SUMMARY
Plants forage soil for water and nutrients, whose distribution is patchy and often dynamic. To improve their foraging activities, plants have evolved mechanisms to modify the physicochemical ...properties and microbial communities of the rhizosphere, i.e. the soil compartment under the influence of the roots. This dynamic interplay in root−soil−microbiome interactions creates emerging properties that impact plant nutrition and health. As a consequence, the rhizosphere can be considered an extended root phenotype, a manifestation of the effects of plant genes on their environment inside and/or outside of the organism. Here, we review current understanding of how plants shape the rhizosphere and the benefits it confers to plant fitness. We discuss future research challenges and how applying their solutions in crops will enable us to harvest the benefits of the extended root phenotype.
Significance Statement
Plants have evolved mechanisms to modify the physicochemical properties and microbial communities of the rhizosphere. Here, we review our current knowledge on how plants create this extended phenotype through root−soil−microbiome interactions and the benefits it confers to plant fitness.
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•A ‘second green revolution’ using crops with improved below-ground traits is needed.•Phenotyping plant roots poses practical and data challenges.•Technologies for 2D root phenotyping ...include rhizotrons, paper pouches, and plates.•MRI, PET and X-ray CT allow 3D and 4D root phenotyping in soil.•Non-invasive techniques for field phenotyping have recently advanced.•Deep machine learning techniques are transforming the root phenotyping landscape.
Major increases in crop yield are required to keep pace with population growth and climate change. Improvements to the architecture of crop roots promise to deliver increases in water and nutrient use efficiency but profiling the root phenome (i.e. its structure and function) represents a major bottleneck. We describe how advances in imaging and sensor technologies are making root phenomic studies possible. However, methodological advances in acquisition, handling and processing of the resulting ‘big-data’ is becoming increasingly important. Advances in automated image analysis approaches such as Deep Learning promise to transform the root phenotyping landscape. Collectively, these innovations are helping drive the selection of the next-generation of crops to deliver real world impact for ongoing global food security efforts.
Soil compaction represents a major challenge for modern agriculture. Compaction is intuitively thought to reduce root growth by limiting the ability of roots to penetrate harder soils. We report that ...root growth in compacted soil is instead actively suppressed by the volatile hormone ethylene. We found that mutant
and rice roots that were insensitive to ethylene penetrated compacted soil more effectively than did wild-type roots. Our results indicate that soil compaction lowers gas diffusion through a reduction in air-filled pores, thereby causing ethylene to accumulate in root tissues and trigger hormone responses that restrict growth. We propose that ethylene acts as an early warning signal for roots to avoid compacted soils, which would be relevant to research into the breeding of crops resilient to soil compaction.
The holistic rhizosphere York, Larry M.; Carminati, Andrea; Mooney, Sacha J. ...
Journal of experimental botany,
06/2016, Letnik:
67, Številka:
12
Journal Article
Recenzirano
Odprti dostop
Despite often being conceptualized as a thin layer of soil around roots, the rhizosphere is actually a dynamic system of interacting processes. Hiltner originally defined the rhizosphere as the soil ...influenced by plant roots. However, soil physicists, chemists, microbiologists, and plant physiologists have studied the rhizosphere independently, and therefore conceptualized the rhizosphere in different ways and using contrasting terminology. Rather than research-specific conceptions of the rhizosphere, the authors propose a holistic rhizosphere encapsulating the following components: microbial community gradients, macroorganisms, mucigel, volumes of soil structure modification, and depletion or accumulation zones of nutrients, water, root exudates, volatiles, and gases. These rhizosphere components are the result of dynamic processes and understanding the integration of these processes will be necessary for future contributions to rhizosphere science based upon interdisciplinary collaborations. In this review, current knowledge of the rhizosphere is synthesized using this holistic perspective with a focus on integrating traditionally separated rhizosphere studies. The temporal dynamics of rhizosphere activities will also be considered, from annual fine root turnover to diurnal fluctuations of water and nutrient uptake. The latest empirical and computational methods are discussed in the context of rhizosphere integration. Clarification of rhizosphere semantics, a holistic model of the rhizosphere, examples of integration of rhizosphere studies across disciplines, and review of the latest rhizosphere methods will empower rhizosphere scientists from different disciplines to engage in the interdisciplinary collaborations needed to break new ground in truly understanding the rhizosphere and to apply this knowledge for practical guidance.
