Introduction

Soil is a complex living system that serves as Earth’s primary biological reservoir (Wall et al. 2019). Healthy soils play a crucial role in providing several ecosystem services, including food and energy production, water quality regulation, and nutrient cycling (Costanza et al. 1997). These ecosystem services are supported by a highly interconnected network of diverse species, such as plants, animals, and micro- and macro-fauna (Adhikari and Hartemink 2016). In particular, soil physical properties are crucial to biological functions due to their influence on plant growth, control of water transport and storage, and nutrient cycling (Bagnall et al. 2022; Lal 2009).

One of the most disruptive activities with a long-term effect on soil functions is modern agriculture. Agricultural practices have a significantly negative impact on the soil’s chemical, physical, and biological properties that ultimately affect the ecosystem services it provides (Tittonell 2020). Among the negative effects of agriculture on soil properties is its compaction, which is the process of increasing soil density by reducing the pore space between soil particles. This phenomenon is a very common consequence of agricultural practices, having a significant detrimental effect on soil degradation, and is estimated to affect more than 70 MHa worldwide (Fig. 1a). Compaction negatively affects the processes that occur in the soil matrix and its inhabitants. Once the soil has been compacted, recovery to its original state is usually very slow, and can take up to several decades depending on the physical and mineralogical composition of the soil (Jourgholami et al. 2019).

Fig. 1
figure 1

Soil compaction is a global problem. a Global distribution of subsoil compaction susceptibility index (SCSI) relating estimated mean tractor-applied stress to soil strength at a depth of 0.5 m. The estimations were based on the mechanization levels, farm sizes, estimated tractor size, soil texture, and soil water content (calculated at a 0.1°resolution) (adapted from Keller and Or (2022). b Example of soil compacted by machinery traffic showing the accumulation of water in the compacted area due to the low permeability of the soil

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The progression of soil densification and the reduction of its porosity due to its compaction leads to a severe modification of the soil structure associated with an increase in its resistance to being penetrated and a decrease in its hydraulic conductivity (Soane and Van Ouwerkerk 1994; Hillel 1980) frequently resulting in further loss of soil structure (Mc Garry and Sharp 2003). For example, the altered pore-size distribution due to compaction results in an unstable consolidation of soil aggregates (Mapa and Gunasena 1995). The main causes of soil compaction have been associated with the use of heavy agricultural machinery (Keller et al. 2019), the soil’s physical characteristics (Zink et al. 2011), and soil manipulation techniques in preparation for crop production including the different types of tillage (Badalíková 2010; Quiroga et al. 1999) and the treading action of animals (Drewry et al. 2008; Herbin et al. 2011). Soil susceptibility to compaction changes from soil to soil and is mostly determined by soil texture, the degree of soil particle aggregation, and the soil’s capacity to retain water (Horn et al. 1995). Of all, soil water content is the most critical element modulating soil vulnerability to compaction (Van der Watt 1969). Higher soil water content reduces macropore spaces, resulting in a lower ability of the soil to withstand pressure without changing its density (Liepic et al. 2002). Therefore, soils are more prone to compaction when the water content is high or near the optimal value for plant growth (Mitchell and Berry 2001). Dryer soils, on the other hand, are more resistant to compaction than wetter ones (Drewry and Paton 2000; Ishaq et al. 2001).

Soil compaction is not a homogeneous process; therefore, it is common to find regions where only the surface layer of the soil is compacted or areas where compaction includes or is only present in the subsoil. As a result, soil mechanical impedance is not uniformly distributed and this heterogeneity can have a complex impact on plant root systems and overall crop production (Konôpka et al. 2008). This phenomenon reflects the different origins of compaction and its different consequences, so the management of compacted soils should be individualized to minimize the negative consequences of compaction on agricultural yields (Bengough et al. 2011; Mueller et al. 2010; Obour and Ugarte 2021).

This review is based on several publications on recent advances in understanding the impact of compaction on soil properties and functions, with a focus on (a) how compaction affects the physical and chemical properties of soil, (b) how plants react to compacted soils, and (c) how soil microbiota changes in compacted soils. Given the detrimental impact of compaction on soil health, we will address some potential options involving various agricultural management and crop selection to reduce the impact of compaction on agricultural production.

