Rhizobacterial mediation of plant hormone status

Plant growth-promoting rhizobacteria are commonly found in the rhizosphere (adjacent to the root surface) and may promote plant growth via several diverse mechanisms, including the production or degradation of the major groups of plant hormones that regulate plant growth and development. Although rhizobacterial production of plant hormones seems relatively widespread (as judged from physico-chemical measurements of hormones in bacterial culture media), evidence continues to accumulate, particularly from seedlings grown under gnotobiotic conditions, that rhizobacteria can modify plant hormone status. Since many rhizobacteria can impact on more than one hormone group, bacterial mutants in hormone production/degradation and plant mutants in hormone sensitivity have been useful to establish the importance of particular signalling pathways. Although plant roots exude many potential substrates for rhizobacterial growth, including plant hormones or their precursors, limited progress has been made in determining whether root hormone efflux can select for particular rhizobacterial traits. Rhizobacterial mediation of plant hormone status not only has local effects on root elongation and architecture, thus mediating water and nutrient capture, but can also affect plant root-to-shoot hormonal signalling that regulates leaf growth and gas exchange. Renewed emphasis on providing sufficient food for a growing world population, while minimising environmental impacts of agriculture because of overuse of fertilisers and irrigation water, will stimulate the commercialisation of rhizobacterial inoculants (including those that alter plant hormone status) to sustain crop growth and yield. Combining rhizobacterial traits (or species) that impact on plant hormone status thereby modifying root architecture (to capture existing soil resources) with traits that make additional resources available (e.g. nitrogen fixation, phosphate solubilisation) may enhance the sustainability of agriculture.     

Root-targeted biotechnology to mediate hormonal signalling and improve crop stress tolerance

Since plant root systems capture both water and nutrients essential for the formation of crop yield, there has been renewed biotechnological focus on root system improvement. Although water and nutrient uptake can be facilitated by membrane proteins known as aquaporins and nutrient transporters, respectively, there is a little evidence that root-localised overexpression of these proteins improves plant growth or stress tolerance. Recent work suggests that the major classes of phytohormones are involved not only in regulating aquaporin and nutrient transporter expression and activity, but also in sculpting root system architecture. Root-specific expression of plant and bacterial phytohormone-related genes, using either root-specific or root-inducible promoters or grafting non-transformed plants onto constitutive hormone producing rootstocks, has examined the role of root hormone production in mediating crop stress tolerance. Root-specific traits such as root system architecture, sensing of edaphic stress and root-to-shoot communication can be exploited to improve resource (water and nutrients) capture and plant development under resource-limited conditions. Thus, root system engineering provides new opportunities to maintain sustainable crop production under changing environmental conditions.     

Genetic approach towards the identification of auxin-cytokinin crosstalk components involved in root development

Phytohormones are important plant growth regulators that control many developmental processes, such as cell division, cell differentiation, organogenesis and morphogenesis. They regulate a multitude of apparently unrelated physiological processes, often with overlapping roles, and they mutually modulate their effects. These features imply important synergistic and antagonistic interactions between the various plant hormones. Auxin and cytokinin are central hormones involved in the regulation of plant growth and development, including processes determining root architecture, such as root pole establishment during early embryogenesis, root meristem maintenance and lateral root organogenesis. Thus, to control root development both pathways put special demands on the mechanisms that balance their activities and mediate their interactions. Here, we summarize recent knowledge on the role of auxin and cytokinin in the regulation of root architecture with special focus on lateral root organogenesis, discuss the latest findings on the molecular mechanisms of their interactions, and present forward genetic screen as a tool to identify novel molecular components of the auxin and cytokinin crosstalk.     

Genetic approach towards the identification of auxin–cytokinin crosstalk components involved in root development

Phytohormones are important plant growth regulators that control many developmental processes, such as cell division, cell differentiation, organogenesis and morphogenesis. They regulate a multitude of apparently unrelated physiological processes, often with overlapping roles, and they mutually modulate their effects. These features imply important synergistic and antagonistic interactions between the various plant hormones. Auxin and cytokinin are central hormones involved in the regulation of plant growth and development, including processes determining root architecture, such as root pole establishment during early embryogenesis, root meristem maintenance and lateral root organogenesis. Thus, to control root development both pathways put special demands on the mechanisms that balance their activities and mediate their interactions. Here, we summarize recent knowledge on the role of auxin and cytokinin in the regulation of root architecture with special focus on lateral root organogenesis, discuss the latest findings on the molecular mechanisms of their interactions, and present forward genetic screen as a tool to identify novel molecular components of the auxin and cytokinin crosstalk.     

