The ability of maize roots to grow through compacted soil is not dependent on the amount of roots formed
Introduction
The ability of plants to acquire nutrients and water is dependent on soil exploration. Mechanical impedance can lead to reduced total root length and/or a redistribution of root length within the soil profile (Pfeifer et al., 2014a; Shierlaw and Alston, 1984), which could affect the acquisition of water and nutrients. As soils get denser and stronger with depth, due to overburden pressure (Gao et al., 2012, 2016), mechanical impedance will often restrict deeper rooting root phenotypes more than topsoil foraging root phenotypes. Periodic droughts are common in many ecosystems and drier soils are generally harder (Gao et al., 2012; To and Kay, 2005; Vaz et al., 2011; Whalley et al., 2005; Suralta et al., 2018). However, plants with root systems that grow deeper are in general better adapted to drought (Chimungu et al., 2014a; Lilley and Kirkegaard, 2016; Lynch, 2013; Zhan et al., 2015). Certain soils offer very large mechanical impedance to roots, for example hard-setting soils in Australia (Mullins et al., 1987) or rainfed lowland rice cultivation systems (Suralta et al., 2018). Different agricultural management approaches can also introduce compaction and plough pans by wheeled traffic or trampling (Batey, 2009; Hamza and Anderson, 2005). Depending on the soil textural characteristics, suboptimal soil conditions during trafficking (such as high moisture contents) will exacerbate compaction (Horn et al., 1995; Raper, 2005). Roots can become confined to surface soil strata when not capable of penetrating through a hard soil layer such as a plough pan (Barraclough and Weir, 1988; Ehlers et al., 1983). Root systems are able to compensate root growth by exploiting the lesser impeded regions of the soil, as illustrated by split pot experiments (Bingham and Bengough, 2003; Pfeifer et al., 2014a) or layered pot systems (Shierlaw and Alston, 1984). Roots of maize (Chimungu et al., 2015), rice (Chandra Babu et al., 2001; Clark et al., 2000, 2002; Yu et al., 1995), wheat (Botwright Acuña and Wade, 2005; Kubo et al., 2006) and common bean (Rivera et al., 2019) show substantial genotypic variability for penetrating strong wax layers simulating mechanical impedance.
Root systems consist of distinct root classes which vary by taxa, for example many dicot taxa have a dominant taproot, while monocots, such as cereals, form nodal roots from shoot nodes (Hochholdinger et al., 2004; Lynch and Brown, 2012; Rich and Watt, 2013). Adult maize root systems consist of primary, seminal, crown (belowground nodal) and brace (aboveground nodal) roots, all these classes form lateral roots. For monocotyledons, nodal roots are the main parent axes of lateral roots present at depth as these laterals proliferate from nodal roots (Cairns et al., 2004; Nagel et al., 2012).
Genotypic variation for lateral root phenotypes has functional consequences in maize (Postma et al., 2014; Zhan et al., 2015; Zhan and Lynch, 2015; Jia et al., 2018). Root classes have different elongation rates that vary greatly as a function of time. For maize, lateral roots have been found to elongate at 2.2 cm day−1 for 2.5 days, while nodal roots elongated at a rate of 3 cm day−1 over a 5 week period (Cahn et al., 1989). Under non-impeded conditions primary roots of maize elongated at 4.8 cm day−1, while seminals only elongated at 3.2 cm day-1 (Veen and Boone, 1990). Differences in elongation rates between root types can lead to soils being differentially explored with time by each root type and could affect the volume and depth of bulk soil that can be explored within a certain time by different root types. Biomechanical properties also vary according to root class, with seminal roots being stronger than lateral roots (Loades et al., 2013). Whether this translates to specific penetration ability under impeded soil conditions according to root class remains to be investigated. It has been hypothesised that the contrasting phenotypes of distinct root classes adds to a plants’ plasticity and flexibility when interacting with different environments (Chochois et al., 2015; Wu et al., 2016) but the functional implications of the differential effects of mechanical impedance on distinct root classes are poorly understood.
Root system size differs among genotypes and different soil conditions (Gao and Lynch, 2016; Nakhforoosh et al., 2014). Root system size, expressed as total root length or root length density, can be split between coarse and fine roots (Cahn et al., 1989; Steinemann et al., 2015; Varney et al., 1991). Small grain cereals such as wheat or barley are characterised by fine axial roots, maize has thicker axial roots, while dicots and perennials have very coarse axial roots. But for all these species, a distinction between main root axes and smaller diameter lateral roots can be made. Coarser roots are needed in order to deploy finer roots within the soil profile. Studies on wheat suggest that wheat genotypes with more root axes have greater penetration of wax layers (Whalley et al., 2013).
