Root System Architecture In Response Research Articles

Efficient root systems for enhancing tolerance of crops to water and phosphorus limitation

Development of future crop varieties with efficient root systems for enhanced water and phosphorus uptake is essential for improving crop adaptation and hence food security. Root system architecture (RSA) traits that overcome low-water and low-phosphorus stresses are critical to maintaining structural and functional properties, and are considered the first-order targets in breeding programmes for rainfed environments. Modification of root system architecture could contribute to improvements of desirable agronomic and physiological traits such as biomass, yield, drought resistance, and tolerance to nutrient deficiencies. Advanced phenotyping, imaging, modelling and molecular biotechnologies offer promise in identifying RSA traits for efficient resource acquisition and adaptation to abiotic stresses. This review highlights the complexity and regulation of RSA in response to water and P stresses.

Identification of genomic regions regulating ammonium-dependent inhibition of primary root length in Arabidopsis thaliana

ABSTRACTPlant roots grow into the soil for efficient acquisition of various nutrients, such as inorganic nitrogen, ammonium, and nitrate. A previous study has revealed the genetic diversity of foliar functions of Arabidopsis thaliana ecotypes in an environment containing ammonium; however, the function of roots remains unclear. This work focuses on the root system architecture (RSA) of Arabidopsis ecotypes to investigate the genetic factors regulating ammonium-dependent RSA changes. Arabidopsis ecotypes were grown on vertical agar medium containing ammonium as a major nitrogen source, and root growth and RSA were determined. Arabidopsis ecotypes showed differential sensitivity to ammonium. The shoot dry weight of some ecotypes decreased, whereas that of other ecotypes increased in ammonium medium. The RSA changes also varied among the different ecotypes in response to ammonium. The total root length, measured as the sum of primary root and lateral root length, of some ecotypes was reduced, whereas that of other ecotypes showed no significant difference in ammonium medium. Compared with lateral roots, the primary roots showed a sharp response to ammonium supply. Notably, the RSA showed a partial correlation with shoot dry weight in ammonium medium. Because Col-4 and Ler-0 showed opposite RSA responses to ammonium supply, these two ecotypes were selected for further genetic analysis. Quantitative trait locus (QTL) analysis of recombinant inbred lines of Col and Ler showed the involvement of several genetic factors in ammonium-dependent RSA changes. Moreover, QTL analysis revealed that the primary structure of nitrogen-related enzymes do not account for changes in RSA in response to ammonium supply.

The possible interaction of ammonium and auxin polar transport on root system architectures in the two ecotypes of Arabidopsis thaliana

ABSTRACTPlant growth requires mineral nutrients from soil environment. It is important for plant to develop its root to import mineral nutrient from environment. Both inorganic nitrogen source and plant hormone auxin influence the root system architecture (RSA). Previous study indicated that polar auxin transport is partly involved in ammonium-inhibition of primary root in an Arabidopsis ecotype, Columbia 0 (Col-0); however, the effect of auxin in other ecotypes remains unclear. The purpose of this study is to describe and examine the effect of TIBA, an inhibitor for the auxin polar transport, in ammonium supply-dependent changes of root development. Two Arabidopsis ecotypes, Col-0 and Landsberg erecta 2 (Ler-2), were used due to their different response to ammonium supply. The changes of the RSA in response to ammonium supply on vertical agar medium containing three levels of TIBA and four levels of ammonium were determined in two ecotypes. The primary root length of Ler-2 was markedly shortened by increasing ammonium concentration in the medium, while that of Col-0 was relatively insensitive to ammonium. Conversely, the lateral root length of Ler-2 was increased by ammonium supply. Both primary and lateral root of Col-0 were more sensitive to TIBA than those of Ler-2. ANOVA indicated the significant interaction of TIBA and ammonium in Col-0; however, no interaction in Ler-2. These results suggested the genetic diversity in the interactive effect of auxin and ammonium.

Genetic diversity of root system architecture in response to drought stress in grain legumes.

