New frontiers in root biology: understanding complexity in roots and root systems
The structure and function of plant roots and their interactions with soil are exciting frontiers for advancing agriculture, providing global food security and sustaining ecosystem management. ( Ryan et al. (pp. 555–559 )).
Roots provide a fascinating array of structural and functional diversity. The papers in this root biology Special Issue represent a wide range of root research, encompassing spatial dimensions spanning from the gene to the roots’ land-use systems, providing opportunities for advancements in the field of root biology and furthering our knowledge of the fundamental aspects of root anatomy, growth, signalling and genetics, the functionality of roots for water and nutrient uptake, and the wider interaction of roots within the soil biome.
Rhizosphere biophysics and root water uptake
The combination of soil drying and a high transpiration rate causes severe water stress in plants. In their Viewpoint article, Carminati et al. (pp. 561–571 ) develop a biophysical model to describe how low soil moisture and high transpiration rates result in dramatic reduction of xylem water potential occurring across the rhizosphere as the soil dries, eventually leading to root dehydration and loss of contact with the soil. Plants adopt several mechanisms that could attenuate such drops in water potential and facilitate root water uptake. In particular, mucilage exudation and root hairs can act as a bridge between the root surface and the adjacent bulk soil, thereby maintaining the hydraulic connection across the rhizosphere.
Root system based limitations to agriculture
Improving root systems can be a step towards sustainable intensification in crop production. Using the contrasting wheat cropping systems of Australia and Denmark as examples, Thorup-Kristensen et al. (pp. 573–592 ) find that increased rooting depth is the most promising trait for improved water and nitrogen use. Root systems and depth can be improved through genetics and breeding. This review finds that contrasting cropping systems, together with effective agricultural management schemes, frequently have a greater impact on the successful development of deeper, thriving root systems. The extent of the deeper rooting is also shown to be determined by the management of both crop and field in the months and years before crop production, by affecting the availability of nutritional resources in the lower soil layers.
Root adaptations to infertile soils
Phenotypic characterisation of root adaptations to infertile soils enables plant breeders to develop improved cultivars that not only yield more, but also contribute to yield stability and nutritional security in the face of climate variability. Rao et al. (pp. 593–605 ) review the adaptive responses of root systems to soils with low fertility and aluminum toxicity. A number of root architectural, morphological, anatomical and metabolic phenes contribute to the superior performance and yield of soils with low fertility and aluminum toxicity. Major advances have been made in identifying root phenes in order to improve adaptation to soils with low nitrogen, low phosphorus or high aluminum. Advanced root phenotyping tools could help to develop new cultivars that are better adapted to soils with low fertiity and aluminum toxicity.
Aminotransferases provide the signals for root growth
Uncovering the role of new aminotransferases in the regulation of the signals behind root growth, Le Deunff et al. (pp. 607–620 ) show that l -aminoethoxyvinylglycine (AVG) acts as an ethylene and auxin biosynthesis inhibitor. AVG is also shown to inhibit other aminotransferases implied in nitrogen metabolism. Given the central role played by aminotransferases in nutrient and carbon shuttling and hormone biosynthesis, this review concludes that an identification of aminotransferases’ targets and an understanding of the interactions between ethylene levels and nitrogen metabolism can contribute to the development of a root morphogenetic programme. This aims for improved efficiency of nitrate absorption rates.
Deep roots and their functions in ecosystems
Deep roots determine many ecosystem services but remain understudied, due to the challenges involved in the observation and measurement of deep roots. In this paper, Pierret et al. (pp. 621–635 ) show that root structures and functions differ according to their depth and suggest that deep rooting systems could be more widespread than was previously thought. Many accepted hypotheses about root traits and the drivers governing root functioning have been predominantly based upon observations and models of shallow rather than deep roots. The authors present examples to suggest that the position of roots within the soil profile determines their different structures and roles in major biochemical cycles. Formulating a framework for the analysis of deep root growth and functioning, this review proposes that increased knowledge pertaining to the deep rooting traits of a variety of crops and plants could have scope to influence the effective management of natural and cultivated ecosystems.
Phosphoenolpyruvate carboxylase activation by reversible phosphorylation in white lupin cluster roots
Phosphoenolpyruvate carboxylase (PEPC) is a tightly regulated enzyme that controls carbohydrate partitioning to organic acid anions (malate, citrate) that are excreted in copious amounts by cluster (proteoid) roots of phosphate-deprived white lupin. Shane et al . (pp. 637–643 ) establish a novel mechanistic link between reversible, light-dependent activation of PEPC by in vivo phosphorylation, and the concentrations of sucrose, and its signalling metabolite trehalose-6-phosphate in lupin cluster roots. PEPC’s phosphorylation is correlated with enhanced rates of root organic anion exudation and phosphate uptake, and appears to be modulated by sucrose translocated from illuminated CO 2 -fixing leaves into the non-photosynthetic cluster roots.