Root system architecture: insights from Arabidopsis and cereal crops

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. Understanding the development and architecture of roots holds potential for the exploitation and manipulation of root characteristics to both increase food plant yield and optimize agricultural land use. This theme issue highlights the importance of investigating specific aspects of root architecture in both the model plant Arabidopsis thaliana and (cereal) crops, presents novel insights into elements that are currently hardly addressed and provides new tools and technologies to study various aspects of root system architecture. This introduction gives a broad overview of the importance of the root system and provides a snapshot of the molecular control mechanisms associated with root branching and responses to the environment in A. thaliana and cereal crops.     

Strigolactones are regulators of root development

Strigolactones (SLs) have been defined as a new group of plant hormones or their derivatives that suppress lateral shoot branching. Recently, a new role for SLs was discovered, in the regulation of root development. Strigolactones were shown to alter root architecture and affect root-hair elongation. Here, I review the recent findings regarding the effects of SLs on root growth and development, and their association with changes in auxin flux. The networking between SLs and other plant hormones that regulate root development is also presented. Strigolactone regulation of plant development suggests that they are coordinators of shoot and root development and mediators of plant responses to environmental conditions.     

Intrinsic and environmental response pathways that regulate root system architecture

Root system development is an important agronomic trait. The right architecture in a given environment allows plants to survive periods of water of nutrient deficit, and compete effectively for resources. Root systems also provide an optimal system for studying developmental plasticity, a characteristic feature of plant growth. This review proposes a framework for describing the pathways regulating the development of complex structures such as root systems: intrinsic pathways determine the characteristic architecture of the root system in a given plant species, and define the limits for plasticity in that species. Response pathways co-ordinate environmental cues with development by modulating intrinsic pathways. The current literature describing the regulation of root system development is summarized here within this framework. Regulatory pathways are also organized based on their specific developmental effect in the root system. All the pathways affect lateral root formation, but some specifically target initiation of the lateral root, while others target the development and activation of the lateral root primordium, or the elongation of the lateral root. Finally, we discuss emerging approaches for understanding the regulation of root system architecture.     

Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system

The postembryonic developmental program of the plant root system is plastic and allows changes in root architecture to adapt to environmental conditions such as water and nutrient availability. Among essential nutrients, phosphorus (P) often limits plant productivity because of its low mobility in soil. Therefore, the architecture of the root system may determine the capacity of the plant to acquire this nutrient. We studied the effect of P availability on the development of the root system in Arabidopsis. We found that at P-limiting conditions (<50 microM), the Arabidopsis root system undergoes major architectural changes in terms of lateral root number, lateral root density, and primary root length. Treatment with auxins and auxin antagonists indicate that these changes are related to an increase in auxin sensitivity in the roots of P-deprived Arabidopsis seedlings. It was also found that the axr1-3, axr2-1, and axr4-1 Arabidopsis mutants have normal responses to low P availability conditions, whereas the iaa28-1 mutant shows resistance to the stimulatory effects of low P on root hair and lateral root formation. Analysis of ethylene signaling mutants and treatments with 1-aminocyclopropane-1-carboxylic acid showed that ethylene does not promote lateral root formation under P deprivation. These results suggest that in Arabidopsis, auxin sensitivity may play a fundamental role in the modifications of root architecture by P availability.     

Auxin fluxes in the root apex co-regulate gravitropism and lateral root initiation

Root architecture plays an important role in water and nutrient acquisition and in the ability of the plant to adapt to the soil. Lateral root development is the main determinant of the shape of the root system and is controlled by external factors such as nutrient concentration. Here it is shown that lateral root initiation and root gravitropism, two processes that are regulated by auxin, are co-regulated in Arabidopsis. A mathematical model was generated that can predict the effects of gravistimulations on lateral root initiation density and suggests that lateral root initiation is controlled by an inhibitory fields mechanism. Moreover, gene transactivation experiments suggest a mechanism involving a single auxin transport route for both responses. Finally, co-regulation may offer a selective advantage by optimizing soil exploration as supported by a simple quantitative analysis.     

