Plant phylogeny, traits and fungal community composition as drivers of plant–soil feedbacks

Abstract

1 INTRODUCTION

Plant–soil feedbacks (PSFs) are a key component of terrestrial ecosystem functioning and influence vegetation dynamics in many ways, such as: the maintenance of species coexistence (Crawford et al., 2019; Klironomos, 2002; Teste et al., 2017), plant invasiveness (Aldorfová et al., 2020; Levine et al., 2006) and successional changes in plant community composition (Bauer et al., 2015; Kardol et al., 2006). PSFs involve the modification of soil biological and abiotic properties by a given plant species that have downstream effects on the growth of future individuals in the same soil. These PSFs can be positive, negative or neutral, where plant performance is improved, reduced or unaffected, respectively, when grown in soil previously occupied by the same species compared with soil conditioned by other species (Bever et al., 1997; Van der Putten et al., 2013). Given this wide variation in PSF observed among species, there is considerable interest in developing a framework that can be used to predict the direction and magnitude of PSF responses as a function of plant species characteristics (de Vries et al., 2023; Rutten & Allan, 2023; Semchenko et al., 2022). However, despite an abundance of studies exploring individual aspects of PSFs, our understanding of how plant traits and phylogeny, via associated effects on soil microbial communities, shape PSFs is still limited by the lack of comprehensive empirical tests.

Plants modify their immediate environment in many ways and can shape the composition and diversity of microbial communities within their root zones (Grayston et al., 1998; Hu et al., 2018). This ‘conditioning’ of rhizosphere microbial communities can regulate PSFs, and, as such, PSF responses may be predictable based upon how a particular plant species modifies its root-associated microbiome (Fitzpatrick et al., 2018; Semchenko et al., 2018; Wilschut et al., 2019). Previous studies indicate that root-associated fungi, especially arbuscular mycorrhizal fungi (AMF) and fungal pathotrophs, play an important role in determining PSFs (Cortois et al., 2016; Semchenko et al., 2018). Several studies show that these fungal guilds are strongly influenced by plant species identity (Frac et al., 2018; Semchenko et al., 2018) and that increased associations with AMF (Cortois et al., 2016; Semchenko et al., 2018) or fungal pathotrophs (Semchenko et al., 2018; Wilschut et al., 2019) lead to more positive and negative PSFs, respectively. There is also evidence that AMF and pathotroph communities are strongly determined by plant phylogenetic relatedness (Barberán et al., 2015; Sweeney et al., 2021) and functional traits, particularly root traits (Bergmann et al., 2020; Eissenstat et al., 2015; Sweeney et al., 2021). This suggests, therefore, that the prediction of the direction and magnitude of PSFs requires better understanding of how soil microbial communities and their effects on plant performance are shaped by plant functional traits and phylogeny.

Several studies demonstrate that plant functional traits can act as important determinants of PSFs (Baxendale et al., 2014; Kardol et al., 2015; Rutten & Allan, 2023; Teste et al., 2017). Indeed, root traits known to influence AMF or pathotroph communities (Bergmann et al., 2020; McCormack & Iversen, 2019; Semchenko et al., 2018; Sweeney et al., 2021; Wilschut et al., 2019), including root diameter (Semchenko et al., 2018), percentage colonisation by AMF and specific root length (Cortois et al., 2016), have been shown to determine the outcome of PSFs. These traits represent the ‘collaboration axis’ of root resource economics (Bergmann et al., 2020), suggesting that a plant's strategy to partner with AMF for nutrient uptake is a key determinant of PSFs. However, the ‘conservation axis’ of the root economics space, reflecting the longevity and construction cost of root tissues, has also been found to determine the direction and magnitude of PSFs (Spitzer et al., 2022). Above-ground plant traits have also been linked to PSFs (Baxendale et al., 2014; Fitzpatrick et al., 2017; Semchenko et al., 2018), including shoot nitrogen content (Semchenko et al., 2018) and specific leaf area (Fitzpatrick et al., 2017). Importantly, these above-ground traits represent fast–slow plant resource economics and are independent of traits indicative of reliance on mycorrhizal fungi for nutrient acquisition (Bergmann et al., 2020). As both plant resource acquisition (Cortois et al., 2016; Semchenko et al., 2018) and resource conservation strategies (Baxendale et al., 2014) have been linked to PSFs (Rutten & Allan, 2023; Semchenko et al., 2022; Xi et al., 2021), further work is required to determine which plant traits determine PSF outcomes and the mechanisms behind these relationships.