Ethylene affects cell wall remobilisation
Seeking to uncover the effects of ethylene on the metabolic process and pectin remobilising capacity of rice ( Oryza sativa ) that is grown in phosphorus (P)-deficient conditions, Zhu et al. (pp. 645–653 ) find that ethylene positively regulates the cell wall pectin content of two rice cultivars. Mediated by the expression of OsPT2, more soluble P was released to the root and translocated to the shoots, and more recycled soluble P and ethylene content was found in cultivar Nipponbare, compared with Kasalath.
Seedling root traits correlate with yield in Brassica napus
Aiming to discover an optimum, cost-effective technique which can be applied to the selection of root traits for crop improvement, Thomas et al. (pp. 655–665 ) screen seedling root traits of elite oilseed rape (OSR; Brassica napus ) varieties in a low-cost, high-throughput root phenotyping (HTP) system. The same canola varieties were grown to maturity according to conventional practices, at two UK field sites each year for three years. Seedling primary root length (PRL) in the HTP system is shown to correlate with seed yield, early shoot vigour and emergence in most of the field experiments. Some associations between lateral root density (LRD) and nutrient uptake relating to calcium and zinc concentrations in the leaves can be observed and the authors conclude that it may be possible to use HTP systems to screen for beneficial root traits in more genetically diverse, non-field-adapted OSR.
Asymmetrical root development as a reaction to abiotic stresses
Roots can develop resilience and protective barriers to drought and cadmium-induced (Cd) stress. Líška et al. (pp. 667–674 ) study the ways in which the vascular tissues of roots develop characteristics to mitigate the effects of local abiotic stressors, and report that contact with air, or with toxic metals such as cadmium, induces an earlier and asymmetrical development of the cell wall polymer suberin lamellae in both the endodermis and the exodermis on the exposed side of the primary root surface of maize. Suberin provides a barrier to the movement of water and solutes. Moreover, local Cd exposure induces early differentiation of the endodermis in the exposed area and in basipetally localized tissues. As a result of these physiological responses, the root endodermis and exodermis provide protection for the plant's vascular tissues against abiotic stresses.
Aquatic adventitious roots of alligator weed and capacity for oxygen absorption
The formation of aquatic adventitious roots is a common response of terrestrial plants to flooding. Previous research has found that aquatic adventitious roots on submerged plants can absorb water and nutrients, but no experimental evidence hitherto has shown that adventitious roots can absorb oxygen, which benefits the submerged plants. In this study, Ayi et al. (pp. 675–683 ) demonstrate that the aquatic adventitious roots of alligator weed ( Alternanthera philoxeroides ) formed upon submergence can absorb O 2 from ambient water, thereby increasing the oxygen content in plant tissues. This enables the efficient utilization of carbohydrates for vigorous root growth and extending the plant’s life-cycle.
Maize root growth responses to penetration of a bilayered soil
Studying the influence of soil strength on root growth dynamics, Popova et al. (pp. 685–698 ) document the mechanical and tropic responses of primary roots of maize ( Zea mays ) seedlings further to penetration of a bilayered soil consisting of loose loamy sand on top and a coarser, denser layer beneath. Upon reaching the compacted soil in the lower layer, the elongation rate of the primary roots nearly halved and the tortuosity and deflection of the root path significantly changed in response to contact with the changing soil texture. The resulting ‘waviness’ of the root serves as a key indicator of the maize roots’ response to touch stimuli as they encounter a changing physical soil environment.
The effect of hybridisation on root depth distribution of white clover
Although white clover ( Trifolium repens ) is a major temperate legume, its production is limited by low soil moisture. Using 1m deep sand culture, Nichols et al. (pp. 699–710 ) examined the effect of hybridisation with the wild relative T. uniflorum on rooting depth and root depth distribution. They found that hybridisation affected various root characteristics, most likely reflecting edaphic adaptations from the T. uniflorum parent. Roots of the hybrids penetrated deeper than white clover, but distribution of root mass was similar to T. uniflorum . The changes in root traits and architecture which result from these targeted breeding strategies may improve access to water, but also to soil phosphorus. Consequently these results could have wide-reaching implications for improved pasture production.
