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WIREs Dev Biol
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Nutritional regulation of root development

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Mineral nutrients such as nitrogen (N), phosphorus (P), and iron (Fe) are essential for plant growth, development, and reproduction. Adequate provision of nutrients via the root system impacts greatly on shoot biomass and plant productivity and is therefore of crucial importance for agriculture. Nutrients are taken up at the root surface in ionic form, which is mediated by specific transport proteins. Noteworthy, root tips are able to sense the local and internal concentrations of nutrients to adjust growth and developmental processes, and ultimately, to increase or decrease the exploratory capacity of the root system. Recently, important progress has been achieved in identifying the mechanisms of nutrient sensing in wild‐ and cultivated species, including Arabidopsis, bean, maize, rice, lupin as well as in members of the Proteaceae and Cyperaceae families, which develop highly sophisticated root clusters as adaptations to survive in soils with very low fertility. Major findings include identification of transporter proteins and transcription factors regulating nutrient sensing, miRNAs as mobile signals and peptides as repressors of lateral root development under heterogeneous nutrient supply. Understanding the roles played by N, P, and Fe in gene expression and biochemical characterization of proteins involved in root developmental responses to homogeneous or heterogeneous N and P sources has gained additional interest due to its potential for improving fertilizer acquisition efficiency in crops. WIREs Dev Biol 2015, 4:431–443. doi: 10.1002/wdev.183 This article is categorized under: Plant Development > Root Development Plant Development > Vegetative Development Plant Development > Cell Growth and Differentiation
Regulatory elements involved in LR growth in response to homogeneous or heterogeneous N sources. Homogenous supply of triggers lateral root initiation, while ‐rich patches stimulates lateral root elongation. (a) In Arabidopsis, NRT1.1 is a dual‐affinity transporter involved in both high‐ and low‐affinity uptake. The switch between the two affinities is controlled by phosphorylation at the T101, and this phosphorylation is regulated by the calcineurin B‐like‐interacting protein kinase CIPK23. NRT1.1 promotes LR growth in ‐rich patches likely through the transcription factor ANR1. levels affect root development through modulation of auxin synthesis and signaling via TAR2, AFB3 and ARF8. Solid arrows indicate positive effects, blunt solid arrows indicate negative effects, and dashed lines indicate possible interactions. (b) Root foraging for involves both local and systemic signaling. Roots respond to low local levels of by producing CEP1 and CLE3 peptides, which are repressors of lateral root growth. CEP1 moves upward to the shoot and is received by the LRR‐RKs proteins CEPR1 and CEPR2. Long‐distance signaling to the root halve grown under high involves cytokinin (CK) biosynthesis and requires the transcription factor TCP20, which activates the expression of genes involved in N uptake and is necessary for the induction of development.
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Influence of phosphate supply on dauciform‐root formation in the south‐western Australian native Cyperaceae Carex fascicularis. The formation of highly specialised dauciform roots increases dramatically on plants as the Pi level is decreased in nutrient solution (from left to right). This particular species of Carex develops relatively small dauciform roots in series (arrows) along the axes of growing LR (cf. Figure (c) and (e)). Scale bar; 13 mm.
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Root‐cluster morphologies in Proteaceae, Cyperaceae, and Fabaceae. All species are well adapted to soils of extremely low P concentrations. Plants were grown in nutrient solutions containing ≤1 µM phosphate. (a) Proteoid roots (compound type) of Banksia prionotes (Proteaceae). (b) Cluster roots (simple type) of Lupinus albus L. (Fabaceae). (c) Dauciform roots of Schoenus unispiculatus (Cyperaceae). (d) Proteoid roots of Hakea prostrata (simple type, Proteaceae). (e) Stages of dauciform root development in S. unispiculatus. Dauciform roots were initially white, but often turned bright yellow as they matured. Remarkably large numbers of long root hairs with a similar final length were fully developed after ca. 7–9 days. The axes of very young dauciform roots (1–3 days old) illustrate the ‘carrot shape’ of the dauciform root axes, and a slender stalk connected the carrot‐shaped axis to the main root. After 10–12 days, the dauciform roots senesced. (f) Stages of proteoid‐root development in H. prostrata from rootlet initiation to senescence (∼20 days old, far right). Scale bars in mm (a) 10; (b) 4; (c) 3; (d) 11; (e) 5; and (f) 9.
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Iron signaling regulates root architecture. Fe is taken up into the symplast by IRT1 transporters at the root surface. Reduction of Fe by FRO2, and FRO5 reductases, contribute to increased Fe acquisition. Fe can diffuse through the symplastic space to the pericycle and then to the vasculature. BTS and PYE, a putative E3 ligase and a bHLH transcription factor, respectively, are specifically induced in root pericycle cells under Fe deficiency. PYE and other bHLHs transcription factors likely regulate the genes responsive to activate pericycle cells for LR initiation under Fe deprivation. Fe translocation inside the plant is associated with suitable chelating molecules such as organic acids and loading from vasculature to mesophyll tissue occurs via YSL transporters.
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Phosphorus starvation signaling pathways regulate primary and LR development. Pi is sensed in root tips by an unknown P starvation sensor, which triggers the signaling pathways that modulate root architecture. Low Pi promotes LR proliferation through increasing auxin transport and BIG function, and auxin signaling that involves TIR1, IAA14, ARF7, and ARF19. SLR1/IAA14 is a member of Aux/IAA family that represses the activity of ARF7 and ARF19 in lateral root initiation. The effects of low Pi stress on cell division and differentiation is regulated through the transcription factor SCR and LPR and PDR proteins. Other transcription factors such as WRKY75 regulate LR proliferation and anthocyanin accumulation.
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Arabidopsis root architectural responses to low Pi stress. Representative root architectures of seedlings grown for 12 days on medium supplied with (a) 1000 µM (high Pi) or (b) 1 µM (low Pi). Note the highly branched root systems in low Pi conditions due to proliferation of LR. Expression of Pi transporter AtPT2 in primary root tips of seedlings grown under high Pi (c) or low Pi (d) supply coincides with high root‐hair proliferation capacity. (e) Phenotypes of Arabidopsis WT (Col‐0) and low phosphorus insensitive 1 mutant seedlings grown under low P stress. Note the long primary roots developed by the mutants indicative of altered perception of low Pi availability.
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