Climate change has increased the occurrence of extreme weather patterns globally, causing significant reductions in crop production, and hence threatening food security. In order to meet the food demand of the growing world population, a faster rate of genetic gains leading to productivity enhancement for major crops is required. Grain legumes are an essential commodity in optimal human diets and animal feed because of their unique nutritional composition. Currently, limited water is a major constraint in grain legume production. Root system architecture (RSA) is an important developmental and agronomic trait, which plays vital roles in plant adaptation and productivity under water-limited environments. A deep and proliferative root system helps extract sufficient water and nutrients under these stress conditions. The integrated genetics and genomics approach to dissect molecular processes from genome to phenome is key to achieve increased water capture and use efficiency through developing better root systems. Success in crop improvement under drought depends on discovery and utilization of genetic variations existing in the germplasm. In this review, we summarize current progress in the genetic diversity in major legume crops, quantitative trait loci (QTLs) associated with RSA, and the importance and applications of recent discoveries associated with the beneficial root traits towards better RSA for enhanced drought tolerance and yield.

Physiological and genetic analysis for maize root characters and yield in response to low phosphorus stress.

Root system architecture (RSA) plays an important role in the acquisition of mineral nutrients. Nevertheless, RSA has seldom been selected as an important agricultural trait in conventional breeding programs. Little is known about the response of RSA and phosphorus use efficiency (PUE) in regards to phosphorus (P) availability between parental inbred lines and their F1. In this study, 6 maize inbred lines and their 15 F1 generated by a diallel mating system, were used to analyze the genetic associations between RSA and PUE. Heterosis for PUE-related traits were comparatively greater under high P condition and reduced significantly under low P condition. Relative mid-parent heterosis for root traits were expressed more under the low P condition. Low P supply had a significant effect on heterosis, GCA and SCA of RSA- and PUE- related traits. The hybrid C3 (7922 × 8703-2), which had the highest PUE, showed an average yield with a lower P uptake under the both P conditions. Results from this study suggested breeding for a relatively high grain yield with reducing aboveground P demand and grain P concentration should be sufficient to reduce P fertilizer input and improve P efficiency.

LBD14/ASL17 Positively Regulates Lateral Root Formation and is Involved in ABA Response for Root Architecture in Arabidopsis

The LATERAL ORGAN BOUNDARIES (LOB) DOMAIN/ASYMMETRIC LEAVES2-LIKE (LBD/ASL) gene family members play key roles in diverse aspects of plant development. Previous studies have shown that LBD16, 18, 29 and 33 are critical for integrating the plant hormone auxin to control lateral root development in Arabidopsis thaliana. In the present study, we show that LBD14 is expressed exclusively in the root where it promotes lateral root (LR) emergence. Repression of LBD14 expression by ABA correlates with the inhibitory effects of ABA on LR emergence. Transient gene expression assays with Arabidopsis protoplasts demonstrated that LBD14 is a nuclear-localized transcriptional activator. The knock-down of LBD14 expression by RNA interference (RNAi) resulted in reduced LR formation by delaying both LR primordium development and LR emergence, whereas overexpression of LBD14 in Arabidopsis enhances LR formation. We show that ABA (but not other plant hormones such as auxin, brassinosteroids and cytokinin) specifically down-regulated β-glucuronidase (GUS) expression under the control of the LBD14 promoter in transgenic Arabidopsis during LR development from initiation to emergence and endogenous LBD14 transcript levels in the root. Moreover, RNAi of LBD14 enhanced the LR suppression in response to ABA, whereas LBD14 overexpression did not alter the ABA-mediated suppression of LR formation. Taken together, these results suggest that LBD14 promoting LR formation is one of the critical factors regulated by ABA to inhibit LR growth, contributing to the regulation of the Arabidopsis root system architecture in response to ABA.

A RootNav analysis of morphological changes in Brassica napus L. roots in response to different nitrogen forms

Root architecture impacts the capacity of plants to access nutrients and water. By using the RootNav package, comprehensive morphological changes in root system architecture in response to different nitrogen concentrations and sources were investigated in Brassica napus. Ten-day-old seedlings showed a decrease in total root length, lateral root (LR) density and root exploration area with increasing external NO3 − concentrations from 0.5 to 10 mM. The application of 0.5 mM NO3 − induced more branching in the root system relative to the treatments with higher NO3 − concentrations. The allocation of biomass into the root was greater in the low NO3 − treatment relative to the high NO3 − treatments, reflecting the fact that plants invested more resources in their roots when N uptake from the environment was limited. High NH4 + concentration (10 mM) led to a stunted root system in B. napus, which showed a decrease in primary root (PR) length, total root length, LR branching zone, LR density and root exploration area. Increasing l-glutamate concentration from 0.01 to 0.1 mM suppressed PR length and total root length, whilst the LR branching zone did not change in the different l-glutamate treatments, suggesting that l-glutamate even at micromolar level could arrest PR growth and LR growth in B. napus. In conclusion, external N availability induced changes in the overall root morphology, with root elongation decreasing under an extremely N impoverished environment, but increasing under relatively mild N deficiency (for both NO3 − and NH4 +).

To respond or not to respond? Natural variation of root architectural responses to nutrient signals

The amino acid glutamate (Glu) acts as a fast excitatory neurotransmitter in mammals. Its importance in plant signalling was recognized with the discovery of channel proteins similar to mammalian Glu receptors, as well as distinct changes in root-system architecture in response to very small amounts of soil Glu. Based on natural genetic variation within Arabidopsis, Walch-Liu et al. (2017) have now identified a major locus underpinning this root response, as well as several loci controlling it through gene by environment interactions with nitrate and temperature. It is a significant step towards unraveling crosstalk between signalling pathways that enable plants to adjust their growth and development to multiple environmental stimuli.

Overexpression of the protein phosphatase 2A regulatory subunit a gene ZmPP2AA1 improves low phosphate tolerance by remodeling the root system architecture of maize.

Phosphate (Pi) limitation is a constraint for plant growth and development in many natural and agricultural ecosystems. In this study, a gene encoding Zea mays L. protein phosphatase 2A regulatory subunit A, designated ZmPP2AA1, was induced in roots by low Pi availability. The function of the ZmPP2AA1 gene in maize was analyzed using overexpression and RNA interference. ZmPP2AA1 modulated root gravitropism, negatively regulated primary root (PR) growth, and stimulated the development of lateral roots (LRs). A detailed characterization of the root system architecture (RSA) in response to different Pi concentrations with or without indole-3-acetic acid and 1-N-naphthylphthalamic acid revealed that auxin was involved in the RSA response to low Pi availability. Overexpression of ZmPP2AA1 enhanced tolerance to Pi starvation in transgenic maize in hydroponic and soil pot experiments. An increased dry weight (DW), root-to-shoot ratio, and total P content and concentration, along with a delayed and reduced accumulation of anthocyanin in overexpressing transgenic maize plants coincided with their highly branched root system and increased Pi uptake capability under low Pi conditions. Inflorescence development of the ZmPP2AA1 overexpressing line was less affected by low Pi stress, resulting in higher grain yield per plant under Pi deprivation. These data reveal the biological function of ZmPP2AA1, provide insights into a linkage between auxin and low Pi responses, and drive new strategies for the efficient utilization of Pi by maize.

Non-canonical WOX11-mediated root branching contributes to plasticity in Arabidopsis root system architecture.

Lateral roots (LRs), which originate from the growing root, and adventitious roots (ARs), which are formed from non-root organs, are the main contributors to the post-embryonic root system in Arabidopsis. However, our knowledge of how formation of the root system is altered in response to diverse inductive cues is limited. Here, we show that WOX11 contributes to root system plasticity. When seedlings are grown vertically on medium, WOX11 is not expressed in LR founder cells. During AR initiation, WOX11 is expressed in AR founder cells and activates LBD16. LBD16 also functions in LR formation and is activated in that context by ARF7/19 and not by WOX11. This indicates that divergent initial processes that lead to ARs and LRs may converge on a similar mechanism for primordium development. Furthermore, we demonstrated that when plants are grown in soil or upon wounding on medium, the primary root is able to produce both WOX11-mediated and non-WOX11-mediated roots. The discovery of WOX11-mediated root-derived roots reveals a previously uncharacterized pathway that confers plasticity during the generation of root system architecture in response to different inductive cues.

