Introduction
For centuries, natural and artificial selection pressures through crop domestication as well as more recent breeding programs and agricultural management practices have led to significant changes in crop phenotypes based on human requirements. For instance, modern cultivars of various cereal crops (such as rice, wheat, and barley) possess an increased number of grains per panicle, larger seeds, uniform germination and flowering timings, reduced seed dormancy and dispersal, loss of shattering, and shorter longevity in contrast to higher photosynthetic rates and nitrogen content in leaves (Meyer, DuVal & Jensen 2012; Preece et al. 2017; Roucou et al. 2018). Modern crop cultivars also tend to grow faster due to homogenous environmental conditions and ample availability of soil resources, suggesting that they may have adapted toward quick-to-acquire (acquisitive) strategies. This so-called domestication syndrome has led to lesser resource investment in the physical and chemical defense system of modern crop cultivars (Turcotte, Turley & Johnson 2014; Simpson, Wade, Rees, Osborne & Hartley 2017; Fernandez, Sáez, Quintero, Gleiser & Aizen 2021; Allaby, Stevens, Kistler & Fuller 2022). In a meta-analysis, Fernandez et al. (2021) provided strong evidence across a range of crops that plant damage by herbivory was higher in modern crop cultivars whereas the defense level was higher in their putative wild counterparts. They showed that, in modern crop cultivars, the average defense production lowered by only 10% whereas their susceptibility to herbivory increased by up to 430% in comparison with putative wild relatives. These results can be only partly explained by differential resource investments and their potential cost-benefit tradeoffs and sought for further empirical evidence to have a holistic understanding of mismatches for growth and defense mechanisms in modern crops in developing novel crop varieties (Tracy et al. 2020; York et al. 2022a; York, Griffiths & Maaz 2022b).
Nonetheless, despite recent research advancements in identifying such remarkable resource tradeoffs and altered phenotypes between modern crop cultivars and their putative wild relatives, most of such advancements have focused on aboveground plant traits whereas the belowground plant traits have not been given significant attention. We lack a clear understanding of whether and how crop domestication and breeding programs have led to changes in functional root traits, including their interactions with soil microbes. It is becoming increasingly important to understand how the traits have changed through crop domestication as they were not directly targeted in crop breeding programs for cereal crops (Milla, Osborne, Turcotte & Violle 2015) yet a range of different traits related to resilience in a changing world are set to gain in importance in agriculture. This will likely help us know whether and how modern crop cultivars are adapted to ever-changing environmental conditions and agricultural management practices. Given the importance of root traits to crops’ ability to efficiently acquire soil resources, only a few attempts have been made which explicitly linked root phenotypes to plant performance (Schneider & Lynch 2020; Guo et al. 2021). This is, in part because, firstly, it is extremely difficult to quantify various root traits due to technical challenges, and secondly, root traits for resource acquisition are more complex than aboveground traits (Meister, Rajani, Ruzicka & Schachtman 2014; Isaacet al. 2021). For instance, root exudates – chemical compounds released by roots, mediate numerous biogeochemical processes in the rhizosphere. Only recently, root exudation has been considered a functional root trait and linked to the multidimensional root economic space for the acquisition of soil resources, where, distinct functional roles of exudates have been proposed for N and P acquisition (Wen, White, Shen & Lambers 2022). However, it is not clear whether and how the quality and quantity of root exudates co-vary with other biological, morphological, and architectural root traits. A few studies which have been linking various root traits have shown that a root exudation and root N concentration as well as specific root length are closely connected, whereas root exudation is negatively associated with root diameter, tissue density, and root longevity (Bergmann et al.2020; Wen et al. 2020; Sun et al. 2021). Interestingly, the exudation of enzymes from roots (especially phosphorus mobilizing enzymes such as phosphomonoesterases) to mobilize nutrients in the rhizosphere has been negatively correlated to root colonization by arbuscular mycorrhizal fungi (AMF) (Honvault et al. 2021; Hanet al. 2023). These studies suggest the existence of large variations in root traits across plant species and indicate that root traits correlate with each other and resource tradeoffs among them exist to efficiently acquire soil resources (Kong, Zhang, De Smet & Ding 2014; Wen et al. 2020; Wang, Zhang, Wang, Rengel & Li 2023). They also highlight that different plant species are able to adjust which strategies they use, depending on the potential for symbiosis, thus reaching the same outcomes (growth, reproduction) through different channels.
Next, the assemblages of microbial communities in the rhizosphere of wild progenitors and modern crop cultivars vary which directly feedback to plant fitness. Such variations in rhizosphere microbial communities are attributed to selection pressure, management practices, and root traits (especially root exudation). It is believed that wild plants profit more from rhizosphere microbes whereas intensive management of modern crop cultivars has led to the disruption of such root-microbial interactions (Pérez-Jaramillo, Mendes & Raaijmakers 2016; Martín-Robleset al. 2018, 2020). Empirical evidence has shown domestication-mediated disruption of plant-microbial interactions; for example the responsiveness and efficiency of 27 modern crops to root colonization by AMF was found to be lower than for their wild counterparts (Martín-Robles et al., 2018). The assemblage of distinct bacterial communities in the rhizosphere of wild progenitors and domesticated crops has also been highlighted in other studies (Bulgarelli et al. 2015; Pérez-Jaramillo et al. 2017). Using a plant-soil feedback approach, Martín-Robles et al. (2020) showed across 10 crop species that modern crops and their wild counterparts recruited soil biota in opposing ways. They highlighted the microbial recruitments in the rhizosphere to be crop specific and dependent on edaphic factors, which makes it difficult to utilize this knowledge for generalization for other crops. Altered microbial communities in the rhizosphere may also indirectly feedback to plant fitness by altering decomposers’ activities and therefore nutrient cycling via soil organic matter decomposition (Kuzyakov 2002; Pausch et al. 2016; Kumar, Kuzyakov & Pausch 2016). Therefore, it becomes crucial to investigate for specific crops how domestication has led to changes in root-microbial interactions and variation in plant traits and their coordination for resource acquisition. This information will help us to improve the nutrient acquisition of modern crop cultivars in a rapidly changing world where the ability to withstand harsher conditions (e.g.stress related to extreme weather events) is rapidly becoming more important for food security. By adopting management practices that favor positive rhizosphere interactions (Rillig et al. 2019) and incorporation of functional traits (especially root traits) future crop breeding programs will be better equipped increase the efficiency of crops to acquire soil resources in a world of global change.
Therefore, through a comparative approach by using modern- and wild barley species, we investigated whether and how crop domestication has led to changes in functional root traits and assemblage of rhizosphere bacterial communities. We further determined whether there had been changes in root traits and assemblage of rhizosphere bacterial communities depending on soil microbial diversity for which we experimentally manipulated soil microbial life by using soil sterilization.
We hypothesized that: