Modulation of plant immunity and biotic interactions under phosphate deficiency.

Phosphorus (P) is an essential macronutrient for plant life and growth. P is primarily acquired in the form of inorganic phosphate (Pi) from soil. To cope with Pi deficiency, plants have evolved an elaborate system to improve Pi acquisition and utilization through an array of developmental and physiological changes, termed Pi starvation response (PSR). Plants also assemble and manage mutualistic microbes to enhance Pi uptake, through integrating PSR and immunity signaling. A trade-off between plant growth and defense favors the notion that plants lower a cellular state of immunity to accommodate host-beneficial microbes for nutrition and growth at the cost of infection risk. However, the existing data indicate that plants selectively activate defense responses against pathogens, but do not or less against non-pathogens, even under nutrient deficiency. In this review, we highlight recent advances in the principles and mechanisms with which plants balance immunity and growth-related processes to optimize their adaptation to Pi deficiency.

Silicon regulates phosphate deficiency through involvement of auxin and nitric oxide in barley roots.

MAIN CONCLUSION: Silicon application mitigates phosphate deficiency in barley through an interplay with auxin and nitric oxide, enhancing growth, photosynthesis, and redox balance, highlighting the potential of silicon as a fertilizer for overcoming nutritional stresses. Silicon (Si) is reported to attenuate nutritional stresses in plants, but studies on the effect of Si application to plants grown under phosphate (Pi) deficiency are still very scarce, especially in barley. Therefore, the present work was undertaken to investigate the potential role of Si in mitigating the adverse impacts of Pi deficiency in barley Hordeum vulgare L. (var. BH902). Further, the involvement of two key regulatory signaling molecules--auxin and nitric oxide (NO)--in Si-induced tolerance against Pi deficiency in barley was tested. Morphological attributes, photosynthetic parameters, oxidative stress markers (O2·-, H2O2, and MDA), antioxidant system (enzymatic--APX, CAT, SOD, GR, DHAR, MDHAR as well as non-enzymatic--AsA and GSH), NO content, and proline metabolism were the key traits that were assessed under different treatments. The P deficiency distinctly declined growth of barley seedlings, which was due to enhancement in oxidative stress leading to inhibition of photosynthesis. These results were also in parallel with an enhancement in antioxidant activity, particularly SOD and CAT, and endogenous proline level and its biosynthetic enzyme (P5CS). The addition of Si exhibited beneficial effects on barley plants grown in Pi-deficient medium as reflected in increased growth, photosynthetic activity, and redox balance through the regulation of antioxidant machinery particularly ascorbate-glutathione cycle. We noticed that auxin and NO were also found to be independently participating in Si-mediated improvement of growth and other parameters in barley roots under Pi deficiency. Data of gene expression analysis for PHOSPHATE TRANSPORTER1 (HvPHT1) indicate that Si helps in increasing Pi uptake as per the need of Pi-deficient barley seedlings, and also auxin and NO both appear to help Si in accomplishing this task probably by inducing lateral root formation. These results are suggestive of possible application of Si as a fertilizer to correct the negative effects of nutritional stresses in plants. Further research at genetic level to understand Si-induced mechanisms for mitigating Pi deficiency can be helpful in the development of new varieties with improved tolerance against Pi deficiency, especially for cultivation in areas with Pi-deficient soils.

Factors governing the transcriptome changes and chronological lifespan of fission yeast during phosphate starvation.

Starvation of Schizosaccharomyces pombe for inorganic phosphate elicits adaptive transcriptome changes in which mRNAs driving ribosome biogenesis, tRNA biogenesis, and translation are globally downregulated, while those for autophagy and phosphate mobilization are upregulated. Here, we interrogated three components of the starvation response: upregulated autophagy; the role of transcription factor Pho7 (an activator of the PHO regulon); and upregulated expression of ecl3, one of three paralogous genes (ecl1, ecl2, and ecl3) collectively implicated in cell survival during other nutrient stresses. Ablation of autophagy factor Atg1 resulted in early demise of phosphate-starved fission yeast, as did ablation of Pho7. Transcriptome profiling of phosphate-starved pho7Δ cells highlighted Pho7 as an activator of genes involved in phosphate acquisition and mobilization, not limited to the original three-gene PHO regulon, and additional starvation-induced genes (including ecl3) not connected to phosphate dynamics. Pho7-dependent gene induction during phosphate starvation tracked with the presence of Pho7 DNA-binding elements in the gene promoter regions. Fewer ribosome protein genes were downregulated in phosphate-starved pho7Δ cells versus WT, which might contribute to their shortened lifespan. An ecl3Δ mutant elicited no gene expression changes in phosphate-replete cells and had no impact on survival during phosphate starvation. By contrast, pan-ecl deletion (ecl123Δ) curtailed lifespan during chronic phosphate starvation. Phosphate-starved ecl123Δ cells experienced a more widespread downregulation of mRNAs encoding aminoacyl tRNA synthetases vis-à-vis WT or pho7Δ cells. Collectively, these results enhance our understanding of fission yeast phosphate homeostasis and survival during nutrient deprivation.