Roots Withstanding their Environment: Exploiting Root System Architecture Responses to Abiotic Stress to Improve Crop Tolerance.

To face future challenges in crop production dictated by global climate changes, breeders and plant researchers collaborate to develop productive crops that are able to withstand a wide range of biotic and abiotic stresses. However, crop selection is often focused on shoot performance alone, as observation of root properties is more complex and asks for artificial and extensive phenotyping platforms. In addition, most root research focuses on development, while a direct link to the functionality of plasticity in root development for tolerance is often lacking. In this paper we review the currently known root system architecture (RSA) responses in Arabidopsis and a number of crop species to a range of abiotic stresses, including nutrient limitation, drought, salinity, flooding, and extreme temperatures. For each of these stresses, the key molecular and cellular mechanisms underlying the RSA response are highlighted. To explore the relevance for crop selection, we especially review and discuss studies linking root architectural responses to stress tolerance. This will provide a first step toward understanding the relevance of adaptive root development for a plant’s response to its environment. We suggest that functional evidence on the role of root plasticity will support breeders in their efforts to include root properties in their current selection pipeline for abiotic stress tolerance, aimed to improve the robustness of crops.

Phosphate-dependent root system architecture responses to salt stress

Nutrient availability and salinity of the soil affect the growth and development of plant roots. Here, we describe how inorganic phosphate (Pi) availability affects the root system architecture (RSA) of Arabidopsis (Arabidopsis thaliana) and how Pi levels modulate responses of the root to salt stress. Pi starvation reduced main root length and increased the number of lateral roots of Arabidopsis Columbia-0 seedlings. In combination with salt, low Pi dampened the inhibiting effect of mild salt stress (75 mm) on all measured RSA components. At higher salt concentrations, the Pi deprivation response prevailed over the salt stress only for lateral root elongation. The Pi deprivation response of lateral roots appeared to be oppositely affected by abscisic acid signaling compared with the salt stress response. Natural variation in the response to the combination treatment of salt and Pi starvation within 330 Arabidopsis accessions could be grouped into four response patterns. When exposed to double stress, in general, lateral roots prioritized responses to salt, while the effect on main root traits was additive. Interestingly, these patterns were not identical for all accessions studied, and multiple strategies to integrate the signals from Pi deprivation and salinity were identified. By genome-wide association mapping, 12 genomic loci were identified as putative factors integrating responses to salt stress and Pi starvation. From our experiments, we conclude that Pi starvation interferes with salt responses mainly at the level of lateral roots and that large natural variation exists in the available genetic repertoire of accessions to handle the combination of stresses.

X-Ray Computed Tomography Reveals the Response of Root System Architecture to Soil Texture.

Root system architecture (RSA) impacts plant fitness and crop yield by facilitating efficient nutrient and water uptake from the soil. A better understanding of the effects of soil on RSA could improve crop productivity by matching roots to their soil environment. We used x-ray computed tomography to perform a detailed three-dimensional quantification of changes in rice (Oryza sativa) RSA in response to the physical properties of a granular substrate. We characterized the RSA of eight rice cultivars in five different growth substrates and determined that RSA is the result of interactions between genotype and growth environment. We identified cultivar-specific changes in RSA in response to changing growth substrate texture. The cultivar Azucena exhibited low RSA plasticity in all growth substrates, whereas cultivar Bala root depth was a function of soil hardness. Our imaging techniques provide a framework to study RSA in different growth environments, the results of which can be used to improve root traits with agronomic potential.

A Small GTPase, OsRab6a, is Involved in the Regulation of Iron Homeostasis in Rice.