Compaction affects the soil’s physical and chemical properties

Soil compaction is produced by a change in its apparent density per unit of soil volume. This change is associated with variations in soil porosity, particularly in the volume of large pores between aggregates, which as a result of compaction are rearranged with less space between solid particles (DeJong-Hughes et al. 2001). Thus, the increase in soil apparent density due to densification in particle distribution results in a decrease in soil macropores (Ball et al. 2007; Leeds-Harrison et al. 1986), which are responsible for adequate soil aeration and water mobility (Fig. 2). As a consequence of the reduction of soil macropores, there is a decrease in the circulation of air and water, as well as their retention within the soil profile, resulting in a predominance of conditions of low oxygen concentration (anoxia) (Berisso et al. 2012). At the same time, soil compaction also affects soil penetration resistance, which is the ability of soil to be penetrated by water, air, or plant roots (Greacen and Sands 1980). Decreased infiltration rates often result in increased runoff volume and surface water accumulation, decreased groundwater recharge within watersheds (Gregory et al. 2006), and plant root failure to penetrate the soil (Berisso et al. 2012), decreasing the plant’s ability to absorb nutrients (Correa et al. 2019).

Fig. 2
figure 2

The physical properties of soil change under compaction. a A non-invasive X-ray CT image of a column of uncompacted soil (bulk density: 1.1 g cm−3) sampled from an agricultural farm at the University of Nottingham, with a high presence of macroaggregates (red arrows) and pore formations (blue arrows) that allow optimal development of the soil function, for example allowing the penetration of plant roots. b A CT image of the same soil, artificially compacted (bulk density: 1.6 g cm−3), to illustrate the reduction in pore volumes and macroaggregates number in compacted soils that compromise soil functions

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Soil compaction also affects the stability of soil aggregates, which is a direct measure of soil health (Rieke et al. 2022). Aggregate stability defines the ability of soil particles and aggregates to adhere, as a result of cohesive forces between them and organic matter, and its reduction is an early indicator of soil degradation (Six et al. 2004). As the mineralogical composition of soil aggregates is different, as well as their abundance, organic composition, water, and oxygen content (Allison and Jastrow 2006; Beare et al. 1994; Christensen 2001; Kandeler et al. 1999; Lagomarsino et al. 2012), it is therefore expected that soil compaction processes also change the spatial distribution profiles of nutrients in the soil. These changes impact the life cycle of the members of the soil ecosystem that have to adapt to changes in their niches. For example, some forms of soil tillage, affect the stability of soil aggregates, also favours compaction. Tillage can break up larger aggregates (Kahle et al. 2013; Tisdall and Oades 1980), leading to rapid and heavy redistribution of soil organic carbon within the topsoil along with reduced pore spaces, resulting in reduced water and nutrient infiltration and increased vulnerability to erosive factors, such as wind and water (Tapela and Colvin 2002). However, other forms of tillage, such as deep non-inversion tillage, could be used as a strategy to decrease soil bulk density, increase infiltration rate, and decrease soil penetration in compacted soils (Peralta et al. 2021). Nevertheless, because the long-term relationship between tillage forms and soil vulnerability to compaction is not yet well established, it is important to combine these strategies with others compaction prevention and soil regeneration practices. Soil compaction is not only associated with changes in the physical and structural properties of the soil but also alters some chemical and biochemical processes that occur within the soil matrix. One of the more affected processes is the redox potential of soil solutions (Lipiec and Hatano 2003) and the availability of N, P, and K (Nawaz et al. 2013). This is essentially a direct consequence of soil anoxia favouring the reduction of the redox potential of valence-dependent soil molecules, such as those that include iron in their structures (Faulkner and Patrick 1992). The absence of oxygen results in the formation of reduced forms of iron (Fe2+), increased iron hydroxides in solution, and organically complex forms of iron (Ponnamperuma 1985). This phenomenon can be observed in soil with a grey-bluish tint in contrast with reddish-to-brown tints in well-aerated soils.

