A. Glyn Bengough

Rhizosphere: biophysics, biogeochemistry and ecological relevance

Life on Earth is sustained by a small volume of soil surrounding roots, called the rhizosphere. The soil is where most of the biodiversity on Earth exists, and the rhizosphere probably represents the most dynamic habitat on Earth; and certainly is the most important zone in terms of defining the quality and quantity of the Human terrestrial food resource. Despite its central importance to all life, we know very little about rhizosphere functioning, and have an extraordinary ignorance about how best we can manipulate it to our advantage. A major issue in research on rhizosphere processes is the intimate connection between the biology, physics and chemistry of the system which exhibits astonishing spatial and temporal heterogeneities. This review considers the unique biophysical and biogeochemical properties of the rhizosphere and draws some connections between them. Particular emphasis is put on how underlying processes affect rhizosphere ecology, to generate highly heterogeneous microenvironments. Rhizosphere ecology is driven by a combination of the physical architecture of the soil matrix, coupled with the spatial and temporal distribution of rhizodeposits, protons, gases, and the role of roots as sinks for water and nutrients. Consequences for plant growth and whole-system ecology are considered. The first sections address the physical architecture and soil strength of the rhizosphere, drawing their relationship with key functions such as the movement and storage of elements and water as well as the ability of roots to explore the soil and the definition of diverse habitats for soil microorganisms. The distribution of water and its accessibility in the rhizosphere is considered in detail, with a special emphasis on spatial and temporal dynamics and heterogeneities. The physical architecture and water content play a key role in determining the biogeochemical ambience of the rhizosphere, via their effect on partial pressures of O2 and CO2, and thereby on redox potential and pH of the rhizosphere, respectively. We address the various mechanisms by which roots and associated microorganisms alter these major drivers of soil biogeochemistry. Finally, we consider the distribution of nutrients, their accessibility in the rhizosphere, and their functional relevance for plant and microbial ecology. Gradients of nutrients in the rhizosphere, and their spatial patterns or temporal dynamics are discussed in the light of current knowledge of rhizosphere biophysics and biogeochemistry. Priorities for future research are identified as well as new methodological developments which might help to advance a comprehensive understanding of the co-occurring processes in the rhizosphere.

Root elongation, water stress, and mechanical impedance: a review of limiting stresses and beneficial root tip traits

Root elongation in drying soil is generally limited by a combination of mechanical impedance and water stress. Relationships between root elongation rate, water stress (matric potential), and mechanical impedance (penetration resistance) are reviewed, detailing the interactions between these closely related stresses. Root elongation is typically halved in repacked soils with penetrometer resistances >0.8-2 MPa, in the absence of water stress. Root elongation is halved by matric potentials drier than about -0.5 MPa in the absence of mechanical impedance. The likelihood of each stress limiting root elongation is discussed in relation to the soil strength characteristics of arable soils. A survey of 19 soils, with textures ranging from loamy sand to silty clay loam, found that ∼10% of penetration resistances were >2 MPa at a matric potential of -10 kPa, rising to nearly 50% >2 MPa at - 200 kPa. This suggests that mechanical impedance is often a major limitation to root elongation in these soils even under moderately wet conditions, and is important to consider in breeding programmes for drought-resistant crops. Root tip traits that may improve root penetration are considered with respect to overcoming the external (soil) and internal (cell wall) pressures resisting elongation. The potential role of root hairs in mechanically anchoring root tips is considered theoretically, and is judged particularly relevant to roots growing in biopores or from a loose seed bed into a compacted layer of soil.