Root hydraulics of drought-tolerant and susceptible rice varieties
Drought-tolerant and drought-susceptible rice ( Oryza sativa ) varieties have previously been shown to exhibit different trends in root hydraulic traits. Henry et al. (pp. 711–724 ) carry out an investigation to measure root xylem sap bleeding rates and root hydraulic conductivity in order to understand how environmental factors affect the physiological features of these groupings. The study shows that varietal differences in root hydraulic properties are partly explained by transpiration rates and levels of irradiance in the field, and also by the physiological traits governing osmotic potential, such as suberin content. By affecting water movement within the plant, such varietal differences in root hydraulic properties may provide important resources for further improving and understanding the drought responses of rice.
Soil bacteria can promote or inhibit the formation of root clusters
Root clusters (also known as proteoid or cluster roots) are bunches of hairy rootlets recorded in > 1800 species from nine families so far. The possible involvement of microorganisms in root cluster formation has produced conflicting results over the last 40 years. Lamont et al. (pp. 725–732 ) show that there are circumstances where soil bacteria can promote or inhibit root-cluster formation in their study of the effects of inoculation with seven different bacterial strains and nitrogen treatments on three different genera: Leucadendron (protea) from the Cape of South Africa, Viminaria (legume) from Australia and Lupinus (legume) from Europe. The outcome, whether promotion or inhibition of root cluster formation, depends on the identity of bacterium used, the identity of the host species and the nutritional environment, specifically nitrogen status. Thus, growth promoting bacteria can be described as having a facultatively beneficial influence on plants.
Unravelling the roots of lianas
Woody vines collectively known as lianas are fundamental components of tropical forests but their root structure is largely unexplored. Stems of Sapindaceae display diverse architectures and an anatomical pattern typical of climbing plants. Bastos et al. (pp. 733–746 ) explore the root structure of well-developed roots in numerous lianoid genera of this family. All roots exhibited a lianescent anatomy marked by the presence of vessel dimorphism but most lacked cambial variants. Exceptions were observed such as the lobed roots of Urvillea rufescens and phloem wedges in Serjania lethalis and Serjania caracasana . Neo-formed peripheral vascular strands and cylinders were common in mature roots of Serjania caracasana . Vascular connections were found uniting peripheral and central vascular cylinders through phloem wedges, as revealed by anatomical and micro-CT analyses. The study provides an overview of the diverse traits, architectural structures and underlying mechanisms of lianas’ roots.
Anchorage failure is prevented by a rigid central part of the root system
Storms can cause catastrophic damage to European forests. Surmising that anchorage is partly determined by root architecture, Dorval et al. (pp. 747–762 ) computed the mechanical characteristics of the main components of root systems from 3D digitising data of 48 undamaged, leaning or heavily toppled Pinus pinaster trees from stands damaged by a storm 3 years previously. The results show that it was mainly the flexural stiffness of the large main taproot at the central part of the root system that secured anchorage, preventing leaning and stump displacement. The distal section of the taproot and attached deep roots contributed to strong anchorage support and toppled trees were shown to have a lower relative root biomass - stump excluded - than straight trees. A variety of architectural root designs can provide good anchorage for trees, depending partly on available soil depth.
Mapping developmental zones at the root apex using the multiple structural change algorithm
In the root apex, cell length is a function of its position within a cell file. Applying a mathematical approach using a multiple structural change (MSC) algorithm, Pacheco-Escobedo et al. (pp. 763–776 ) developed a spatial model to identify that the growing part of Arabidopsis root is composed of three discrete developmental zones: the proliferation domain (PD), the transition domain (TD), and the elongation zone (EZ). The PD and the TD comprise the root apical meristem (RAM). The MSC approach enables unambiguous, rapid, and automated determination of the RAM/ EZ and the PD/TD boundaries. This publicly available tool facilitates root phenotyping of different genetic backgrounds and experimental treatments.
Aquaporin function and exogenous application of abscisic acid (ABA) to barley roots
Using an immunochemical approach to reveal the link between changes in abscisic acid (ABA) levels, aquaporin function and changes in root cell hydraulic conductivity (Lp Cell ), Sharipova et al . (pp. 777–785 ) compared the abundance of AQPs and ABA by means of immunolocalization in the tissue of barley ( Hordeum vulgare ) roots, and related it to Lp Cell. Shortly after (< 2 hours) ABA application to the roots of ABA-deficient barley, increased tissue ABA concentrations and AQP abundance (especially the plasma-membrane localised isoforms HvPIP2;1 and HvPIP2;2) were spatially correlated in root epidermal cells and the cortical cell layer located beneath, in conjunction with increased Lp Cell of the cortical cells.
