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:
- Intensive management and selection pressures, whether direct or
indirect, result in the development of acquisitive plant traits in
modern barley, whereas wild barley tends to exhibit relatively more
conservative traits.
- Wild barley demonstrates a stronger response to changes in soil
microbiome compared to modern barley, possibly due to the tight
co-evolutionary links between them. In contrast, domestication may
have hindered such links in modern barley.
- Both modern and wild barley possess distinct species-specific
bacterial communities in the rhizosphere.
- The coupling of plant traits is expected to be stronger with more
interactions in wild barley compared to its modern
counterpart.