Root phenomics of crops: opportunities and challenges

Reliable techniques for screening large numbers of plants for root traits are still being developed, but include aeroponic, hydroponic and agar plate systems. Coupled with digital cameras and image analysis software, these systems permit the rapid measurement of root numbers, length and diameter in moderate (typically <1000) numbers of plants. Usually such systems are employed with relatively small seedlings, and information is recorded in 2D. Recent developments in X-ray microtomography have facilitated 3D non-invasive measurement of small root systems grown in solid media, allowing angular distributions to be obtained in addition to numbers and length. However, because of the time taken to scan samples, only a small number can be screened (typically <10 per day, not including analysis time of the large spatial datasets generated) and, depending on sample size, limited resolution may mean that fine roots remain unresolved. Although agar plates allow differences between lines and genotypes to be discerned in young seedlings, the rank order may not be the same when the same materials are grown in solid media. For example, root length of dwarfing wheat (Triticum aestivum L.) lines grown on agar plates was increased by ~40% relative to wild-type and semi-dwarfing lines, but in a sandy loam soil under well watered conditions it was decreased by 24-33%. Such differences in ranking suggest that significant soil environment-genotype interactions are occurring. Developments in instruments and software mean that a combination of high-throughput simple screens and more in-depth examination of root-soil interactions is becoming viable.

Disentangling the impact of AM fungi versus roots on soil structure and water transport

The relative importance of roots and AM-fungi on soil physical processes was investigated by controlling the presence of roots and AM fungi in pot experiments using a mycorrhiza-defective tomato mutant and a wild-type tomato (Solanum lycopersicum L.). Root-Zone and Bulk Soil sections were established by splitting pots into two lengthwise halves using a nylon mesh that contained roots whilst allowing the free movement of fungal hyphae. Post-incubation microbial populations and fungal biomass were measured and related to soil stability, pore structure and water repellency. Unplanted controls consistently had the least fungal biomass, fatty acids, water-stable aggregates (WSA) and water repellency. Wild-type-planted treatments had significantly more WSA than mycorrhiza-defective treatments (P < 0.01). Fluctuations in water content induced by transpiration caused significant changes in soil pore structure, measured using high-resolution X-Ray computer tomography. Porosity and mean pore size increased in soil aggregates from planted treatments, which had larger more heterogeneous pores than those in the unplanted soils. AM fungi accentuated soil stability. However, changes were not linked to repellency and fungal biomass. The presence of plants, regardless of AM fungi, appears to have the greatest impact on increasing soil stability.

Analyzing lateral root development: how to move forward.

Roots are important to plants for a wide variety of processes, including nutrient and water uptake, anchoring and mechanical support, storage functions, and as the major interface between the plant and various biotic and abiotic factors in the soil environment. Therefore, understanding the development and architecture of roots holds potential for the manipulation of root traits to improve the productivity and sustainability of agricultural systems and to better understand and manage natural ecosystems. While lateral root development is a traceable process along the primary root and different stages can be found along this longitudinal axis of time and development, root system architecture is complex and difficult to quantify. Here, we comment on assays to describe lateral root phenotypes and propose ways to move forward regarding the description of root system architecture, also considering crops and the environment.

Root growth models: towards a new generation of continuous approaches

Models of root system growth emerged in the early 1970s, and were based on mathematical representations of root length distribution in soil. The last decade has seen the development of more complex architectural models and the use of computer-intensive approaches to study developmental and environmental processes in greater detail. There is a pressing need for predictive technologies that can integrate root system knowledge, scaling from molecular to ensembles of plants. This paper makes the case for more widespread use of simpler models of root systems based on continuous descriptions of their structure. A new theoretical framework is presented that describes the dynamics of root density distributions as a function of individual root developmental parameters such as rates of lateral root initiation, elongation, mortality, and gravitropsm. The simulations resulting from such equations can be performed most efficiently in discretized domains that deform as a result of growth, and that can be used to model the growth of many interacting root systems. The modelling principles described help to bridge the gap between continuum and architectural approaches, and enhance our understanding of the spatial development of root systems. Our simulations suggest that root systems develop in travelling wave patterns of meristems, revealing order in otherwise spatially complex and heterogeneous systems. Such knowledge should assist physiologists and geneticists to appreciate how meristem dynamics contribute to the pattern of growth and functioning of root systems in the field.

