Unique bacterial assembly, composition, and interactions in a parasitic plant and its host.

Adam C Schneider,Connor R Fitzpatrick,Robert Hancock

doi:10.1093/jxb/erz572

Abstract

How plant-associated microbiota are shaped by, and potentially contribute to, the unique ecology and heterotrophic life history of parasitic plants is relatively unknown. Here, we investigate the leaf and root bacterial communities of the root holoparasite Orobanche hederae and its host Hedera spp. from natural populations. Root bacteria inhabiting Orobanche were less diverse, had fewer co-associations, and displayed increased compositional similarity to leaf bacteria relative to Hedera. Overall, Orobanche bacteria exhibited significant congruency with Hedera root bacteria across sites, but not the surrounding soil. Infection had localized and systemic effects on Hedera bacteria, which included effects on the abundance of individual taxa and root network properties. Collectively, our results indicate that the parasitic plant microbiome is derived but distinct from the host plant microbiota, exhibits increased homogenization between shoot and root tissues, and displays far fewer co-associations among individual bacterial members. Host plant infection is accompanied by modest changes of associated microbiota at both local and systemic scales compared with uninfected individuals. Our results are a first step towards extending the growing insight into the assembly and function of the plant microbiome to include the ecologically unique but often overlooked guild of heterotrophic plants.

Highlights

IntroductionPlants harbor rich assemblages of microorganisms, which vary in diversity and composition across host plant tissues, individuals, and species (Bulgarelli et al, 2013).This variation is driven by edaphic features including the regional pool of soil microorganisms (Liu et al, 2019), as well as innate plant immunity (Lebeis et al, 2015; Stringlis et al, 2018), the quality and quantity of plant-derived resources (Zhalnina et al, 2018), and microbe–microbe interactions (Agler et al, 2016; Durán et al., 2018; Carlström et al, 2019)
Similar to other root holoparasites, O. hederae seeds germinate in the presence of a suitable host plant and the seedling immediately attaches to a single host root, where it persists for the remainder of its life (Joel et al, 2013)
Orobanche and Hedera differed in the composition of both leaf and root bacteria (Fig. 2B, C).Variation in functional traits and ecological strategies among plants are thought to contribute to differences in leaf and root microbiota among plant species (Kembel et al, 2014; Laforest-Lapointe et al, 2016; Fitzpatrick et al, 2018)

Summary

Introduction

Plants harbor rich assemblages of microorganisms, which vary in diversity and composition across host plant tissues, individuals, and species (Bulgarelli et al, 2013).This variation is driven by edaphic features including the regional pool of soil microorganisms (Liu et al, 2019), as well as innate plant immunity (Lebeis et al, 2015; Stringlis et al, 2018), the quality and quantity of plant-derived resources (Zhalnina et al, 2018), and microbe–microbe interactions (Agler et al, 2016; Durán et al., 2018; Carlström et al, 2019). Angel et al, 2016; Coleman-Derr et al, 2016; Finkel et al, 2016) Such an investigation provides an opportunity to address how associated microbiota are shaped by, and potentially contribute to, the functional diversity found across plant species. A subset of these are holoparasites, meaning that they rely exclusively on one or more hosts for resources This life history shift has been accompanied by dramatic ecological and physiological shifts such as the complete loss of photosynthetic function, as well as morphological and genomic changes collectively referred to as ‘parasitic reduction syndrome’ (Colwell et al, 1994). Very few studies have investigated changes induced in the composition and assembly of parasitic plant-associated microbial communities (Kruh et al, 2017) in spite of the mounting evidence that such communities are crucial for plant function and fitness (Vogel et al, 2016; Castrillo et al, 2017; Fitzpatrick et al, 2018)

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Conclusion