Genome-wide association study of morphometric and metabolic characteristics in the European populations of the sugar kelp Saccharina latissima

Abstract The sugar kelp Saccharina latissima is a promising candidate for sustainable aquaculture in the North Atlantic and North-East Pacific but genetic improvement has been hindered by limited understanding of the genetic basis of economically important traits. We conducted the first genome-wide association study (GWAS) for this species using 202 self-fertilised pseudo-F1 individuals derived from 12 populations spanning northern and southern European genetic clusters. Individuals were genotyped with ddRAD-seq-derived SNP markers and phenotyped in a common garden experiment for four morphological traits (blade length, blade width, blade area, stipe length) and six metabolic traits related to nitrogen metabolism. We identified 26 significant marker-trait associations, with phenotypic variance explained (PVE) ranging from 0.65% to 52.44%. Major-effect loci were detected for blade width (52.44% PVE) and blade area (45.22% PVE) and a locus on chromosome 17 influenced both blade length and blade area. Marker-based heritability estimates ranged from 0.75 to 0.99 for morphological traits and from 0.00 to 0.99 for metabolic traits, though with large standard errors. Cross-validation of genomic selection models yielded predictive abilities of 0.21-0.59 across traits. Our findings reveal a mixed genetic architecture with major-effect loci suitable for marker-assisted selection and polygenic traits amenable to genomic selection, providing a foundation for genomics-assisted breeding programs in kelp aquaculture. Competing Interest Statement The authors have declared no competing interest. Footnotes ↵* Joint first authors ↵$ Author for correspondence Credit authorship contribution statement Stéphane Mauger: Writing - original draft (equal), Writing - review & editing (equal), Investigation (equal), Formal analysis (equal), Data curation (equal). Komlan Avia: Writing - original draft (equal), Writing - review & editing (equal), Investigation (equal), Formal analysis (equal), Conceptualization (equal). Lucie Jaugeon: Writing-review& editing (equal), Investigation (equal), Formal analysis (equal). Paolo Ruggeri: Writing - review & editing (equal), Investigation (equal), Formal analysis (equal). Zofia Nehr: Writing - review & editing (equal), Investigation (equal), Visualization (equal). Ousseini Issaka Salia: Writing - review & editing (equal), Investigation (supporting). Jérôme Coudret: Writing - review & editing (supporting), Investigation (equal). Emilie Gouhier: Writing - review & editing (supporting), Investigation (equal). Aurélien Baud: Writing - review & editing (supporting), Investigation (equal). Stéphane Loisel: Writing - review & editing (supporting), Investigation (equal). Antoine Fort: Writing - review & editing (equal), Investigation (equal), resource (equal). Ronan Sulpice: Writing - review & editing (equal), resource (equal), Supervision (equal). Christophe Destombe: Writing - original draft (supporting), Writing - review & editing (equal), Investigation (equal), Supervision (equal). Philippe Potin: Writing - review & editing (equal), Supervision (equal), Project administration (equal), Data curation (equal). J. Mark Cock: Writing - review & editing (equal), Supervision (equal), Project administration (equal), Investigation (equal), Conceptualization (equal). Myriam Valero: Writing - original draft (supporting), review & editing (equal), Supervision (equal), Project administration (equal), Investigation (equal), Data curation (equal), Conceptualization (equal). Abbreviations - Â - allelic richness - AFLP - amplified fragment length polymorphism ANOVA analysis of variance - ATPase - adenosine 5’-TriPhosphatase COI cytochrome-oxydase I - DAPC - discriminant analysis of principal components - ddRAD-seq - double digest restriction-site associated DNA sequencing DEGs differentially expressed genes - EM - Expectation-maximization - eQTL - expression quantitative trait loci - EST - expressed-sequence-tag - FAO - Food and Agriculture Organization - FIS - inbreeding coefficient - FST - fixation index (differentiation among populations) GLM generalized linear model - GS - genomic selection - guanosine-5’-triphosphate - GWAS - genome-wide association study He expected heterozygosity - HN4+ - ammonium - IMTA - integrated multi-trophic aquaculture LD linkage disequilibrium - MAF - minor allele frequency - MAS - marker-assisted selection - NAD+ - nicotinamide adenine dinucleotide oxidized form NADH nicotinamide Adenine Dinucleotide - NO2 - nitrogen dioxide - NO3- - nitrate - PÂ - private allele - PCA - principal component analysis - PES - Provasoli enriched seawater - PVE - phenotypic variance explained - QTL - quantitative trait loci - SLAF-seq - specific locus amplified fragment sequencing SNP single nucleotide polymorphisms - SSR - simple sequence repeats - VCF - variant call format