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

Eric W Morrison,Jeff R Garnas,Jeremy J Heath,Matt T Kasson

doi:10.3389/ffgc.2021.673099

Abstract

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.

Highlights

Plant–microbe or plant–insect interactions are often considered in a pairwise manner with minimal consideration of the impacts of the broader community on the nature and outcomes of herbivory or pathogen attack
In the present study we explored the distribution of N. faginata and N. ditissima, the primary pathogens involved in beech bark disease (BBD), in relation to disease severity and climate characteristics in 10 sites across the range of BBD
This study explores new aspects of the fungal community ecology of the BBD system

Summary

Introduction

Plant–microbe or plant–insect interactions are often considered in a pairwise manner with minimal consideration of the impacts of the broader community on the nature and outcomes of herbivory or pathogen attack. In the most aggressive and well-studied examples (e.g., Chestnut blight, Dutch elm disease, or the more recent Emerald ash borer) disease agent aggressiveness and ensuing host mortality may be sufficiently rapid such that co-occurrence with other organisms is of minimal relevance to system dynamics. Though, even in these disease systems, colonization with certain endophytic microbes can influence host susceptibility (Feau and Hamelin, 2017) or pathogen aggressiveness (Kolp et al, 2020) in subtle or complex ways. The role of the community in determining host fate is extremely difficult to ascertain and could proceed via multiple, potentially interacting mechanisms (Table 1)

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