Plant functional traits reflect the reliance of plants on mycorrhizal fungi and investment in overall defence against pathogens. However, PSFs are also strongly affected by host-specificity of plant–microbial interactions, which are likely determined by complex molecular mechanisms not reflected in commonly measured functional traits (Semchenko et al., 2022). Such interactions may be phylogenetically conserved, hence phylogenetic distance between plant species could be a key predictor of PSF outcomes (Fitzpatrick et al., 2017; Liu et al., 2012). Both AMF and fungal pathotrophs are known to exhibit host-specificity and preferences for closely related plant species (Dickie, 2007; Gilbert & Webb, 2007; Schroeder et al., 2019; Sweeney et al., 2021). Consequently, closely related plant species may share beneficial mutualist communities and plants may grow preferentially in soils conditioned by conspecifics or close phylogenetic relatives (Duell et al., 2023; Segnitz et al., 2020; Semchenko et al., 2018). Alternatively, growth in soil conditioned by increasingly phylogenetically dissimilar species may result in less exposure to specialised pathogens, resulting in pathogen release and improved plant growth (Aldorfová et al., 2020; Segnitz et al., 2020). Importantly, these potential outcomes oppose each other, and from this, we would expect phylogenetic relatedness to be positively and negatively correlated to PSFs, respectively, depending on whether AMF or pathogens are the primary drivers of PSF outcomes. Therefore, the relationship between phylogenetic relatedness and PSFs likely depends on the balance between AMF and pathogens in determining the net outcome of PSFs. This may lead to no overall effect of phylogenetic relatedness in moderating PSFs, should the opposing influences of AMF and pathogens be of equal importance and cancel each other out. This diversity of potential outcomes likely leads to the considerable uncertainty as to the role of plant phylogenetic relatedness in driving PSFs as many studies have provided evidence for (Anacker et al., 2014; Brandt et al., 2009; Crawford et al., 2019; Kempel et al., 2018; Wandrag et al., 2020) and against (Fitzpatrick et al., 2017; Lance et al., 2020; Mehrabi & Tuck, 2015; Wilschut et al., 2019) its significance. Although it is important to note that within the suite of studies reporting the effects of phylogenetic relatedness in determining PSFs, the effects sizes may be small (Crawford et al., 2019; Wandrag et al., 2020) or the results may be context specific and limited to regionally rare species (Kempel et al., 2018). As few studies have directly characterised the roles of AMF and fungal pathotrophs within the context of PSFs (Semchenko et al., 2018; Wilschut et al., 2019, 2023), there remains considerable uncertainty surrounding the microbial drivers of phylogenetic effects on PSFs.

Here, we examined how plant phylogenetic relatedness and functional traits act as determinants of PSFs via their influence on rhizosphere fungal communities, especially AMF and fungal pathotrophs. We hypothesised that both plant phylogenetic relatedness and plant traits determine PSFs and the direction, and magnitude of these relationships is mediated by the degree to which species accumulate AMF and fungal pathotrophs within their rhizosphere. We expect that plant species associating with an increased abundance or diversity of AMF or pathotrophs will experience more positive or negative PSFs, respectively. This was tested using soil from a glasshouse experiment of 21 common temperate grassland plant species representing a broad spectrum of life history strategies, in which we previously identified significant shifts in fungal community structure on the basis of plant phylogeny and functional traits (Sweeney et al., 2021). The present study builds on this work by using the conditioned soil in a PSF experiment in which a randomised phylogenetic gradient was generated between the focal species and the heterospecific species that conditioned the soil.