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

ABSTRACT: 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.

SUBMITTER: Beliveau C

PROVIDER: S-EPMC9210311 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Antifreeze proteins are important antifreeze materials that have been widely used in industry, including in cryopreservation, de-icing, and food storage applications. However, the quantity of some commercially produced antifreeze proteins is insufficient for large-scale industrial applications. Further, many antifreeze proteins have properties such as cytotoxicity, severely hindering their applications. Understanding the mechanisms underlying the protein-ice interactions and identifying novel antifreeze proteins are, therefore, urgently needed. In this study, to uncover the mechanisms underlying protein-ice interactions and provide an efficient and accurate tool for identifying antifreeze proteins, we assessed various evolutionary features based on position-specific scoring matrices (PSSMs) and evaluated their importance for discriminating of antifreeze and non-antifreeze proteins. We then parsimoniously selected seven key features with the highest importance. We found that the selected features showed opposite tendencies (regarding the conservation of certain amino acids) between antifreeze and non-antifreeze proteins. Five out of the seven features had relatively high contributions to the discrimination of antifreeze and non-antifreeze proteins, as revealed by a principal component analysis, i.e., the conservation of the replacement of Cys, Trp, and Gly in antifreeze proteins by Ala, Met, and Ala, respectively, in the related proteins, and the conservation of the replacement of Arg in non-antifreeze proteins by Ser and Arg in the related proteins. Based on the seven parsimoniously selected key features, we established a classifier using support vector machine, which outperformed the state-of-the-art tools. These results suggest that understanding evolutionary information is crucial to designing accurate automated methods for discriminating antifreeze and non-antifreeze proteins. Our classifier, therefore, is an efficient tool for annotating new proteins with antifreeze functions based on sequence information and can facilitate their application in industry.

Project description:In Canada, new forestry practices involving the natural dynamics of tree growth and regeneration are proposed for integrating forest management with biodiversity. In particular, the current spruce budworm [Choristoneura fumiferana (Clemens)] outbreak in northeastern North America is forcing natural resource managers to clarify the potential interactions between natural disturbances and commercial thinning. The aim of this study was to investigate if the spruce budworm outbreak of the 1970s affected the responses of black spruce [Picea mariana (Mill.) B.S.P.] to a subsequent thinning. Stem growth was reconstructed by measuring and cross-dating chronologies of tree-ring width of 1290 adult trees from 34 control and thinned stands within an area of 11,000 km2 in the boreal forest of the Saguenay-Lac-Saint-Jean region (QC, Canada). The treatment consisted of a low thinning performed during 1995-1999 that removed 25-35% of the basal area. Segmented models were applied to the tree-ring chronologies to define the growth pattern during the outbreak and thinning periods within a time window of 8 years, representing the average duration of the effects of defoliation on growth. Trees showed abrupt growth decreases during the outbreak, with the tree-ring index showing minimum values in 1977-1979. The tree-ring index had a flat trend before thinning, while it increased for 6-10 years after thinning. The growth pattern during the outbreak period was characterized by a reduction, mainly in trees with larger tree rings, while slow-growing trees showed less sensitivity to the disturbance. Thinning produced a significant increase in tree growth. No relationship was found between the effects of spruce budworm outbreaks in trees and the changes in growth pattern after thinning. If the timespan between the two disturbances exceeds 7 years, partial cutting can be applied independently of the growth reductions that had occurred during the outbreak. When applied in black spruce stands with high annual radial growth, thinning is expected to optimize the volume growth of the residual trees.

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

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