AFP-containing regions in the genome of C. fumiferana. (a) Graphic representation of C. fumiferana’s 30 chromosomes, in descending order of size; genes encoding CfAFPs were found on the two largest chromosomes, Chr. 1 (Z) and Chr. 18. (b) The AFP-containing region on Chr. 1 (Z) contains a single AFP gene, CfAFP-1 (red arrow). (c) The AFP-containing region on Chr. 18 contains the remaining 15 CfAFP genes (red arrows), one of which appears to be a pseudogene (CfAFP-10). Three small non-AFP genes (uncharacterized proteins; blue arrows; a, b, c) are located between CfAFP-3 and CfAFP-4. Loci are drawn to scale, with each arrow diagram representing both exons and introns of a gene. Arrows pointing in different directions represent genes found on opposite DNA strands.

The Spruce Budworm Genome: Reconstructing the Evolutionary History of Antifreeze Proteins

Catherine Béliveau, Patrick Gagné, Sandrine Picq, Oksana Vernygora, Christopher I. Keeling, Kristine Pinkney, Daniel Doucet, Fayuan Wen, J. Spencer Johnston, Halim Maaroufi, Brian Boyle, Jérôme Laroche, Ken Dewar, Nikoleta Juretic, Gwylim Blackburn, Audrey Nisole, Bryan Brunet, Marcelo Brandao, Lisa Lumley, Jun Duan, Guoxing Quan, Christopher J. Lucarotti, Amanda D. Roe, Felix A.H. Sperling, Roger C. Levesque, Michel Cusson

Genome Biology and Evolution, evac087

Insects have developed various adaptations to survive harsh winter conditions. Among freeze-intolerant species, some produce “antifreeze proteins” (AFPs) that bind to nascent ice crystals and inhibit further ice growth. Such is the case of the spruce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae), a destructive North American conifer pest that can withstand temperatures below -30°C. Despite the potential importance of AFPs in the adaptive diversification of Choristoneura, genomic tools to explore their origins have until now been limited. Here we present a chromosome-scale genome assembly for C. fumiferana, which we used to conduct comparative genomic analyses aimed at reconstructing the evolutionary history of tortricid AFPs. The budworm genome features 16 genes homologous to previously reported C. fumiferana AFPs (CfAFPs), 15 of which map to a single region on chromosome 18. Fourteen of these were also detected in five congeneric species, indicating Choristoneura AFP diversification occurred before the speciation event that led to C. fumiferana. Although budworm AFPs were previously considered unique to the genus Choristoneura, a search for homologs targeting recently sequenced tortricid genomes identified seven CfAFP-like genes in the distantly related Notocelia uddmanniana. High structural similarity between Notocelia and Choristoneura AFPs suggests a common origin, despite the absence of homologs in three related tortricids. Interestingly, one Notocelia AFP formed the C-terminus of a “zonadhesin-like” protein, possibly representing the ancestral condition from which tortricid AFPs evolved. Future work should clarify the evolutionary path of AFPs between Notocelia and Choristoneura and assess the role of the “zonadhesin-like” protein as precursor of tortricid AFPs.