Table_1_Pathogen and Endophyte Assemblages Co-vary With Beech Bark Disease Progression, Tree Decline, and Regional Climate.DOCX

Plant–pathogen interactions are often considered in a pairwise manner with minimal consideration of the impacts of the broader endophytic community on disease progression and/or outcomes for disease agents and hosts. Community interactions may be especially relevant in the context of disease complexes (i.e., interacting or functionally redundant causal agents) and decline diseases (where saprobes and weak pathogens synergize the effects of primary infections and hasten host mortality). Here we describe the bark endophyte communities associated with a widespread decline disease of American beech, beech bark disease (BBD), caused by an invasive scale insect (Cryptococcus fagisuga) and two fungal pathogens, Neonectria faginata and N. ditissima. We show that the two primary fungal disease agents co-occur more broadly than previously understood (35.5% of infected trees), including within the same 1-cm diameter phloem samples. The two species appear to have contrasting associations with climate and stages of tree decline, wherein N. faginata was associated with warmer and N. ditissima with cooler temperatures. Neonectria ditissima showed a positive association with tree crown dieback – no such association was observed for N. faginata. Further, we identify fungal endophytes that may modulate disease progression as entomopathogens, mycoparasites, saprotrophs, and/or additional pathogens, including Clonostachys rosea and Fusarium babinda. These fungi may alter the trajectory of disease via feedbacks with the primary disease agents or by altering symptom expression or rates of tree decline across the range of BBD.

植物-病原物互作的研究通常采用两两配对的模式，极少关注更广泛的内生菌群落（endophytic community）对病害进展，以及病原物与宿主的病害结局的影响。群落互作在病害复合群（即存在互作或功能冗余的致病原）以及衰退型病害（其中腐生菌与弱致病菌协同增强初侵染的危害，加速宿主死亡）的研究中尤为关键。

本研究针对由入侵性介壳虫（Cryptococcus fagisuga）与两种真菌病原物Neonectria faginata和N. ditissima共同引发的广泛发生的美洲山毛榉衰退病害——山毛榉树皮病（BBD），描述了与之相关的树皮内生菌群落。

研究表明，两种主要真菌病原物的共存范围远超此前认知，在35.5%的感病树木中均可检测到二者共存，甚至可同时存在于同一直径1厘米的韧皮部样本中。两种病原物与气候条件及树木衰退阶段呈现出截然不同的关联：Neonectria faginata与较高温度呈正相关，而N. ditissima则偏好较低温度。Neonectria ditissima与树木冠层枯梢呈显著正相关，而Neonectria faginata未表现出此类关联。

此外，本研究还鉴定出一批可通过昆虫病原、重寄生、腐生或作为额外病原物等方式调控病害进展的内生真菌，包括Clonostachys rosea和Fusarium babinda。这些真菌可通过与主要病原物的互作反馈，或通过改变病害症状表现、全分布范围内山毛榉树皮病的树木衰退速率，来改变病害的发展轨迹。