Plants have evolved two distinct strategies to acquire iron (Fe) from soils. However, the regulatory mechanisms underlying the Fe acquisition remain largely elusive. There is emerging evidence that small GTPases are involved in the responses of plants to environmental cues. Here, we identified a gene encoding a small GTPase, OsRab6a, in rice and characterized its role in Fe acquisition by generating transgenic rice plants with overexpression and knockdown of OsRab6a OsRab6a shared conserved functional domains with other known members of the Rab subfamily and localized ubiquitously in the cytoplasm and nucleus. The expression of OsRab6a was rapidly and transiently up-regulated by Fe deficiency. No differences in growth and development among the OsRab6a-overexpression, OsRab6a-RNAi (RNA interference) and wild-type plants were detected when grown in Fe-sufficient medium. However, overexpression of OsRab6a in rice plants conferred greater tolerance to Fe deficiency than RNAi and wild-type plants, as evidenced by higher seedling height, and greater biomass, Chl contents and Fe concentrations in shoots, roots and grains in the overexpression lines than wild-type and RNAi plants. Moreover, the overexpression lines exhibited larger root systems than wild-type and RNAi plants in Fe-deficient medium. Exposure to Fe-deficient medium led to up-regulation of OsIRO2, OsIRT1, OsNAS1 and OsNAS2 in both wild-type and transgenic rice plants, with the magnitude of up-regulation positively correlated with the expression levels of OsRab6a These results may suggest that OsRab6a plays an important role in the regulation of Fe acquisition in rice plants by modulating physiological processes involved in Fe acquisition and root system architecture in response to Fe-deficient medium.

Strigolactone versus gibberellin signaling: reemerging concepts?

Main conclusionIn this review, we compare knowledge about the recently discovered strigolactone signaling pathway and the well established gibberellin signaling pathway to identify gaps of knowledge and putative research directions in strigolactone biology. Communication between and inside cells is integral for the vitality of living organisms. Hormonal signaling cascades form a large part of this communication and an understanding of both their complexity and interactive nature is only beginning to emerge. In plants, the strigolactone (SL) signaling pathway is the most recent addition to the classically acting group of hormones and, although fundamental insights have been made, knowledge about the nature and impact of SL signaling is still cursory. This narrow understanding is in spite of the fact that SLs influence a specific spectrum of processes, which includes shoot branching and root system architecture in response, partly, to environmental stimuli. This makes these hormones ideal tools for understanding the coordination of plant growth processes, mechanisms of long-distance communication and developmental plasticity. Here, we summarize current knowledge about SL signaling and employ the well-characterized gibberellin (GA) signaling pathway as a scaffold to highlight emerging features as well as gaps in our knowledge in this context. GA signaling is particularly suitable for this comparison because both signaling cascades share key features of hormone perception and of immediate downstream events. Therefore, our comparative view demonstrates the possible level of complexity and regulatory interfaces of SL signaling.

Statistical modeling of nitrogen‐dependent modulation of root system architecture in Arabidopsis thaliana

Plant root development is strongly affected by nutrient availability. Despite the importance of structure and function of roots in nutrient acquisition, statistical modeling approaches to evaluate dynamic and temporal modulations of root system architecture in response to nutrient availability have remained as widely open and exploratory areas in root biology. In this study, we developed a statistical modeling approach to investigate modulations of root system architecture in response to nitrogen availability. Mathematical models were designed for quantitative assessment of root growth and root branching phenotypes and their dynamic relationships based on hierarchical configuration of primary and lateral roots formulating the fishbone-shaped root system architecture in Arabidopsis thaliana. Time-series datasets reporting dynamic changes in root developmental traits on different nitrate or ammonium concentrations were generated for statistical analyses. Regression analyses unraveled key parameters associated with: (i) inhibition of primary root growth under nitrogen limitation or on ammonium; (ii) rapid progression of lateral root emergence in response to ammonium; and (iii) inhibition of lateral root elongation in the presence of excess nitrate or ammonium. This study provides a statistical framework for interpreting dynamic modulation of root system architecture, supported by meta-analysis of datasets displaying morphological responses of roots to diverse nitrogen supplies.

Natural genetic variation of Arabidopsis thaliana root morphological response to magnesium supply

Plants dynamically cope with the variability of mineral nutrient distribution in soil by constantly modulating nutrient uptake and shaping root-system architecture. The changes in root morphology in response to major essential elements are largely documented, but little is known about how the root system responds to magnesium (Mg) availability. Thirty-six natural accessions of the model species Arabidopsis thaliana were subjected to an in vitro screen for identifying variation in root system architecture in response to Mg availability. Response of root morphology was observed on 2-dimensional agar plates. Low Mg supply repressed the elongation of the lateral roots more than of the primary root. However, some accessions exhibited higher number and length of lateral roots than the reference Columbia-0. Across all accessions, the root morphological traits did not correlate with tissue Mg concentrations. Interestingly, shoot calcium and root phosphorus concentrations were positively correlated with the number and length of lateral roots, whereas root iron concentration was negatively correlated with the primary root length. The diversity of root phenotypes identified in this report is a useful resource to study the genetic component determining root morphology in response to Mg availability.

