscle. To confirm that photostimulated changes were linked with migration, similar measurements were done on photoperiodic non-migratory Indian weaverbirds (Ploceus philippinus), which share the habitat with buntings for almost half-a-year. Buntings were fattened and gained weight and had elevated serum triglyceride levels and recrudesced testes under LD, but not SD. The SDS-polyacrylamide gel electrophoresis revealed differences between SD and LD conditions in the flight muscle protein profiles of buntings, but not of weaverbirds. Two-dimensional gel electrophoresis of flight muscle of bunting separated three proteins, of which two were upregulated under LD condition. Mass spectroscopic analysis and a protein database search identified them as the fatty acid binding protein (FABP), myoglobin and creatine kinase (CK). Further semi-quantitative and quantitative PCR assays revealed that FABP and myoglobin transcript levels in buntings, but not in weaverbirds, were upregulated under LD condition. However, there was no difference in CK mRNA levels between SD and LD in both the species. High FABP is perhaps linked with increased energy demands and high myoglobin with intense physical activity during migration. A difference in the CK protein, but not in mRNA levels between SD and LD may possibly indicate its photoperiodic regulation at the translational level.

Obese super athletes: fat-fueled migration in birds and bats

“…Transcriptomic and proteomic analyses provide unbiased assessments of changes in gene transcription and protein levels. Proteomic comparison of pectoralis muscles between non-migratory (short day) and migratory (long day) phenotypes of the black-headed bunting (Emberiza melanocephala) revealed significant upregulation of H-FABP, myoglobin and creatine kinase, and upregulation of H-FABP and myoglobin transcripts were also evident (Srivastava et al, 2014). Such changes did not occur in the Indian weaverbird (Ploceus philippinus), a full-year resident species (Srivastava et al, 2014).…”

“…Proteomic comparison of pectoralis muscles between non-migratory (short day) and migratory (long day) phenotypes of the black-headed bunting (Emberiza melanocephala) revealed significant upregulation of H-FABP, myoglobin and creatine kinase, and upregulation of H-FABP and myoglobin transcripts were also evident (Srivastava et al, 2014). Such changes did not occur in the Indian weaverbird (Ploceus philippinus), a full-year resident species (Srivastava et al, 2014). A proteomic analysis of the red-headed bunting revealed 24 proteins that were upregulated in the pre-migratory phase compared with non-migrants, and two proteins that were only expressed in premigrants (Banerjee and Chaturvedi, 2016).…”

Migration-induced variation of fatty acid transporters and cellular metabolic intensity in passerine birds

“…Intracellular fatty acid transport is mediated by cytosolic fatty acid binding protein (FABP c ) in skeletal muscles and heart (Guglielmo et al 1998;Liknes et al 2014). A few studies of migration and winter acclimatization show that increases in FABP c levels are consistent correlates of pre-migratory (Pelsers et al 1999;Srivastava et al 2014), migratory (Guglielmo et al 1998(Guglielmo et al , 2002McFarlan et al 2009;Price et al 2010), and winter phenotypes (Liknes et al 2014) in birds. Upon reaching the mitochondrion, carnitine palmitoyl transferase (CPT) mediates the transport of fatty acids across mitochondrial membranes (Guglielmo 2010; Price et al 2011;Swanson 2010).…”

Altered expression of pectoral myosin heavy chain isoforms corresponds to migration status in the white-crowned sparrow (Zonotrichia leucophrys gambelii)

“…training effect). Such finding suggests that these morphological changes may be controlled by a seasonally regulated mechanism similar to other preparatory processes, specifically those associated with the seasonal increase in photoperiod that occurs prior to spring migration [38,39,76]. Such distinctions across migratory species are of interest and deserve further investigation.…”

“…These stores are depleted over the course of the migration due to enhanced capacity for lipid transport to and oxidation within the flight muscles compared with non-migratory periods and species [14,15,37,38]. The seasonally driven changes in extracellular lipid stores and their importance for fuelling sustained flight is well established in many birds [14,16,19,34,38,39]; yet, as a primary site of lipid utilization [37,38], little is known about the role intramuscular lipid stores may play as birds prepare for and complete migration.…”