The role of XAL1 in the root cell dynamics underpinning root growth
Morphogenesis depends on the modulation of cell proliferation and differentiation . The reverse genetics approach of García-Cruz et al. (pp. 787–796 ) reveals that such modulation is dynamically adjusted in response to various signals via a complex transcriptional regulatory network that mediates between such signals and cell-cycle regulation and cell-fate decisions resulting in proliferation, growth or differentiation. XAL1 ( AGL12 ) is a MADS-box transcription factor and an important component of such networks. This gene participates in root meristem proliferation by regulating cell-cycle components. Interestingly, overexpression of XAL1 is able to affect stem-cell divisions. The study shows that XAL1 is involved in the modulation of cell proliferation to differentiation, transitioning the entrance to the endoreplicative cell cycle during root development.
Galactose-containing enriched root exudates of potato interfere with the growth of Pectobacterium atrosepticum
Potato ( Solanum tuberosum ) is a major food crop worldwide and its cultivation is fraught with difficulty. This is because potato roots and tubers are susceptible to many devastating diseases caused by soil-borne pathogens. Previous research on potato has been dedicated mainly to the tubers, with less research available on potato root structure and function, the processes of potato root exudation and the production of root border cells. Koroney et al. (pp. 797–808 ) show that root exudates from S. tuberosum are radically enriched by galactose-containing molecules, including arabinogalactan proteins. The composition of potato root exudates is shown to be affected in response to elicitors from Pectobacterium atrosepticum . These findings indicate that the galactose-containing polymers of potato root exudates play a central role in root-microbe interactions, interfering with the growth of P. atrosepticum.
Shoot control of root aquaporin expression in rice
Seeking to uncover the responses of root hydraulics and water uptake to transpirational water loss, Meng et al. (pp. 809–819 ) analyse three-week old rice plants, observing changes in root aquaporin expression and hydraulic conductivity (Lp) in response to shoot removal. A rapid decrease (5-60 min) in gene expression (qPCR) of root plasma membrane intrinsic aquaporin proteins (PIPs) is shown to result from shoot removal in rice. Lp decreased in parallel. Application of tension, using a vacuum pump, to detached root systems prevented the decrease in aquaporin expression. The study concludes that xylem tension produces a signal which coordinates and connects root and shoot hydraulics.
Root-mediated transmission of systemic acquired resistance
Plants modulate their defence signalling networks in response to various biotic stresses via inter-organ communication. Song et al. (pp. 821–832 ) evaluate the root-mediated transmission of systemic acquired resistance (SAR) in response to soil-borne and air-borne plant pathogens. The SAR-triggering chemical benzothiadiazole (BTH) induces a SAR signal which is transmitted through the root-to-root system from SAR-induced plants to neighbouring plants subjected to local chemical and pathogenic bacteria. Salicylic acid (SA) is shown to be a major signal molecule in this SAR transmission through the root system.
Deep root biomass and bNPP of a coffee agroforestry system in Costa Rica
Costa Rican coffee ( Coffea arabica ) plants are often grown in agroforests. Studying the relationship between shade-inducing trees on coffee plant biomass and root competition in the topsoil, and overall belowground net primary productivity (bNPP), Defrenet et al. (pp. 833–851 ) estimate root biomass and bNPP at the stand level, taking into account deep roots and the positioning of coffee plants in relation to trees. Coffee root systems are shown to comprise 49% of the total plant biomass; such a high ratio is possibly a consequence of shoot pruning. There was no significant impact of shade-inducing trees on the fine root biomass (2.3 t ha-1), suggesting that coffee root systems are very competitive in the topsoil.
Hydraulic conductivity of roots
Radial and axial hydraulic conductivities are key parameters for understanding and modelling root water uptake. Despite their importance, there is limited experimental information relating to how the radial and axial hydraulic conductivities vary along roots growing in soil. Zarebanadkouki et al. (pp. 853–864 ) adopt a new approach to estimating the profiles of hydraulic conductivities using a three-dimensional model of root water uptake and a neutron radiography technique applied to the roots of transpiring lupine plants grown in soil.
Asymmetric responses of the woody poplar taproot axis to bending stress
Mechanical bending stress can result in cell wall strengthening and increased wood formation across root axes together with an attendant asymmetrical accumulation of phytohormones. De Zio et al. (pp. 865–883 ) show how different mechanical force intensities act across the compressed concave and stretched convex sides of the woody bent poplar taproot. The results show that, in contrast to the response of the poplar stem, bending stress applied to woody poplar taproots results in increased wood formation toward the concave side (compressed zone), characterized by the highest values of quantity of cambial cells, xylem thickness and lignin content. The highest quantity of lateral roots is revealed in the stretched zone of the convex side, which constitutes the site for an asymmetrical accumulation of auxin, the phytohormone responsible for triggering lignin deposition and cell wall strengthening in the concave sides.