Unraveling the potential of the strigolactones-NSP1/NSP2 friendship in crop improvement.

Strigolactones (SLs) are fundamental to the ability of plants to cope with phosphate deficiency. A recent study by Yuan et al. indicates that the genetic module PHR2/NSP1/NSP2 is crucial in activating SL biosynthesis and signaling under inorganic phosphate (Pi) deficiency. Furthermore, this genetic module is essential for improving Pi and nitrogen homeostasis in rice.

A phosphate-sensing organelle regulates phosphate and tissue homeostasis.

Inorganic phosphate (Pi) is one of the essential molecules for life. However, little is known about intracellular Pi metabolism and signalling in animal tissues1. Following the observation that chronic Pi starvation causes hyperproliferation in the digestive epithelium of Drosophila melanogaster, we determined that Pi starvation triggers the downregulation of the Pi transporter PXo. In line with Pi starvation, PXo deficiency caused midgut hyperproliferation. Interestingly, immunostaining and ultrastructural analyses showed that PXo specifically marks non-canonical multilamellar organelles (PXo bodies). Further, by Pi imaging with a Förster resonance energy transfer (FRET)-based Pi sensor2, we found that PXo restricts cytosolic Pi levels. PXo bodies require PXo for biogenesis and undergo degradation following Pi starvation. Proteomic and lipidomic characterization of PXo bodies unveiled their distinct feature as an intracellular Pi reserve. Therefore, Pi starvation triggers PXo downregulation and PXo body degradation as a compensatory mechanism to increase cytosolic Pi. Finally, we identified connector of kinase to AP-1 (Cka), a component of the STRIPAK complex and JNK signalling3, as the mediator of PXo knockdown- or Pi starvation-induced hyperproliferation. Altogether, our study uncovers PXo bodies as a critical regulator of cytosolic Pi levels and identifies a Pi-dependent PXo-Cka-JNK signalling cascade controlling tissue homeostasis.

Research Advances in the Mutual Mechanisms Regulating Response of Plant Roots to Phosphate Deficiency and Aluminum Toxicity.

Low phosphate (Pi) availability and high aluminum (Al) toxicity constitute two major plant mineral nutritional stressors that limit plant productivity on acidic soils. Advances toward the identification of genes and signaling networks that are involved in both stresses in model plants such as Arabidopsis thaliana and rice (Oryza sativa), and in other plants as well have revealed that some factors such as organic acids (OAs), cell wall properties, phytohormones, and iron (Fe) homeostasis are interconnected with each other. Moreover, OAs are involved in recruiting of many plant-growth-promoting bacteria that are able to secrete both OAs and phosphatases to increase Pi availability and decrease Al toxicity. In this review paper, we summarize these mutual mechanisms by which plants deal with both Al toxicity and P starvation, with emphasis on OA secretion regulation, plant-growth-promoting bacteria, transcription factors, transporters, hormones, and cell wall-related kinases in the context of root development and root system architecture remodeling that plays a determinant role in improving P use efficiency and Al resistance on acidic soils.

PHOSPHATE STARVATION RESPONSE transcription factors enable arbuscular mycorrhiza symbiosis.

Arbuscular mycorrhiza (AM) is a widespread symbiosis between roots of the majority of land plants and Glomeromycotina fungi. AM is important for ecosystem health and functioning as the fungi critically support plant performance by providing essential mineral nutrients, particularly the poorly accessible phosphate, in exchange for organic carbon. AM fungi colonize the inside of roots and this is promoted at low but inhibited at high plant phosphate status, while the mechanistic basis for this phosphate-dependence remained obscure. Here we demonstrate that a major transcriptional regulator of phosphate starvation responses in rice PHOSPHATE STARVATION RESPONSE 2 (PHR2) regulates AM. Root colonization of phr2 mutants is drastically reduced, and PHR2 is required for root colonization, mycorrhizal phosphate uptake, and yield increase in field soil. PHR2 promotes AM by targeting genes required for pre-contact signaling, root colonization, and AM function. Thus, this important symbiosis is directly wired to the PHR2-controlled plant phosphate starvation response.

Transcriptome analysis provides new insights into plants responses under phosphate starvation in association with chilling stress.

BACKGROUND: Chilling temperature reduces the rate of photosynthesis in plants, which is more pronounced in association with phosphate (Pi) starvation. Previous studies showed that Pi resupply improves recovery of the rate of photosynthesis in plants much better under combination of dual stresses than in non-chilled samples. However, the underlying mechanism remains poorly understood. RESULTS: In this study, RNA-seq analysis showed the expression level of 41 photosynthetic genes in plant roots increased under phosphate starvation associated with 4 °C (-P 4 °C) compared to -P 23 °C. Moreover, iron uptake increased significantly in the stem cell niche (SCN) of wild type (WT) roots in -P 4 °C. In contrast, lower iron concentrations were found in SCN of aluminum activated malate transporter 1 (almt1) and its transcription factor, sensitive to protein rhizotoxicity 1 (stop1) mutants under -P 4 °C. The Fe content examined by ICP-MS analysis in -P 4 °C treated almt1 was 98.5 ng/µg, which was only 17% of that of seedlings grown under -P 23 °C. Average plastid number in almt1 root cells under -P 4 °C was less than -P 23 °C. Furthermore, stop1 and almt1 single mutants both exhibited increased primary root elongation than WT under combined stresses. In addition, dark treatment blocked the root elongation phenotype of stop1 and almt1. CONCLUSIONS: Induction of photosynthetic gene expression and increased iron accumulation in roots is required for plant adjustment to chilling in association with phosphate starvation.

Early sensing of phosphate deprivation triggers the formation of extra root cap cell layers via SOMBRERO through a process antagonized by auxin signaling.

KEY MESSAGE: The role of the root cap in the plant response to phosphate deprivation has been scarcely investigated. Here we describe early structural, physiological and molecular changes prior to the determinate growth program of the primary roots under low Pi and unveil a critical function of the transcription factor SOMBRERO in low Pi sensing. Mineral nutrient distribution in the soil is uneven and roots efficiently adapt to improve uptake and assimilation of sparingly available resources. Phosphate (Pi) accumulates in the upper layers and thus short and branched root systems proliferate to better exploit organic and inorganic Pi patches. Here we report an early adaptive response of the Arabidopsis primary root that precedes the entrance of the meristem into the determinate developmental program that is a hallmark of the low Pi sensing mechanism. In wild-type seedlings transferred to low Pi medium, the quiescent center domain in primary root tips increases as an early response, as revealed by WOX5:GFP expression and this correlates with a thicker root tip with extra root cap cell layers. The halted primary root growth in WT seedlings could be reversed upon transfer to medium supplemented with 250 µM Pi. Mutant and gene expression analysis indicates that auxin signaling negatively affects the cellular re-specification at the root tip and enabled identification of the transcription factor SOMBRERO as a critical element that orchestrates both the formation of extra root cap layers and primary root growth under Pi scarcity. Moreover, we provide evidence that low Pi-induced root thickening or the loss-of-function of SOMBRERO is associated with expression of phosphate transporters at the root tip. Our data uncover a developmental window where the root tip senses deprivation of a critical macronutrient to improve adaptation and surveillance.

Phosphate Restriction Promotes Longevity via Activation of Autophagy and the Multivesicular Body Pathway.

Nutrient limitation results in an activation of autophagy in organisms ranging from yeast, nematodes and flies to mammals. Several evolutionary conserved nutrient-sensing kinases are critical for efficient adaptation of yeast cells to glucose, nitrogen or phosphate depletion, subsequent cell-cycle exit and the regulation of autophagy. Here, we demonstrate that phosphate restriction results in a prominent extension of yeast lifespan that requires the coordinated activity of autophagy and the multivesicular body pathway, enabling efficient turnover of cytoplasmic and plasma membrane cargo. While the multivesicular body pathway was essential during the early days of aging, autophagy contributed to long-term survival at later days. The cyclin-dependent kinase Pho85 was critical for phosphate restriction-induced autophagy and full lifespan extension. In contrast, when cell-cycle exit was triggered by exhaustion of glucose instead of phosphate, Pho85 and its cyclin, Pho80, functioned as negative regulators of autophagy and lifespan. The storage of phosphate in form of polyphosphate was completely dispensable to in sustaining viability under phosphate restriction. Collectively, our results identify the multifunctional, nutrient-sensing kinase Pho85 as critical modulator of longevity that differentially coordinates the autophagic response to distinct kinds of starvation.

PERK13 modulates phosphate deficiency-induced root hair elongation in Arabidopsis.

Phosphate starvation (-Pi)-induced root hair is crucial for enhancing plants' Pi absorption. Proline-rich extensin-like receptor kinase 13 (PERK13) is transcriptionally induced by -Pi and co-expressed with genes associated with root hair growth. However, how PERK13 participates in -Pi-induced root hair growth remains unclear. Here, we found that PERK13 was transcriptionally responsive to Pi, nitrogen, and iron deficiencies. Loss of PERK13 function (perk13) enhanced root hair growth under Pi/nitrogen limitation. Similar phenotype was also observed in transgenic lines overexpressing PERK13 (PERK13ox). Under -Pi, both perk13 and PERK13ox showed prolonged root hair elongation and increased reactive oxygen species (ROS). Deletion analysis showed, in PERK13ox, the extracellular domain was indispensable for PERK13 in -Pi-induced root hair growth. Different transcription profiles were observed under -Pi between perk13 and PERK13ox with the jasmonate zim-domain genes being repressed in perk13 and genes involved in cell wall remodeling being increased in PERK13ox. Taken together, we demonstrated that PERK13 participates in -Pi-induced root hair growth probably via regulating root hair elongation and the generation of ROS. Our study also suggested PERK13 probably being a vital hub coupling the environmental cues and root hair growth, and might play dual roles in -Pi-induced root hair growth via different processes.

A phosphate starvation response-centered network regulates mycorrhizal symbiosis.

To secure phosphorus (P) from soil, most land plants use a direct phosphate uptake pathway via root hairs and epidermis and an indirect phosphate uptake pathway via mycorrhizal symbiosis. The interaction between these two pathways is unclear. Here, we mapped a network between transcription factors and mycorrhizal symbiosis-related genes using Y1H. Intriguingly, this gene regulatory network is governed by the conserved P-sensing pathway, centered on phosphate starvation response (PHR) transcription factors. PHRs are required for mycorrhizal symbiosis and regulate symbiosis-related genes via the P1BS motif. SPX-domain proteins suppress OsPHR2-mediated induction of symbiosis-related genes and inhibit mycorrhizal infection. In contrast, plants overexpressing OsPHR2 show improved mycorrhizal infection and are partially resistant to P-mediated inhibition of symbiosis. Functional analyses of network nodes revealed co-regulation of hormonal signaling and mycorrhizal symbiosis. This network deciphers extensive regulation of mycorrhizal symbiosis by endogenous and exogenous signals and highlights co-option of the P-sensing pathway for mycorrhizal symbiosis.

Transcription Factor WRKY33 Mediates the Phosphate Deficiency-Induced Remodeling of Root Architecture by Modulating Iron Homeostasis in Arabidopsis Roots.

The remodeling of root architecture is regarded as a major development to improve the plant's adaptivity to phosphate (Pi)-deficient conditions. The WRKY transcription factors family has been reported to regulate the Pi-deficiency-induced systemic responses by affecting Pi absorption or transportation. Whether these transcription factors act as a regulator to mediate the Pi-deficiency-induced remodeling of root architecture, a typical local response, is still unclear. Here, we identified an Arabidopsis transcription factor, WRKY33, that acted as a negative regulator to mediate the Pi-deficiency-induced remodeling of root architecture. The disruption of WRKY33 in wrky33-2 mutant increased the plant's low Pi sensitivity by further inhibiting the primary root growth and promoting the formation of root hair. Furthermore, we revealed that WRKY33 negatively regulated the remodeling of root architecture by controlling the transcriptional expression of ALMT1 under Pi-deficient conditions, which further mediated the Fe3+ accumulation in root tips to inhibit the root growth. In conclusion, this study demonstrates a previously unrecognized signaling crosstalk between WRKY33 and the ALMT1-mediated malate transport system to regulate the Pi deficiency responses.

