Introduction

Plant galls are the growth of abnormal plant tissue induced by other organisms (e.g. viruses, bacteria, fungi, nematodes or insects) and are found on many plant species. Insect-induced plant galls impact plant development by triggering morphological and physiological changes in the host plant tissues. Oviposition in leaf tissues initiates these cellular modifications through changes in plant development pathways, nutrient concentrations, the disruption of plant defence, selection for gall induction traits and the advent of insect-derived effectors (Giron et al., 2016; Oates et al., 2021). Plant tissues stressed in such a way, potentially also change the conditions for the colonisation or proliferation of co-existing organisms, including foliar fungi.

It is well known that fungal community diversity and the colonisation of plant host niches are influenced by abiotic, microbial and host factors (e.g. Bálint et al., 2013; Kemen, 2014; Vivas et al., 2017; Gomes et al., 2018). A clear difference between the fungal communities of healthy and yellowing Citrus limon leaves, where yellowing leaves had the least species diversity, exemplifies the influence of plant physiology on microbial community patterns (Douanla-Meli et al., 2013). It must therefore be assumed that galls, which function as metabolic sinks (Allison and Schultz, 2005; Dardeau et al., 2014), also influence fungal community diversity. Some studies indeed show that fungal communities in galls are different than in the surrounding leaf tissue. Cultivated fungal communities associated with aphid-induced galls in cottonwood (Populus deltoides) for instance exhibit distinct fungal richness and diversity in galls compared to the surrounding tissues (Lawson et al., 2014). A metabarcoding study of fungal communities showed differences in richness, diversity and composition between galls induced by Dryocosmus kuriphilus and surrounding chestnut leaf tissues (Fernandez-Conradi et al., 2019). Whether different levels of severity of gall formation affect the fungal community in surrounding healthy tissue is, however, not known.

Eucalyptus plantations are of high economic value globally (Wingfield et al., 2015). In recent years, their yield has been jeopardised by the gall-forming wasp Leptocybe invasa Fisher and LaSalle (Hymenoptera: Eulophidae), which deposits eggs into new growth of Eucalyptus trees (Naidoo et al., 2011; Dittrich-Schröder et al., 2018; Mhoswa et al., 2020). A high density of L. invasa can cause heavy galling, malformation, stunted growth and in extreme cases, tree death (Mendel et al., 2004; Zheng et al., 2014; Csóka et al., 2017). The egg oviposition into the Eucalyptus spp. leaf tissues initiates the expression of pathogen-related genes by the host and localised cell death causing desiccation, detachment or is directly ovicidal (Geuss et al., 2017; Griese et al., 2017). Within 24 h after oviposition, Eucalyptus spp. tissues accumulate reactive oxygen species and phenolics, as well as phytohormones (especially jasmonic acid, salicylic acid and ethylene) as a defence against biotic stress (Berens et al., 2017). The egg and oviposition fluid may redirect the hosts’ responses towards gall development (e.g. cell division) and is thus responsible for initiating galling (Oates et al., 2021). Gall-forming insects are also known to modify the availability of sugars, lipids and proteins in the nutritive tissue of the gall chamber (Huang et al., 2014; Ferreira et al., 2015). A study on the influence of L. invasa gall development on frost resistance in eucalypts found that the physiological changes on the plant foliage increased plant defence mechanisms against cold. The toll of galling by herbivores may thus have a positive indirect effect on the host plant (Rocha et al., 2013).

Fungal diversity associated with healthy and diseased Eucalyptus spp. has been explored for several decades (e.g. Bird et al., 1974; Bettucci and Alonso, 1997; Barbed et al., 2003; Roux et al., 2003; Hunter et al., 2011; Márquez et al., 2011; Jimu et al., 2015). The recent application of high-throughput sequencing of fungal-specific PCR amplicons has revealed enormous species diversity and richness in Eucalyptus spp. (Kemler et al., 2013). Such studies have identified potential pathogens existing in the fungal community of trees without visible symptoms of disease or decay. Additionally, community patterns have been shown to be highly dependent on environmental factors, as well as maternal effects that could influence the formation of fungal communities in seedlings (Vivas et al., 2017). With increasing L. invasa infestations in plantations (Hurley et al., 2016; Dittrich-Schröder et al., 2018), it is important to understand its influence on the associated fungal community and whether the added stress increases the occurrence of potentially pathogenic fungi.

In this study, we analysed fungal community diversity, composition and co-occurrence network structures in E. grandis trees with different levels of L. invasa infestation. We aimed to answer three questions: (i) Do L. invasa infestation levels correlate with fungal community diversity and composition in surrounding healthy leaf tissue?; (ii) Do co-occurrence patterns of fungal taxa correlate with L. invasa infestation?; and (iii) Do increased L. invasa infestation levels lead to an increased abundance of potential Eucalyptus pathogens?

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Source: FABI
Original Source: Frontiers in Microbiology