Genotypes of offspring from the RxS cross.

Elucidating the genomic architecture of quantitative traits is essential for our understanding of adaptation and for breeding in domesticated organisms. Penicillium roqueforti is the mold used worldwide for the blue cheese maturation, contributing to flavors through proteolytic and lipolytic activities. The two domesticated cheese populations display very little genetic diversity, but are differentiated and carry opposite mating types. We produced haploid F1 progenies from five crosses, using parents belonging to cheese and non-cheese populations. Analyses of high-quality genome assemblies of the parental strains revealed five large translocations, two having occurred via a circular intermediate, one with footprints of Starship giant mobile elements. Offspring genotyping with genotype-by-sequencing (GBS) revealed several genomic regions with segregation distortion, possibly linked to degeneration in cheese lineages. We found transgressions for several traits relevant for cheese making, with offspring having more extreme trait values than parental strains. We identified quantitative trait loci (QTLs) for colony color, lipolysis, proteolysis, extrolite production, including mycotoxins, but not for growth rates. Some genomic regions appeared rich in QTLs for both lipid and protein metabolism, and other regions for the production of multiple extrolites, indicating that QTLs have pleiotropic effects. Some QTLs corresponded to known biosynthetic gene clusters, e.g., for the production of melanin or extrolites. F1 hybrids constitute valuable strains for cheese producers, with new traits and new allelic combinations, and allowed identifying target genomic regions for traits important in cheese making, paving the way for strain improvement. The findings further contribute to our understanding of the genetic mechanisms underlying rapid adaptation, revealing convergent adaptation targeting major gene regulators.解析数量性状（quantitative traits）的基因组架构，对于理解生物适应性以及开展驯化生物的育种工作至关重要。娄地青霉（Penicillium roqueforti）是全球范围内用于蓝纹奶酪成熟发酵的工业霉菌，通过蛋白水解与脂解活性赋予奶酪独特风味。两个驯化的奶酪源种群遗传多样性极低，但彼此存在显著遗传分化，且携带相反的交配型。我们以奶酪源和非奶酪源种群的菌株作为亲本，通过5组杂交组合获得了单倍体F1后代群体。对亲本菌株的高质量基因组组装结果进行分析，共鉴定出5处大片段易位事件：其中2起通过环状中间体介导发生，1起带有星舰（Starship）型大型可移动遗传元件的序列足迹特征。通过测序分型（genotype-by-sequencing, GBS）技术对后代群体进行基因分型，发现多个基因组区域存在分离偏倚现象，该现象可能与奶酪源谱系的退化过程相关。我们还发现多个与奶酪生产相关的性状存在超亲分离现象，即后代的性状表型值较亲本菌株更为极端。我们成功鉴定出与菌落颜色、脂解活性、蛋白水解活性、外代谢物（extrolite）合成相关的数量性状位点（quantitative trait loci, QTLs），但未发现与生长速率相关的QTL。部分基因组区域同时富集脂类与蛋白质代谢相关的QTL，另有部分区域则调控多种外代谢物的合成，这表明QTL存在多效性效应。部分QTL对应已报道的生物合成基因簇，例如调控黑色素或外代谢物合成的基因簇。F1杂交菌株拥有全新的性状组合与等位基因搭配，可为奶酪生产商提供极具应用价值的生产菌株；同时本研究还鉴定出了与奶酪生产关键性状相关的基因组靶标区域，为后续菌株改良工作铺平了道路。本研究结果进一步加深了我们对生物快速适应性背后遗传机制的理解，揭示了靶向主效基因调控因子的趋同适应性演化模式。