Phosphate starvation responsive GmSPX5 mediates nodule growth through interaction with GmNF-YC4 in soybean (Glycine max).

Phosphorus (P) deficiency adversely affects nodule development as reflected by reduced nodule fresh weight in legume plants. Though mechanisms underlying nodule adaptation to P deficiency have been studied extensively, it remains largely unknown which regulator mediates nodule adaptation to P deficiency. In this study, GUS staining and quantitative reverse transcription-PCR analysis reveal that the SPX member GmSPX5 is preferentially expressed in soybean (Glycine max) nodules. Overexpression of GmSPX5 enhanced soybean nodule development particularly under phosphate (Pi) sufficient conditions. However, the Pi concentration was not affected in soybean tissues (i.e., leaves, roots, and nodules) of GmSPX5 overexpression or suppression lines, which distinguished it from other well-known SPX members functioning in control of Pi homeostasis in plants. Furthermore, GmSPX5 was observed to interact with the transcription factor GmNF-YC4 in vivo and in vitro. Overexpression of either GmSPX5 or GmNF-YC4 significantly upregulated the expression levels of five asparagine synthetase-related genes (i.e., GmASL2-6) in soybean nodules. Meanwhile, yeast one-hybrid and luciferase activity assays strongly suggested that interactions of GmSPX5 and GmNF-YC4 activate GmASL6 expression through enhancing GmNF-YC4 binding of the GmASL6 promoter. These results not only demonstrate the GmSPX5-GmNF-YC4-GmASL6 regulatory pathway mediating soybean nodule development, but also considerably improve our understanding of SPX functions in legume crops.

Combined Transcriptome and Proteome Analysis of Maize (Zea mays L.) Reveals A Complementary Profile in Response to Phosphate Deficiency.

A deficiency in the macronutrient phosphate (Pi) brings about various changes in plants at the morphological, physiological and molecular levels. However, the molecular mechanism for regulating Pi homeostasis in response to low-Pi remains poorly understood, particularly in maize (Zea mays L.), which is a staple crop and requires massive amounts of Pi. Therefore, in this study, we performed expression profiling of the shoots and roots of maize seedlings with Pi-tolerant genotype at both the transcriptomic and proteomic levels using RNA sequencing and isobaric tags for relative and absolute quantitation (iTRAQ). We identified 1944 differentially expressed transcripts and 340 differentially expressed proteins under low-Pi conditions. Most of the differentially expressed genes were clustered as regulators, such as transcription factors involved in the Pi signaling pathway at the transcript level. However, the more functional and metabolism-related genes showed expression changes at the protein level. Moreover, under low-Pi conditions, Pi transporters and phosphatases were specifically induced in the roots at both the transcript and protein levels, and increased amounts of mRNA and protein of two purple acid phosphatases (PAPs) and one UDP-sulfoquinovose synthase (SQD) were specifically detected in the roots. The new insights provided by this study will help to improve the P-utilization efficiency of maize.

Greater morphological and primary metabolic adaptations in roots contribute to phosphate-deficiency tolerance in the bread wheat cultivar Kenong199.

BACKGROUND: Phosphate (Pi) deficiency severely affects crop growth and productivity, including wheat, therefore it is necessary to develop cultivars with enhanced Pi-deficiency tolerance. However, the underlying mechanism of Pi-deficiency tolerance in wheat is still elusive. Two contrasting wheat cultivars, low-Pi tolerant Kenong199 (KN199) and low-Pi sensitive Chinese Spring (CS) were used to reveal adaptations in response to Pi deficiency at the morphological, physiological, metabolic, and molecular levels. RESULTS: KN199 was more tolerant to Pi deficiency than CS with significantly increased root biomass and R/S ratio. Root traits, the total root length, total root surface area, and total root volume, were remarkably enhanced by Pi deficiency in KN199. The shoot total P and soluble Pi concentrations of KN199 were significantly higher than those of CS, but not in roots. In KN199, high Pi level in shoots is a higher priority than that in roots under Pi deficiency. It was probably due to differentially regulation in the miR399-mediated signaling network between the shoots of the two cultivars. The Pi deficiency-induced root architecture adaptation in KN199 was attributed to the regulation of the hormone-mediated signaling (ethylene, gibberellin, and jasmonates). The expression of genes associated with root development and Pi uptake was enhanced in KN199. Some primary metabolites (amino acids and organic acids) were significantly accumulated in roots of KN199 under Pi deficiency. CONCLUSIONS: The low-Pi tolerant wheat cultivar KN199 possessed greater morphological and primary metabolic adaptations in roots than CS under Pi deficiency. The adaption and the underlying molecular mechanisms in wheat provide a better understanding of the Pi-deficiency tolerance and the strategies for improving Pi efficiency in wheat.