Soil strength and macropore volume limit root elongation rates in many UK agricultural soils

BACKGROUND AND AIMS Simple indicators of crop and cultivar performance across a range of soil types and management are needed for designing and testing sustainable cropping practices. This paper determined the extent to which soil chemical and physical properties, particularly soil strength and pore-size distribution influences root elongation in a wide range of agricultural top soils, using a seedling-based indicator. METHODS Intact soil cores were sampled from the topsoil of 59 agricultural fields in Scotland, representing a wide geographic spread, range of textures and management practices. Water release characteristics, dry bulk density and needle penetrometer resistance were measured on three cores from each field. Soil samples from the same locations were sieved, analysed for chemical characteristics, and packed to dry bulk density of 1.0 g cm(-3) to minimize physical constraints. Root elongation rates were determined for barley seedlings planted in both intact field and packed soil cores at a water content close to field capacity (-20 kPa matric potential). KEY RESULTS Root elongation in field soil was typically less than half of that in packed soils. Penetrometer resistance was typically between 1 and 3 MPa for field soils, indicating the soils were relatively hard, despite their moderately wet condition (compared with <0.2 MPa for packed soil). Root elongation was strongly linked to differences in physical rather than chemical properties. In field soil root elongation was related most closely to the volume of soil pores between 60 µm and 300 µm equivalent diameter, as estimated from water-release characteristics, accounting for 65.7 % of the variation in the elongation rates. CONCLUSIONS Root elongation rate in the majority of field soils was slower than half of the unimpeded (packed) rate. Such major reductions in root elongation rates will decrease rooting volumes and limit crop growth in soils where nutrients and water are scarce.

Root hairs improve root penetration, root–soil contact, and phosphorus acquisition in soils of different strength

Root hairs are a key trait for improving the acquisition of phosphorus (P) by plants. However, it is not known whether root hairs provide significant advantage for plant growth under combined soil stresses, particularly under conditions that are known to restrict root hair initiation or elongation (e.g. compacted or high-strength soils). To investigate this, the root growth and P uptake of root hair genotypes of barley, Hordeum vulgare L. (i.e. genotypes with and without root hairs), were assessed under combinations of P deficiency and high soil strength. Genotypes with root hairs were found to have an advantage for root penetration into high-strength layers relative to root hairless genotypes. In P-deficient soils, despite a 20% reduction in root hair length under high-strength conditions, genotypes with root hairs were also found to have an advantage for P uptake. However, in fertilized soils, root hairs conferred an advantage for P uptake in low-strength soil but not in high-strength soil. Improved root-soil contact, coupled with an increased supply of P to the root, may decrease the value of root hairs for P acquisition in high-strength, high-P soils. Nevertheless, this work demonstrates that root hairs are a valuable trait for plant growth and nutrient acquisition under combined soil stresses. Selecting plants with superior root hair traits is important for improving P uptake efficiency and hence the sustainability of agricultural systems.

On boundary conditions in the lattice Boltzmann model for advection and anisotropic dispersion equation

A mirror-image method is proposed in this paper to solve the boundary conditions in the lattice Boltzmann model proposed by Zhang et al. [Adv. Water Resour. 25 (2002) 1] for the advection and anisotropic dispersion of solute transport in porous media. Three types of boundary are considered: prescribed concentration boundary, prescribed flux boundary and prescribed concentration-gradient boundary. The accuracy of the proposed method is verified against benchmark problems and finite difference method.

Understanding the genetic control and physiological traits associated with rhizosheath production by barley (Hordeum vulgare)

There is an urgent need for simple rapid screens of root traits that improve the acquisition of nutrients and water. Temperate cereals produce rhizosheaths of variable weight, a trait first noted on desert species sampled by Tansley over 100 yr ago. This trait is almost certainly important in tolerance to abiotic stress. Here, we screened association genetics populations of barley for rhizosheath weight and derived quantitative trait loci (QTLs) and candidate genes. We assessed whether rhizosheath weight was correlated with plant performance and phosphate uptake under combined drought and phosphorus deficiency. Rhizosheath weight was investigated in relation to root hair length, and under both laboratory and field conditions. Our data demonstrated that rhizosheath weight was correlated with phosphate uptake under dry conditions and that the differences in rhizosheath weight between genotypes were maintained in the field. Rhizosheath weight also varied significantly within barley populations, was correlated with root hair length and was associated with a genetic locus (QTL) on chromosome 2H. Putative candidate genes were identified. Rhizosheath weight is easy and rapid to measure, and is associated with relatively high heritability. The breeding of cereal genotypes for beneficial rhizosheath characteristics is achievable and could contribute to agricultural sustainability in nutrient- and water-stressed environments.