Endophyte roles in nutrient acquisition,root system architecture development and oxidative stress tolerance

Plants associate with communities of microbes (bacteria and fungi) that play critical roles in plant development, nutrient acquisition and oxidative stress tolerance. The major share of plant microbiota is endophytes which inhabit plant tissues and help them in various capacities. In this article, we have reviewed what is presently known with regard to how endophytic microbes interact with plants to modulate root development, branching, root hair formation and their implications in overall plant development. Endophytic microbes link the interactions of plants, rhizospheric microbes and soil to promote nutrient solubilization and further vectoring these nutrients to the plant roots making the soil-plant-microbe continuum. Further, plant roots internalize microbes and oxidatively extract nutrients from microbes in the rhizophagy cycle. The oxidative interactions between endophytes and plants result in the acquisition of nutrients by plants and are also instrumental in oxidative stress tolerance of plants. It is evident that plants actively cultivate microbes internally, on surfaces and in soils to acquire nutrients, modulate development and improve health. Understanding this continuum could be of greater significance in connecting endophytes with the hidden half of the plant that can also be harnessed in applied terms to enhance nutrient acquisition through the development of favourable root system architecture for sustainable production under stress conditions.     

Dynamic root growth and architecture responses to limiting nutrient availability: linking physiological models and experimentation

In recent years the study of root phenotypic plasticity in response to sub-optimal environmental factors and the genetic control of these responses have received renewed attention. As a path to increased productivity, in particular for low fertility soils, several applied research projects worldwide target the improvement of crop root traits both in plant breeding and biotechnology contexts. To assist these tasks and address the challenge of optimizing root growth and architecture for enhanced mineral resource use, the development of realistic simulation models is of great importance. We review this research field from a modeling perspective focusing particularly on nutrient acquisition strategies for crop production on low nitrogen and low phosphorous soils. Soil heterogeneity and the dynamics of nutrient availability in the soil pose a challenging environment in which plants have to forage efficiently for nutrients in order to maintain their internal nutrient homeostasis throughout their life cycle. Mathematical models assist in understanding plant growth strategies and associated root phenes that have potential to be tested and introduced in physiological breeding programs. At the same time, we stress that it is necessary to carefully consider model assumptions and development from a whole plant-resource allocation perspective and to introduce or refine modules simulating explicitly root growth and architecture dynamics through ontogeny with reference to key factors that constrain root growth. In this view it is important to understand negative feedbacks such as plant–plant competition. We conclude by briefly touching on available and developing technologies for quantitative root phenotyping from lab to field, from quantification of partial root profiles in the field to 3D reconstruction of whole root systems. Finally, we discuss how these approaches can and should be tightly linked to modeling to explore the root phenome.     

The nutritional control of root development

Root development is remarkably sensitive to variations in the supply and distribution of inorganic nutrients in the soil. Here we review examples of the ways in which nutrients such as N, P, K and Fe can affect developmental processes such as root branching, root hair production, root diameter, root growth angle, nodulation and proteoid root formation. The nutrient supply can affect root development either directly, as a result of changes in the external concentration of the nutrient, or indirectly through changes in the internal nutrient status of the plant. The direct pathway results in developmental responses that are localized to the part of the root exposed to the nutrient supply; the indirect pathway produces systemic responses and seems to depend on long-distance signals arising in the shoot. We propose the term `trophomorphogenesis' to describe the changes in plant morphology that arise from variations in the availability or distribution of nutrients in the environment. We discuss what is currently known about the mechanisms of external and internal nutrient sensing, the possible nature of the long-distance signals and the role of hormones in the trophomorphogenic response.     

植物根构型的定量分析

植物根系具有锚定植株、吸收和运输土壤中的水分及养分、合成和贮藏营养物质等重要功能。根构型是根系在土壤中的空间造型和分布。对植物根构型进行定量分析, 有助于人们了解根系结构和根系功能在生态系统中的重要作用。本文对植物根构型的概念及其定量分析研究进展进行了概述, 并介绍了植物根构型的主要研究方法和定量分析技术。     

植物根构型的定量分析

植物根系具有锚定植株、吸收和运输土壤中的水分及养分、合成和贮藏营养物质等重要功能。根构型是根系在土壤中的空间造型和分布。对植物根构型进行定量分析,有助于人们了解根系结构和根系功能在生态系统中的重要作用。本文对植物根构型的概念及其定量分析研究进展进行了概述,并介绍了植物根构型的主要研究方法和定量分析技术。     

Root architecture and hydraulic conductance in nutrient deprived Pistacia lentiscus L. seedlings