Modulation of Phosphate Deficiency-Induced Metabolic Changes by Iron Availability in Arabidopsis thaliana.

Concurrent suboptimal supply of several nutrients requires the coordination of nutrient-specific transcriptional, phenotypic, and metabolic changes in plants in order to optimize growth and development in most agricultural and natural ecosystems. Phosphate (Pi) and iron (Fe) deficiency induce overlapping but mostly opposing transcriptional and root growth responses in Arabidopsis thaliana. On the metabolite level, Pi deficiency negatively modulates Fe deficiency-induced coumarin accumulation, which is controlled by Fe as well as Pi deficiency response regulators. Here, we report the impact of Fe availability on seedling growth under Pi limiting conditions and on Pi deficiency-induced accumulation of amino acids and organic acids, which play important roles in Pi use efficiency. Fe deficiency in Pi replete conditions hardly changed growth and metabolite profiles in roots and shoots of Arabidopsis thaliana, but partially rescued growth under conditions of Pi starvation and severely modulated Pi deficiency-induced metabolic adjustments. Analysis of T-DNA insertion lines revealed the concerted coordination of metabolic profiles by regulators of Fe (FIT, bHLH104, BRUTUS, PYE) as well as of Pi (SPX1, PHR1, PHL1, bHLH32) starvation responses. The results show the interdependency of Pi and Fe availability and the interplay between Pi and Fe starvation signaling on the generation of plant metabolite profiles.

Primary root and root hair development regulation by OsAUX4 and its participation in the phosphate starvation response.

Among the five members of AUX1/LAX genes coding for auxin carriers in rice, only OsAUX1 and OsAUX3 have been reported. To understand the function of the other AUX1/LAX genes, two independent alleles of osaux4 mutants, osaux4-1 and osaux4-2, were constructed using the CRISPR/Cas9 editing system. Homozygous osaux4-1 or osaux4-2 exhibited shorter primary root (PR) and longer root hair (RH) compared to the wild-type Dongjin (WT/DJ), and lost response to indoleacetic acid (IAA) treatment. OsAUX4 is intensively expressed in roots and localized on the plasma membrane, suggesting that OsAUX4 might function in the regulation of root development. The decreased meristem cell division activity and the downregulated expression of cell cycle genes in root apices of osaux4 mutants supported the hypothesis that OsAUX4 positively regulates PR elongation. OsAUX4 is expressed in RH, and osaux4 mutants showing longer RH compared to WT/DJ implies that OsAUX4 negatively regulates RH development. Furthermore, osaux4 mutants are insensitive to Pi starvation (-Pi) and OsAUX4 effects on the -Pi response is associated with altered expression levels of Pi starvation-regulated genes, and auxin distribution/contents. This study revealed that OsAUX4 not only regulates PR and RH development but also plays a regulatory role in crosstalk between auxin and -Pi signaling.

Long-distance blue light signalling regulates phosphate deficiency-induced primary root growth inhibition.

Although roots are mainly embedded in the soil, recent studies revealed that light regulates mineral nutrient uptake by roots. However, it remains unclear whether the change in root system architecture in response to different rhizosphere nutrient statuses involves light signaling. Here, we report that blue light regulates primary root growth inhibition under phosphate-deficient conditions through the cryptochromes and their downstream signaling factors. We showed that the inhibition of root elongation by low phosphate requires blue light signal perception at the shoot and transduction to the root. In this process, SPA1 and COP1 play a negative role while HY5 plays a positive role. Further experiments revealed that HY5 is able to migrate from the shoot to root and that the shoot-derived HY5 autoactivates root HY5 and regulates primary root growth by directly activating the expression of LPR1, a suppressor of root growth under phosphate starvation. Taken together, our study reveals a regulatory mechanism by which blue light signaling regulates phosphate deficiency-induced primary root growth inhibition, providing new insights into the crosstalk between light and nutrient signaling.