Testing the ‘Hybrid Susceptibility’ and ‘Phenological Sink’ Hypotheses Using the P. balsamifera – P. deltoides Hybrid Zone and Septoria Leaf Spot [Septoria musiva]

Hybrid genotypes that arise between plant species frequently have increased susceptibility to arthropod pests and fungal pathogens. This pattern has been attributed to the breakdown of plant defenses (‘Hybrid susceptibility’ hypothesis) and (or) to extended periods of susceptibility attributed to plant phenologies in zones of species overlap and (or) hybridization (‘phenological sink’ hypothesis). We examined these hypotheses by assessing the susceptibility of parental and hybrid Populus host genotypes to a leaf spot disease caused by the fungal pathogen Septoria musiva. For this purpose, 214 genotypes were obtained from morphologically pure zones of P. balsamifera and P. deltoides, and from an intervening zone of overlap and hybridization on the drainage of the Red Deer River, Alberta, Canada. Genotypes were identified as P. balsamifera, P. deltoides, or hybrid using a suite of 27 species-specific SNP markers. Initially the genetic structure of the hybrid zone was characterized with 27.7% of trees classified as admixed individuals. To test the hybrid susceptibility hypothesis, a subset of 52 genotypes was inoculated with four isolates of S. musiva. Levels of susceptibility were P. balsamifera > F1 hybrid > P. deltoides. A further 53 genotypes were grown in a common garden to assess the effect of genotype on variation in leaf phenology. Leaf phenology was more variable within the category of hybrid genotypes than within categories of either parental species. Leaf phenology was also more variable for the category of trees originating in the hybrid (P. balsamifera – P. deltoides [hybrid and parental genotypes combined]) zone than in adjacent pure zones of the parental species. The results from the inoculation experiment support the hybrid intermediacy hypothesis. The results from the common garden experiment support the ‘phenological sink’ hypothesis. These findings have greatly increased our understanding of the epidemiology and ecology of fungal pathogens in plant hybrid zones.植物物种间杂交产生的杂种基因型，通常对节肢动物害虫及真菌病原菌的易感性显著提升。这一现象可归因于两类机制：一是植物防御体系的崩溃（即“杂种易感性（Hybrid Susceptibility）”假说），二或为由物种重叠区与杂交带中植物物候期引发的易感性持续延长（即“物候汇（Phenological Sink）”假说）。本研究以杨属（Populus）宿主为材料，通过评估其亲本与杂种基因型对真菌病原菌杨生壳针孢（Septoria musiva）引发的叶斑病的易感性，对上述两项假说进行检验。实验材料取自加拿大阿尔伯塔省雷德迪尔河流域的美洲杨（P. balsamifera）、三角杨（P. deltoides）的纯形态分布区，以及二者重叠杂交的过渡带，共获取214份基因型材料。研究团队利用一套包含27个物种特异性单核苷酸多态性（Single Nucleotide Polymorphism，SNP）的标记组合，将所有基因型材料鉴定为美洲杨、三角杨或杂种。初步表征该杂交带的遗传结构后发现，27.7%的个体为遗传混杂型。为检验杂种易感性假说，研究人员选取52份基因型材料，采用4株杨生壳针孢分离株开展接种实验。实验结果显示，宿主的易感性水平由高到低依次为：美洲杨 > F1杂种 > 三角杨。另有53份基因型材料被种植于同质种植园（Common Garden）中，用以评估基因型对叶物候变异的影响。相较于两个亲本物种类群，杂种基因型类群内的叶物候变异程度更高；且相较于相邻的亲本纯合分布区，源自杂交带（美洲杨-三角杨[杂种与亲本基因型合并类群]）的树木类群，其叶物候变异程度同样更为显著。接种实验的结果支持“杂种中间易感性（Hybrid Intermediacy）”假说，而同质种植园实验的结果则支持“物候汇（Phenological Sink）”假说。上述研究结果极大地加深了我们对植物杂交带中真菌病原菌流行学与生态学的认知。