Climate-driven shifts in plant–soil feedback of a perennial grass species

1 INTRODUCTION

Plant–soil feedback (PSF)—a process where plants alter the biotic and abiotic properties of soil they grow in, which subsequently influences the performance of plants grown in that soil in the future (Bever et al., 1997)—has been recognized as an important driver of plant community assembly and ecosystem functioning (Bardgett & van der Putten, 2014; Reynolds et al., 2003). High rates of recently observed as well as expected changes in temperature and precipitation regimes (IPCC, 2014) are likely going to affect the distribution of soil microbes and plants and modify the ways plants and soil interact (van der Putten et al., 2016). Understanding the impact of climate change on PSF is thus crucial for predicting the consequences of climate change for ecosystems and for providing avenues to mitigate its consequences in natural and applied systems.

Plants exhibit local adaptations to specific climatic conditions (Anderson & Song, 2020; Nicotra et al., 2010; Sammarco et al., 2022) and their associated soil biota (Crémieux et al., 2008; Johnson et al., 2010; Pánková et al., 2014). At the same time, soil biota can adapt to specific climate and to local plant genotypes (Johnson et al., 2010; Tack et al., 2012). These adaptations, along with changes in the composition of soil biota communities in response to genetic or species composition of local plant communities, shape the outcome of plant–soil interactions (Blanquart et al., 2013; Hoeksema & Forde, 2008; Kulmatiski et al., 2008; van der Putten et al., 2013). The distribution of both plants and their associated soil biota is largely driven by spatial variation in climatic conditions (Blankinship et al., 2011; Zhou et al., 2020). It may thus be expected that climate change will affect PSF as well (van der Putten et al., 2016). Indeed, Hassan et al. (2022) in their meta-analysis showed that drought and warming can induce context-specific shifts in PSF, which are dependent on plant functional groups, life history traits and experimental conditions.

Climate change may lead to novel or altered interactions between plants and soil biota (Bardgett & Wardle, 2010) due to differences in their respective rates and mechanisms of adaptation to novel conditions (van der Putten et al., 2009). For example, in case of asynchronous range shifts, that is in a situation when soil biota migrate faster to the new environment than plants (or oppositely), plants of a certain climatic origin encounter soil biota of a different climatic origin. This can disrupt established negative PSF caused by specialized antagonistic microbes in the plant's original range (Engelkes et al., 2008; van Grunsven et al., 2007), while a lack of adapted mutualistic organisms in new ranges can constrain plant growth (Nunez et al., 2009). The environmental context also plays a crucial role in shaping PSF (De Long et al., 2019; van der Putten et al., 2016). Previous studies manipulating cultivation conditions have shown that temperature and moisture levels can affect soil biota composition and activity (Deveautour et al., 2018; Heinze et al., 2017; Siebert et al., 2019), as well as plant biomass allocation and root architecture (Bergmann et al., 2016; Cortois et al., 2016), thereby altering the intensity with which plant roots interact with the soil (Aldorfova & Munzbergova, 2019; Duell et al., 2019; Florianova & Munzbergova, 2018; Fry et al., 2018; Kaisermann et al., 2017). Importantly, individual groups of soil biota may differ in their sensitivity to climatic conditions as well as in the degree of co-adaptation with plants. Generally, soil pathogens are more specialized and show a higher degree of co-adaptation with plants than soil mutualists (Molina & Horton, 2015; Smith & Read, 2008). It can thus be expected that disrupting established plant–soil interactions will lead to less negative overall PSF.

To comprehend how climate change affects plants through changes in soil biota, it is essential to simultaneously manipulate soil origin, plant origin and climatic conditions in all factorial combinations. Several double interactions within this triple framework have been explored, such as the genetic differentiation and phenotypic plasticity of plant populations in response to climate (Hamann et al., 2016; Munzbergova et al., 2017; Nicotra et al., 2010; Valladares et al., 2014), the specificity of soil biota (Cardinaux et al., 2018; Koorem et al., 2020; Pankova et al., 2011; Van Nuland et al., 2017) or climate dependency of soil biota (von Holle et al., 2020). However, very few studies (to our knowledge only Remke et al., 2022 and Aares et al., 2023) have so far manipulated all three components of the climate-plant-soil framework.

In this study, we investigated the interaction between soil biota origin, plant origin, and cultivation climate using Festuca rubra, a perennial grass dominating alpine grasslands in large parts of Europe, as a model. We conducted a two-phase growth chamber experiment, examining the PSF (here in two versions as recommended by Brinkman et al. (2010)—biotic PSF defined as relative performance of plants when grown in live vs. sterile soil, and whole-soil PSF as relative performance of plants when grown in self-conditioned vs. community-conditioned soil) of F. rubra originating from two climatically distinct sites, when grown with local or foreign soil biota (i.e. soil biota originating from either the ‘home’ or ‘away’ site), cultivated in climate representing the climate of either the ‘home’ or ‘away’ site. We assessed Festuca's PSF under all treatments and investigated the changes in soil chemistry following soil conditioning to explain the observed differences in the PSF. We tested the following hypotheses:

• H1: Soil pathogens are more strongly adapted to their climate of origin compared to soil mutualists, and therefore soil biota generates more negative PSF effects in their home than in away climate.
• H2: Plants are adapted for growth in their respective climates of origin, therefore perform better and show less negative PSF in home than in away climate.
• H3: The degree of co-adaptation between plants and soil pathogens is higher than between plants and soil mutualists, making PSF effects more negative when plants are grown with their local soil biota (i.e. soil biota originating from the same site as the plants) than when grown with foreign soil biota (i.e. biota from the other site).
• H4: Due to the above-mentioned mutual adaptations of plants and soil and adaptations of both of these components to climate, PSF is expected to be most negative when plants are grown with their local soil biota under their home climate.