The low concentration of oxygen in the soil due to compaction also affects the availability of nitrogen, due to the oxidation process of ammonia to nitric and nitrous species, followed by a process of denitrification and release of gaseous nitrogen, as nitrous oxide, into the atmosphere (Pulido-Moncada et al. 2020; Wolkowski 1990). In the case of phosphorus and potassium, they become less available to plants (Arocena 2000; Ferreira et al. 2021) due to their low concentrations and mobility in soil solutions, as a result of changes in the rate of diffusion and mass transfer in compacted soils (Kristoffersen and Riley 2005). Overall, higher soil bulk density results in fewer macropores, which reduces the quantity of water and oxygen available in the soil. This change disrupts the biochemical balance of soil nutrients and redox potentials, resulting in changes in the soil’s physical and chemical properties.

Soil compaction modifies plant and crop growth

Soil compaction has a negative impact on the growth and yield of plants and crops, resulting in the loss of over $300 million in crop production annually (Graves et al. 2015). Soil compaction can affect crops in a variety of ways, including the negative effect that increasing soil impedance, decreasing nutrient availability, and lack of oxygen due to frequent waterlogging have on agricultural production (Ferreira et al. 2021; Kristoffersen and Riley 2005).

Plants commonly reduce their root length and the number of lateral roots in response to increased soil density (Hamza and Anderson 2005), resulting in reduced root penetration and depth, and changes in their redistribution in the soil profile (Pfeifer et al. 2014). Since root penetration into compacted soils is significantly affected, the amount of soil that roots can explore to provide nutrients to plants is also significantly reduced in compacted soil conditions, particularly for those nutrients transported by diffusion, such as phosphorus and potassium (Dolan et al. 1992; Shierlaw and Alston 1984). However, the negative impact of soil compaction on crop health and growth is not homogeneous and also depends on plant species and soil properties (Greacen and Sands 1980; Lipiec and Stepniewski 1995). For example, topsoil compaction is a more limiting factor for root growth than subsoil compaction (Botta et al. 2010). Furthermore, Marschner (1995) established that plant growth is not limited in compacted soils with high water availability possibly because the maximum soil force that the root can penetrate is determined by the maximum turgor generated within the root elongation zone and root tip characteristics (Bengough et al. 1997). Therefore, it is of vital importance to define the adaptation mechanisms of plants to compacted soils to mitigate the effect of compaction on crop yields.

Plant molecular mechanisms underpinning soil compaction sensing

Plant hormones, including ethylene, auxin, and abscisic acid (ABA), are well-established key regulators of root growth in both eudicot and monocot species (Smith and De Smet 2012). Ethylene has been specifically associated with adaptive responses of roots to soil strength and mechanical impedance, as demonstrated by previous studies (Kays and Harper 1974; Sarquis et al. 1991). Recent research has further elucidated ethylene’s role in regulating root growth responses to soil compaction in Arabidopsis, rice, and maize (Pandey and Bennett 2023; Pandey et al. 2021; Vanhees et al. 2022).

Ethylene-dependent responses to soil compaction lead to a reduction in root elongation and an increase in radial swelling. Remarkably, ethylene-insensitive mutants no longer exhibit these compaction-induced root growth responses. Surprisingly, Arabidopsis and rice ethylene-insensitive mutants, despite having narrower roots, were still able to penetrate compacted soil. This intriguing finding reveals that while plant roots can exert enough pressure to penetrate compacted soil, their elongation in such soil is significantly inhibited due to the accumulation of ethylene. Roots detect the accumulation of ethylene in compacted soil, which occurs due to slower gas diffusion away from the root surface (Pandey et al. 2021). In compacted soil where pore size and connectivity are reduced, ethylene accumulates around root tips, leading to growth inhibition. In contrast, non-compacted soil with well-connected pores of various sizes allows ethylene released by root tips to rapidly diffuse away. This novel mechanism of ethylene gas diffusion may enable roots to sense and respond to changes in soil structure, thereby triggering adaptive responses in compacted soils.

