Linking Tree Health, Rhizosphere Physicochemical Properties, and Microbiome in Acute Oak Decline

Abstract

Forest decline diseases are complex processes driven by biotic and abiotic factors. Although information about host–microbiome–environment interactions in agricultural systems is emerging rapidly, similar studies on tree health are still in their infancy. We used acute oak decline (AOD) as a model system to understand whether the rhizosphere physicochemical properties and microbiome are linked to tree health by studying these two factors in healthy and diseased trees located in three sites in different AOD stages—low, mid and severe. We found significant changes in the rhizosphere properties and microbiome composition across the different AOD sites and between the tree health conditions. Rhizosphere pH correlated with microbiome composition, with the microbial assemblages changing in more acidic soils. At the severe AOD site, the oak trees exhibited the lowest rhizosphere pH and distinct microbiome, regardless of their health condition, whereas, at the low and mid-stage AOD sites, only diseased trees showed lower pH and the microbial composition differed significantly from healthy trees. On these two sites, less extreme soil conditions and a high presence of host-beneficial microbiota were observed in the healthy oak trees. For the first time, this study gathers evidence of associations among tree health conditions, rhizosphere properties and microbiome as well as links aboveground tree decline symptoms to the belowground environment. This provides a baseline of rhizosphere community profiling of UK oak trees and paves the way for these associations to be investigated in other tree species suffering decline disease events.

Evidence for the Widespread Occurrence of Bacteria Implicated in Acute Oak Decline from Incidental Genetic Sampling

“…Our analysis of the abundance of Acute Oak Decline-associated bacteria showed differences between the geographical sites. This is in line with a study of the oak rhizosphere, which found differences in the bacterial composition of the root microbiome between sites [13]. It is also in line with phyllosphere studies on other tree species, reviewed by Rastogi et al [61] in which geographical location has been shown to be a driver of bacterial community composition.…”

Evidence for the Widespread Occurrence of Bacteria Implicated in Acute Oak Decline from Incidental Genetic Sampling

“…Affected sites are more likely to be found in warmer areas of Britain and areas of low rainfall [11,12]. Soil pH, and the rhizosphere microbiome, have been found to differ between symptomatic and asymptomatic trees at some sites [13,14]. A study that included Hatchlands Park and Sheen Wood (both of which are studied here, see below) found that the bacterial composition of the rhizosphere differed between sites and tree health conditions [13].…”

Global challenges facing plant pathology: multidisciplinary approaches to meet the food security and environmental challenges in the mid-twenty-first century

“…Disease can then be considered as arising from a perturbation of a healthy microbiome. The plant microbiome has received much attention over the last decade (Mercado-Blanco et al 2018;Baldrian 2019;Vonaesch et al 2018), in both food crops (Ding et al 2019) and forest trees (Feau and Hamelin 2017;Koskella et al 2017;Pinho et al 2020). It has long been recognized that plant-associated microbiomes, the phytobiome (e.g., the phyllosphere, endophyte, and rhizosphere microbiome), will affect directly and/or indirectly disease development (Glaeser et al 2019;Martin et al 2019;Rabiey et al 2019;Tsolakidou et al 2019).…”