Genetic basis of growth, spring phenology and susceptibility to biotic stressors in maritime pine

Forest ecosystems are increasingly challenged by extreme events, e.g.
drought, storms, pest and pathogenic fungi outbreaks, causing severe
ecological and economical losses. Understanding the genetic basis of
adaptive traits in tree species is of key importance to preserve forest
ecosystems, as genetic variation in a trait (i.e. heritability) determines
its potential for human-mediated or evolutionary change. Maritime pine
(Pinus pinaster Aiton), a conifer widely distributed in southwestern
Europe and northwestern Africa, grows under contrasted environmental
conditions promoting local adaptation. Genetic variation at adaptive
phenotypes, including height, growth phenology and susceptibility to two
fungal pathogens (Diplodia sapinea and Armillaria ostoyae) and an insect
pest (Thaumetopoea pityocampa), were assessed in a range-wide clonal
common garden of maritime pine. Broad-sense heritability was significant
for height (0.219), growth phenology (0.165-0.310) and pathogen
susceptibility (necrosis length caused by D. sapinea, 0.152; and by A.
ostoyae, 0.021) measured after inoculation under controlled conditions,
but not for pine processionary moth incidence in the common garden. The
correlations of trait variation among populations revealed contrasting
trends for pathogen susceptibility to D. sapinea and A. ostoyae with
respect to height. Taller trees showed longer necrosis length caused by D.
sapinea while shorter trees were more affected by A. ostoyae. Moreover,
maritime pine populations from areas with high summer temperatures and
frequent droughts were less susceptible to D. sapinea but more susceptible
to A. ostoyae. Finally, an association study using 4,227 genome-wide SNPs
revealed several loci significantly associated to each trait (range of
3-26), including a possibly disease-induced translation initiation factor,
eIF-5. This study provides important insights to develop genetic
conservation and breeding strategies integrating species responses to
biotic stressors.

森林生态系统正日益受到极端事件的严峻挑战，例如干旱、风暴、虫害及病原真菌暴发等，这些事件会造成严重的生态与经济损失。解析林木适应性性状的遗传基础，对于保护森林生态系统至关重要，因为某一性状的遗传变异（即遗传力）决定了其经人类干预或自然演化发生改变的潜力。马尾松（*Pinus pinaster* Aiton）是广泛分布于欧洲西南部与非洲西北部的针叶树种，其生长环境差异显著，推动了本地适应性演化。本研究在一项覆盖全分布区的马尾松无性系同质园试验（common garden）林中，对其适应性表型的遗传变异展开了评估，所涉表型包括树高、生长物候，以及对两种病原真菌（*Diplodia sapinea*与*Armillaria ostoyae*）和一种虫害（*Thaumetopoea pityocampa*）的感病性。在受控条件下接种后测定的性状中，树高（0.219）、生长物候（0.165~0.310）以及病原真菌感病性（由*D. sapinea*引发的坏死长度为0.152，由*A. ostoyae*引发的为0.021）的广义遗传力均达到显著水平，但同质园试验林中的松异舟蛾虫害发生率的遗传力未达显著水平。种群间的性状变异相关性分析显示，两种病原真菌的感病性与树高呈现相反的关联趋势：树高较高的个体受*D. sapinea*侵染引发的坏死长度更长，而树高较矮的个体则更易受*A. ostoyae*侵害。此外，来自夏季高温、干旱频发区域的马尾松种群对*D. sapinea*的感病性更低，但对*A. ostoyae*的感病性更高。最后，本研究依托4227个全基因组单核苷酸多态性（Single Nucleotide Polymorphisms, SNPs）开展关联分析，共鉴定出多个与各性状显著关联的基因座（数量范围为3~26），其中包括一个可能为病害诱导型翻译起始因子的eIF-5基因。本研究为制定兼顾物种对生物胁迫响应的遗传保护与育种策略提供了重要理论依据。