Strategies for optimization of mineral nutrient transport in plants: multilevel regulation of nutrient-dependent dynamics of root architecture and transporter activity.

How do sessile plants cope with irregularities in soil nutrient availability? The uptake of essential minerals from the soil influences plant growth and development. However, most environments do not provide sufficient nutrients; rather nutrient distribution in the soil can be uneven and change temporally according to environmental factors. To maintain mineral nutrient homeostasis in their tissues, plants have evolved sophisticated systems for coping with spatial and temporal variability in soil nutrient concentrations. Among these are mechanisms for modulating root system architecture in response to nutrient availability. This review discusses recent advances in knowledge of the two important strategies for optimizing nutrient uptake and translocation in plants: root architecture modification and transporter expression control in response to nutrient availability. Recent studies have determined (i) nutrient-specific root patterns; (ii) their physiological consequences; and (iii) the molecular mechanisms underlying these modulation systems that operate to facilitate efficient nutrient acquisition. Another mechanism employed by plants in nutrient-heterogeneous soils involves modification of nutrient transport activities in a nutrient concentration-dependent manner. In recent years, considerable progress has been made in characterizing the diverse functions of transporters for specific nutrients; it is now clear that the expression and activities of nutrient transporters are finely regulated in multiple steps at both the transcriptional and post-transcriptional levels for adaptation to a wide range of nutrient conditions.

Using X-ray Computed Tomography to explore the role of abscisic acid in moderating the impact of soil compaction on root system architecture

Background and AimsUnderstanding how soil compaction affects root system architecture (RSA) and root deployment within soil is critical to maximise crop growth. This study examined the role of abscisic acid (ABA) in mediating root responses to soil compaction using tomato genotypes with differing endogenous ABA concentrations. MethodsPlants of the wild-type tomato genotype (Solanum lycopersicum L. cv. Ailsa Craig) and its ABA-deficient mutant notabilis, of uniform developmental stage, were transplanted to columns containing a loamy sand soil at bulk densities of 1.2, 1.4 and 1.6Mgm−3. Fourteen days after transplanting (DAT), an X-ray μCT scanner acquired non-destructive 3-D images of RSA. Destructive analysis of RSA was undertaken using WinRHIZO® 2-D scanning equipment. Key resultsIncreased bulk density decreased root volume, surface area, rooting depth and lateral root number (P<0.05), which adversely affected RSA and the subsequent volume of soil explored. The ABA-deficient mutant notabilis displayed a poor rooting phenotype with reduced root volume, surface area and lateral roots at all bulk densities. ConclusionsThe response of RSA to soil compaction in situ differed between the ABA-deficient mutant genotypes of tomato. The differences in rooting phenotype between genotypes suggest that endogenous ABA concentration has a positive influence on RSA when roots encounter compacted soil.

Cytokinin as a mediator for regulating root system architecture in response to environmental cues

Root system architecture (RSA) is developmentally controlled by genetic pathways and their interaction with various environmental cues, in particular soil conditions. One important player in shaping RSA is the hormone cytokinin, which acts as a negative regulator of root elongation and branching. The redundant roles of cytokinin metabolism and signaling genes of Arabidopsis thaliana in regulating early stages of lateral root formation has recently been shown and it has been proposed that this redundancy reflects a role in mediating different environmental cues. Here we report that the transcript levels of cytokinin genes in the root responds to changes in nutrient availability in distinct ways. IPT3, IPT5, CYP735A2, LOG5, and CKX4 are particularly responsive cytokinin metabolism genes, genes encoding different type-A response regulators and the transcriptions factor genes ARR10 and CRF6 are among the most responsive signaling genes. This finding supports the hypothesis that environmental cues operate through fine-tuned transcriptional regulation of cytokinin genes to modulate root development.