Furthermore, ethylene-dependent root compaction responses result in a reduction in cell elongation and increased radial expansion of cortical cells. Recent research has unveiled that these distinct cellular growth responses induced by ethylene are mediated through different hormone signals, such as auxin and ABA (Huang et al. 2022). Auxin primarily acts to reduce root cell elongation during compaction responses, while ABA promotes the radial expansion of cortical cells. Radial swelling can be particularly beneficial for root penetration in hard soil layers (Kirby and Bengough 2002). Interestingly, ABA synthesis mutants in rice disrupted the radial swelling of root tips but exhibited enhanced penetration of compacted soil compared to the wild-type (Huang et al. 2022). The combined effects of auxin and ABA contribute to limiting the rapid elongation of roots in compacted soils (Fig. 3). Compaction in field soils during dry periods may reduce water availability to roots, potentially triggering increased levels of the abiotic stress signal ABA, in addition to its induction by ethylene. The interplay between these responses can lead to complex interactions that influence root morphology, distribution, and water uptake. Understanding these intricate root-soil interactions is a challenging endeavour, but recent advancements in root growth modelling are beginning to provide more realistic insights into these complex processes (De Moraes et al. 2018, Lynch 2022, Strock et al. 2022).

Fig. 3
figure 3

Ethylene controls the inhibition of elongation and promotion of radial expansion of rice roots in compacted soils by stimulating the biosynthesis of auxin and ABA. Model proposed for root responses in (a) noncompacted soil and (b) compacted soil by Huang et al. (2022). Under Compacted soil conditions the ethylene response is induced due to limited diffusion of ethylene in the close proximity of the root. High levels of ethylene promote the activation of OsEIL1, which induces auxin biosynthesis via OsYUC8. As a consequence of enhanced auxin response in epidermal cells in the meristematic and elongation zones of the root, the epidermal cell elongation is inhibited and therefore root elongation. Concomitantly, ethylene signalling indirectly induces ABA biosynthesis in the vasculature promoting radial expansion of root cortical cells, participating also in the inhibition of root elongation in compacted soil. In the figure, red circles represent ethylene molecules, widened yellow or black arrows indicate higher response of auxin and ABA, and yellow arrows denote auxin transport

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Another effective strategy that plants employ to adapt to compacted soil conditions involves the formation of multiseriate cortical sclerenchyma (MCS). This specialized lignified outer cortical cell is a common feature in numerous cereal crop species, including maize, wheat, and barley (Schneider et al. 2021). Its primary function is to enhance the mechanical stability of root tissue, enabling it to penetrate compacted soil with greater efficiency. Notably, the induction of MCS formation is triggered by ethylene, which accumulates in response to soil compaction and serves as a signal for compaction-related adaptations (Schneider et al. 2021).

Soil compaction modifies populations of free-living microbes

Soil microbial communities play a fundamental role in soil processes, such as nutrient cycling, C sequestration, water retention, and soil aggregate formation (Nannipieri et al. 2003). Correspondingly, both the soil structure and the availability of nutrients, oxygen, and water determine the composition and function of soil microbial communities (Delgado-Baquerizo et al. 2016). In the soil, each aggregate fraction with its physical and chemical properties not only represents a distinctive habitat space or niche for microbial communities (Bach et al. 2018) but also influences their composition (Ranjard et al. 2000). Thus, the effect of compaction on soil aggregate stability is expected to impact membership of the soil microbial community. Along these lines, Li et al. (2004) demonstrated that high bulk density reduces soil bacteria and fungus abundance by 26–40%, and as a result general soil microbial activity (Liebig et al. 1995). Similar results have been obtained in other studies (Frey et al. 2011; Hartmann et al. 2014, 2012, Longepierre et al. 2021). However, it is contradictory whether soil compaction affects total microbial abundance. Some studies have shown that, in response to compaction, some soils reduce the total abundance of bacteria (Dick et al. 1988), but other authors have shown that soil compaction does not affect total microbial biomass (Jordan et al. 2003; Ponder and Tadros 2002; Shestak and Busse 2005; Tan et al. 2008, 2005). Therefore, more studies are needed to clarify the effect of soil compaction on the function and abundance of its microbiota.