Mechanical impedance not only affects root growth, it also has an impact on shoot growth. Root to shoot ratios can decrease under compaction (Andrade et al., 1993; Hoffmann and Jungh, 1995; Pfeifer et al., 2014a). Aboveground plant growth is impacted as leaf elongation rates can be reduced (Andrade et al., 1993; Young et al., 1997) and the rate of leaf appearance decreases (Beemster and Masle, 1996) when roots experience mechanical impedance. The reduction of shoot and root growth due to mechanical impedance can result in decreasing yield (Kirkegaard et al., 1992; de Moreas et al., 2020).
Better root growth under mechanical impedance can be attributed to different traits. For instance, the frictional component of mechanical impedance is reduced when roots produce mucilage or border cell sloughing (Iijima et al., 2000, 2004; Bengough and McKenzie, 1997). Smaller root tip radius to length ratios are linked to greater elongation rates under mechanical impedance (Colombi et al., 2017b). Another beneficial trait is the presence of root hairs which can provide anchorage for roots to cross from loose to harder soil layers (Bengough et al., 2011; Haling et al., 2013). Root hairs also maintain water uptake when soils dry (Carminati et al., 2017). Root anatomical traits such as greater cortical cell diameter have been linked to reduced energy costs under impeded conditions (Colombi et al., 2019). It has been suggested that smaller outer cortical cells prevent buckling, which facilitate penetration of harder layers (Chimungu et al., 2015).
Genotypes can adjust their root distribution with depth in response to compaction (Barraclough and Weir, 1988) however few studies have compared different genotypes and their redistribution of roots under compaction. Little is known about root system size for those root systems that do manage to grow deeper in compacted soils. The hypothesis that rooting depth and root length are not related to each other on compacted plots was tested for deeper rooting genotypes.
Section snippets
Plant material and growth conditions
Twelve maize (Zea mays L.) recombinant inbred lines from a study by Chimungu et al. (2015) were selected for different levels of root penetrability of a wax layer. These genotypes were planted in a split-plot design in order to study their root growth in compacted conditions at two field sites. Seeds were obtained from Dr. Shawn Kaeppler (University of Wisconsin, Madison WI, USA – Genetics Cooperations Stock Center, Urbana, IL, USA). Genotypes were grown at the Apache Root Biology Centre
Decrease in root length on compacted soil depends on field site
Total root length (TRL) from ARBC (coarse-loam) soil cores was greater than the total root length in PSU (silt-loam) cores in both compacted and non-compacted plots (Fig. 2, S4). On coarse-loam (ARBC) total root length was reduced by 47.4 % on average across all genotypes when grown on the compacted plots and total root length was clearly reduced for each genotype (Fig. 2, Table 2). As total coarse root length represents only a small part of the total root length (Fig. 2), total root length
Discussion
In this study, on two different soils with compacted and non-compacted plots, we found total root length reduction due to compaction was field site dependent (Figs. 2, Table 2). Coarse root proportions were influenced by genotype at both field sites (Fig. 4, Table 2). Rooting depth of coarse and total roots were strongly correlated (Fig. 5). Root length and rooting depth variables were not correlated when plants were grown on compacted plots (Figs. 6, S5, S6, S7, S8). Our results support the
Conclusions
Rooting depth and root length were not correlated under impeded conditions. Different coarse rooting depths were reached by genotypes characterised by similar root system sizes. We suggest genotypes better adapted to impedance (and therefore rooting deeper) are less at risk of additional stresses such as nutrient deficiency, soil drying, lack of access to water and other environmental conditions. We hypothesise that excessive root formation will introduce greater competition for internal and
Author contributions
Dorien Vanhees: designed and conducted the experiments, analysed and interpreted the data, and wrote the article with contributions from all authors. Kenneth Loades and A. Glyn Bengough contributed to experimental design, data analysis and interpretation, and writing. Sacha Mooney co-supervised the dissertation research of Dorien Vanhees, and contributed to experimental design, data analysis and interpretation, and writing. Jonathan Lynch conceived the project, co-supervised the dissertation
Declaration of Competing Interest
The authors report no declarations of interest.
Acknowledgements
This research was supported by the Howard G. Buffett Foundation, the University of Nottingham and the James Hutton Institute. The James Hutton Institute receives funding from the Rural & Environment Science & Analytical Services Division of the Scottish Government. We thank Hannah Schneider, Stephanie Klein, Chris Strock, Kimo Jin and other members of the PSU roots lab for their help and support during the execution of these field trials.
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