Plants respond to low nutrient availability by modifying root morphology and root system topology. Root responses to nitrogen (N) and phosphorus (P) limitation may affect plant capacity to withstand water stress. But studies on the effect of nutrient availability on plant ability to uptake and transport water are scarce. In this study, we assess the effect of nitrogen and phosphorus limitation on root morphology and root system topology in Pistacia lentiscus L seedlings, a common Mediterranean shrub, and relate these changes to hydraulic conductivity of the whole root system. Nitrogen and phosphorus deprivation had no effect on root biomass, but root systems were more branched in nutrient limited seedlings. Total root length was higher in seedlings subjected to phosphorus deprivation. Root hydraulic conductance decreased in nutrient-deprived seedlings, and was related to the number of root junctions but not to other architectural traits. Our study shows that changes in nutrient availability affect seedling water use by modifying root architecture. Changes in nutrient availability should be taken into account when evaluating seedling response to drought.     

Cytokinin-induced root growth involves actin filament reorganization

Root architecture is developmentally plastic and affected by many intrinsic factors (e.g. plant hormones) and extrinsic factors (e.g. touch, gravity) in order to maximize nutrient and water acquisition. We have recently shown that asymmetrical exposure of cytokinin (CK) at the root tip causes root growth directional changes that is dependent on ethylene signaling and is potentiated by glucose signaling. Auxin homeostasis as maintained by auxin signaling and transport is also involved in CK-induced root cell elongation and differential growth. The signaling pathways eventually converge at actin filament organization since actin filament organization inhibitor latrunculin B (Lat B) can also induce similar growth. We, show that CK can actually alter actin filament organization as seen in actin binding protein 35S::GFP-ABD2-GFP transgenic lines as is also altered by auxin polar transport inhibitor 1-N-naphthylphthalamic acid (NPA) and Lat B in different manners.     

Variation in root system traits among African semi‐arid savanna grasses: Implications for drought tolerance

In arid to semi‐arid grasslands and savannas, plant growth, population dynamics, and productivity are consistently and strongly limited by soil water and nutrient availability. Adaptive traits of the root systems of grasses in these ecosystems are crucial to their ability to cope with strong water and/or nutrient limitation and the increasing drought stress associated with ecosystem degradation or projected climate change. We studied 18 grass species in semi‐arid savanna of the Kalahari region of Botswana to quantify interspecific variation in three important root system traits including root system architecture, rhizosheath thickness and mycorrhizal colonization. Drought‐tolerant species and shorter‐lived species showed greater rhizosheath thickness and fine root development but lower mycorrhizal colonization compared to later successional climax grasses and those characteristic of wetter sites. In addition, there was a significant positive correlation between root fibrousness index and rhizosheath thickness among species and a weak negative correlation between root fibrousness index and mycorrhizal colonization. These patterns suggest that an extensive fine root system and rhizosheath development may be important complementary traits of grasses coping with drought conditions, the former aiding in the acquisition of water by the grass plant and the latter aiding in water uptake and retention, and reducing water loss in the rhizosphere. Within species, both rhizosheath development and mycorrhizal colonization were significantly greater in a wet year than in a year with below‐average precipitation. The observed patterns suggest that the primary benefit of rhizosheath development in African savanna grasses is improved drought tolerance and that it is a plastic trait that can be adjusted annually to changing environmental conditions. The functioning of mycorrhizal symbiosis is likely to be relatively more important in infertile savannas where nutrient limitation is higher relative to water limitation.     

The role of nutrient availability in regulating root architecture

The ability of plants to respond appropriately to nutrient availability is of fundamental importance for their adaptation to the environment. Nutrients such as nitrate, phosphate, sulfate and iron act as signals that can be perceived. These signals trigger molecular mechanisms that modify cell division and cell differentiation processes within the root and have a profound impact on root system architecture. Important developmental processes, such as root-hair formation, primary root growth and lateral root formation, are particularly sensitive to changes in the internal and external concentration of nutrients. The responses of root architecture to nutrients can be modified by plant growth regulators, such as auxins, cytokinins and ethylene, suggesting that the nutritional control of root development may be mediated by changes in hormone synthesis, transport or sensitivity. Recent information points to the existence of nutrient-specific signal transduction pathways that interpret the external and internal concentrations of nutrients to modify root development. Progress in this field has led to the cloning of regulatory genes that play pivotal roles in nutrient-induced changes to root development.