Compacted soils with less available oxygen produce changes in the proportion of the members of the microbial communities, favouring those microbes with anaerobic respiration capacities, such as methanogens (Frey et al. 2011) and denitrifiers (Hartmann et al. 2014; Li et al. 2004; Longepierre et al. 2021, 2022). Further, under compacted soil conditions, changes in the methanogen and denitrifier communities are significantly associated with the change in the amount of NO2 and CO2 in the soil. (Longepierre et al. 2022). Among the bacterial taxa enhanced in compacted soil, which are capable of anaerobic respiration and/or fermentation, Hartmann et al. (2012) found Geobacter, Anaeromyxobacter, Desulfuromonas, Desulfovibrio, Desulfobulbus, Pelobacter, Syntrophobacter, and Sulfurospirillum (all delta-proteobacteria); Rhodoferax, Rhodocyclus, and Dechloromonas (all beta-proteobacteria); or Clostridium, Desulfosporosinus, Sporotalea, Desulfitobacterium, Thermosinus, Bacillus, Paenibacillus, Acetivibrio, Thermincola, and Ethanoligenens (all firmicute). Those taxa were confirmed by Hartmann et al. (2014). Soil compaction also favours the growth of other anaerobic bacteria, such as iron- and sulfate-reducing bacteria.

In the case of fungal communities, soil compaction promotes saprotrophic fungi, such as Mortierella (Mortierellomycota), Mucor (Mucor), Tetracladium, Preussia, Podospora, Pseudobillarda, Botryotrichum, Scutellinia, Trematosphaeria, and Thelebolus (all Ascomycota). More research on the dynamics of changes in microbial communities at the level of soil aggregate resolution is required to truly evaluate the effect of compaction on microbial communities and predict its possible effect on plant microbiota recruitment.

Soil compaction alters plant-microbe interactions

Plants and microbes have coevolved for millions of years (Delaux and Schornack 2021) establishing beneficial interactions that are critical for plants to survive and adapt to the stress conditions frequently found in ecosystems (Castrillo et al. 2017; Harbort et al. 2020; Zhang et al. 2019). In compacted soil, plants exhibit reduced shoot growth and altered root system architecture (Correa et al. 2019; Mulholland et al. 1999). These changes in root architecture, which include a reduction in the primary root and thinner, more fibrous lateral roots (Bingham 2007), alter the interaction between roots and soil microbiota (Eisenhauer et al. 2017). In general, plants grown in compacted soils have a reduced number of root-associated microbes (Hartmann and Six 2023) and less capacity for example to form nodules upon rhizobium colonization (Lindemann et al. 1982). This reduced nodulation has been associated with a decrease in root hairs, critical for the initiation of nodulation (Katoch et al. 1983), in plants grown in compacted soils (Hoffmann and Jungk 1995). Soil compaction also affects the symbiotic association between endophytic fungi and plants. Hosseini et al. (2018) showed that in compacted soils, maize roots reduced their ability to be colonized by the fungus Piriformospora indica by almost 30% compared to non-compacted soils.

One of the main causes of this atypical interaction between roots and soil microbiota could also be attributable to the accumulation of ethylene in the root proximity when growing in compacted soils (Barry et al. 2001; Pandey et al. 2021). Chen et al. (2020) demonstrated that soils artificially supplemented with a high concentration of ethylene increased bacterial diversity in the rhizosphere even more than that observed in compacted soils. Furthermore, an external supply of ethylene to the roots inhibited rhizobia-mediated plant nodulation due to the effect of ethylene on plant sensitivity to Nod factors (Oldroyd et al. 2001). Although some elements of plant-microbiota interactions in compacted soils have been described, it has not yet been studied whether the resident microbiota could influence plant mechanisms to cope with compaction. Furthermore, studies on the influence of plant response to soil compaction on microbe-microbe interactions in the rhizosphere are missing. The results of such studies might be necessary for the design of novel strategies based on the interaction of plants with the soil microbiota to mitigate the detrimental effects of soil compaction on plant performance.