Lateral root (LR) emergence represents a highly coordinated process in which the plant hormone auxin plays a central role. Reactive oxygen species (ROS) have been proposed to function as important ...signals during auxin-regulated LR formation; however, their mode of action is poorly understood. Here, we report that Arabidopsis roots exposed to ROS show increased LR numbers due to the activation of LR pre-branch sites and LR primordia (LRP). Strikingly, ROS treatment can also restore LR formation in pCASP1:shy2-2 and aux1 lax3 mutant lines in which auxin-mediated cell wall accommodation and remodeling in cells overlying the sites of LR formation is disrupted. Specifically, ROS are deposited in the apoplast of these cells during LR emergence, following a spatiotemporal pattern that overlaps the combined expression domains of extracellular ROS donors of the RESPIRATORY BURST OXIDASE HOMOLOGS (RBOH). We also show that disrupting (or enhancing) expression of RBOH in LRP and/or overlying root tissues decelerates (or accelerates) the development and emergence of LRs. We conclude that RBOH-mediated ROS production facilitates LR outgrowth by promoting cell wall remodeling of overlying parental tissues.
Lateral roots (LRs) are crucial for increasing the surface area of root systems to explore heterogeneous soil environments. Major advances have recently been made in the model plant arabidopsis ...(Arabidopsis thaliana) to elucidate the cellular basis of LR development and the underlying gene regulatory networks (GRNs) that control the morphogenesis of the new root organ. This has provided a foundation for understanding the sophisticated adaptive mechanisms that regulate how plants pattern their root branching to match the spatial availability of resources such as water and nutrients in their external environment. We review new insights into the molecular, cellular, and environmental regulation of LR development in arabidopsis.
Major advances have recently been made in arabidopsis to elucidate the cellular basis of LR development and the underlying GRNs.New 4D imaging approaches are revolutionizing the perspective of the field on LR morphogenesis.Recent studies reveal that biomechanical interactions between the new primordia and overlying tissues impact on organ initiation and morphogenesis. We propose a new mechanism, termed the developmental traffic light model, to explain how mechanical signals influence the patterning of the LR primordium.LR research has progressed beyond studying individual genes to characterizing GRNs by exploiting innovative systems and omics-based approaches.Arabidopsis roots employ regulatory mechanisms to sense the availability of water and nutrients so as to adapt their pattern of branching to optimize resource capture.
Abstract
Wheat (Triticum aestivum L.) root growth in the subsoil is usually constrained by soil strength, although roots can use macropores to elongate to deeper layers. The quantitative relationship ...between the elongation of wheat roots and the soil pore system, however, is still to be determined. We studied the depth distribution of roots of six wheat varieties and explored their relationship with soil macroporosity from samples with the field structure preserved. Undisturbed soil cores (to a depth of 100 cm) were collected from the field and then non-destructively imaged using X-ray computed tomography (at a spatial resolution of 90 µm) to quantify soil macropore structure and root number density (the number of roots cm–2 within a horizontal cross-section of a soil core). Soil macroporosity changed significantly with depth but not between the different wheat lines. There was no significant difference in root number density between wheat varieties. In the subsoil, wheat roots used macropores, especially biopores (i.e. former root or earthworm channels) to grow into deeper layers. Soil macroporosity explained 59% of the variance in root number density. Our data suggested that the development of the wheat root system in the field was more affected by the soil macropore system than by genotype. On this basis, management practices which enhance the porosity of the subsoil may therefore be an effective strategy to improve deep rooting of wheat.
The development of the wheat root system in the field was more affected by soil macropore arrangement than by genotype.
Plants adapt to heterogeneous soil conditions by altering their root architecture. For example, roots branch when in contact with water by using the hydropatterning response. We report that ...hydropatterning is dependent on auxin response factor ARF7. This transcription factor induces asymmetric expression of its target gene
in lateral root founder cells. This differential expression pattern is regulated by posttranslational modification of ARF7 with the small ubiquitin-like modifier (SUMO) protein. SUMOylation negatively regulates ARF7 DNA binding activity. ARF7 SUMOylation is required to recruit the Aux/IAA (indole-3-acetic acid) repressor protein IAA3. Blocking ARF7 SUMOylation disrupts IAA3 recruitment and hydropatterning. We conclude that SUMO-dependent regulation of auxin response controls root branching pattern in response to water availability.
Root traits such as root angle and hair length influence resource acquisition particularly for immobile nutrients like phosphorus (P). Here, we attempted to modify root angle in rice by disrupting ...the OsAUX1 auxin influx transporter gene in an effort to improve rice P acquisition efficiency. We show by X-ray microCT imaging that root angle is altered in the osaux1 mutant, causing preferential foraging in the top soil where P normally accumulates, yet surprisingly, P acquisition efficiency does not improve. Through closer investigation, we reveal that OsAUX1 also promotes root hair elongation in response to P limitation. Reporter studies reveal that auxin response increases in the root hair zone in low P environments. We demonstrate that OsAUX1 functions to mobilize auxin from the root apex to the differentiation zone where this signal promotes hair elongation when roots encounter low external P. We conclude that auxin and OsAUX1 play key roles in promoting root foraging for P in rice.
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