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Chasing Clock-Controlled and Migratory Genes in the Monarch Butterfly Brain Using Omics
Abstract
Seasonal animal migration is a common adaptive response to environmental perturbations. However, the molecular processes in the brain regulating physiological and behavioral migratory traits are largely unknown. To address this, we investigated differential mRNA expression and their modes of regulation in different seasonal forms of the migratory monarch butterfly (Danaus plexippus). Every fall, monarchs migrate southward from the northern U.S. to their overwintering sites in Mexico. Exposure of migrants to overwintering coldness switches their flight orientation northward to remigrate back to the U.S in the spring, and their progeny and at least two successive generations will continue northward to complete the multigenerational migratory cycle. Both fall migrants and spring remigrants use a bidirectional sun compass for navigation that is time-compensated by circadian clocks. Because of the critical function of the circadian clock in migratory behavior, we applied RNA-seq and Assay for Transposase-Accessible Chromatin (ATAC)-seq from brains of wild-type and clock-deficient monarchs to identify clock-controlled genes (CCGs) and their regulatory factors. We found 217 CCGs, many of which are involved in biological processes key to brain function, such as glucose metabolism and neurotransmission, and showed that they are temporally regulated by candidate transcription factors (TFs) belonging to the bHLH, forkhead, HTH, and MADS TF families. The season-specific phenotypic differences in response to environmental changes in migrants and remigrants, which share virtually the same genomic background with their non-migratory parents, strongly suggest that epigenetic changes reprogram the transcriptional landscape in the monarch brain to regulate seasonal behavior. Focusing on flight orientation reversal, bulk and single-cell RNA-seq revealed a cold-induced down-regulation of integrins and integrin-related genes in immune-like cells in the brain, which may mediate extracellular matrix remodeling and synapse reorganization. Correlating the differential gene expression, particularly that of integrins and integrin-related genes, with differentially bound TF motifs detected in cis-regulatory elements by ATAC-seq and histone modifications profiled by chromatin immunoprecipitation (ChIP)-seq, could establish the epigenetic regulatory network in the brain driving cold-induced flight orientation reversal. The findings of our study could prove fundamental in understanding the molecular and cellular bases of seasonal flight orientation behavior in monarchs and in other migratory species.
Subject
monarchcircadian clock
migration
epigenetics
RNA-seq
ATAC-seq
ChIP-seq
integrin
single-cell RNA-seq
microglia
Citation
Lugena, Aldrin Benzon (2022). Chasing Clock-Controlled and Migratory Genes in the Monarch Butterfly Brain Using Omics. Doctoral dissertation, Texas A&M University. Available electronically from https : / /hdl .handle .net /1969 .1 /197976.