Possible solutions to alleviate the negative effect of soil compaction

The conservative agriculture movement has never had more momentum than now, which has facilitated the use and implementation of new soil management strategies that could help reduce the negative effects of compaction. One strategy proposed to improve crop performance in compacted soil is increasing soil organic matter, which is the principal nutrient reservoir in the soil. For example, Zhang (1997) investigated the effectiveness of incorporated organic matter (two different types of humified peat) in different soils and under varying soil water conditions, which resulted in a decrease in soil compaction at low soil moisture levels. Similarly, the use of biofertilizers, such as manure or biochar, has been shown to decrease soil bulk density in compacted soils (Blanco-Canqui 2021; Seguel et al. 2013). Thus, increased organic matter can reduce the soil susceptibility to compaction (Soane 1990). In addition to the increase in water retention and nutrient availability (Hudson 1994), organic matter reduces soil bulk density and increases its water infiltration (Hamza and Anderson 2005; Zhang 1997). Soil management practices such as zero tillage, crop rotations, and the addition of winter cover crops are known to boost organic matter positive effect (Thapa et al. 2022).

The selection of crops to be planted in compacted soil is critical to partially overcome the negative effects of soil compaction on plant performance. Perennial and deep-rooted plants with strong soil penetration resistance can help with soil structure recovery, resulting in increased soil penetrability and aeration (Colombi and Keller 2019). Furthermore, selecting genotypes with beneficial root traits is critical for increasing crop production. For example, acute root tip angles (Colombi et al. 2017), high root hair density (Bengough et al. 2016) and roots with increased mucilage excretion (Somasundaram et al. 2008) can help plants grow better in compacted soil.

Several studies have shown that plant growth-promoting rhizobacteria are beneficial for plant growth in compacted soils (Canbolat et al. 2006; Prasad et al. 2020), especially helping plants to cope with the reduced availability of nutrients found in compacted soils. Plants inoculated with Bacillus (strains: RCo1, RCo2, RCo3, and M-13) improve N and Mn uptake and increase the production of larger roots and hairs, allowing plants to minimize other detrimental effects of soil compaction (Canbolat et al. 2006). Positive results have also been observed with the use of arbuscular mycorrhizae in maize and wheat grown in compacted soil (Miransari et al. 2007, 2008, 2009). In both crops, mycorrhiza improved plant root growth and increased nutrient uptake. Despite the efforts to alleviate the negative effects of soil compaction, many existing initiatives still address only part of the problem, attempting to solve only isolated causes of compaction. The design of more holistic strategies, combining several approaches to mitigate the causes and consequences of compaction, is necessary to multiply the positive results of crop performance in compacted soils.

Conclusions

Soil compaction is a global problem in which the soil undergoes a process of densification and reduction of its porosity, resulting in a severe modification of the soil structure associated with an increase in soil resistance and a decrease in hydraulic conductivity. These changes affect the growth and development of crops and modify the structure of the soil microbial communities and their interaction with plants. Although strategies have been designed to mitigate the effect of soil compaction in agricultural settings such as new soil management practices, the selection of crops better adapted to the conditions that compaction imposes, or the development of genetically edited crops to maximize desirable characteristics to cope with compaction, much remains to be investigated. A very promising field in terms of solutions with minimal impact on the environment is the interactions of the plant with the soil microbiota. A deeper understanding of the mechanisms governing plant microbial community selection and function at the root-soil interface in compacted soils may aid in the development of innovative microbe-based solutions to increase crop yields. Therefore, future research should consider exploring the possible mechanisms that the microbiota uses to modulate the plant response to compaction with special emphasis on the production or consumption of modulatory volatile compounds. We should join forces to define the mechanisms of how the root microbiota modulates the plant response to compaction. More emphasis should be placed on elucidating the molecular basis of the filtering mechanisms that operate in the root to select a beneficial microbiota in response to compaction. This knowledge could help design new strategies, which, together with existing ones, could help ensure more food production in compacted soils while they regenerate. This would alleviate the pressure to produce more food with less available soil and resources.