- Research article
- Open Access
Identification and expression analysis of OsLPR family revealed the potential roles of OsLPR3 and 5 in maintaining phosphate homeostasis in rice
© The Author(s). 2016
- Received: 21 February 2016
- Accepted: 14 July 2016
- Published: 3 October 2016
Phosphorus (P), an essential macronutrient, is often limiting in soils and affects plant growth and development. In Arabidopsis thaliana, Low Phosphate Root1 (LPR1) and its close paralog LPR2 encode multicopper oxidases (MCOs). They regulate meristem responses of root system to phosphate (Pi) deficiency. However, the roles of LPR gene family in rice (Oryza sativa) in maintaining Pi homeostasis have not been elucidated as yet.
Here, the identification and expression analysis for the homologs of LPR1/2 in rice were carried out. Five homologs, hereafter referred to as OsLPR1-5, were identified in rice, which are distributed on chromosome1 over a range of 65 kb. Phylogenetic analysis grouped OsLPR1/3/4/5 and OsLPR2 into two distinct sub-clades with OsLPR3 and 5 showing close proximity. Quantitative real-time RT-PCR (qRT-PCR) analysis revealed higher expression levels of OsLPR3-5 and OsLPR2 in root and shoot, respectively. Deficiencies of different nutrients ie, P, nitrogen (N), potassium (K), magnesium (Mg) and iron (Fe) exerted differential and partially overlapping effects on the relative expression levels of the members of OsLPR family. Pi deficiency (−P) triggered significant increases in the relative expression levels of OsLPR3 and 5. Strong induction in the relative expression levels of OsLPR3 and 5 in osphr2 suggested their negative transcriptional regulation by OsPHR2. Further, the expression levels of OsLPR3 and 5 were either attenuated in ossiz1 and ospho2 or augmented in rice overexpressing OsSPX1.
The results from this study provided insights into the evolutionary expansion and a likely functional divergence of OsLPR family with potential roles of OsLPR3 and 5 in the maintenance of Pi homeostasis in rice.
- Phosphate deficiency
- OsLPR family
- Phosphate homeostasis
Phosphorus (P), one of the essential macronutrients, is required for several biochemical and physiological processes and is a component of key macromolecules including nucleic acids, ATP and membrane phospholipids . P is absorbed from rhizosphere as phosphate (Pi), which is often not easily available to plants due to its slow diffusion rates in soils and/or fixation as immobile organic Pi . Limited Pi availability adversely affects growth and development of plants .
In Arabidopsis thaliana, Pi deficiency triggers progressive loss of meristematic activity in primary root tip thereby inhibiting primary root growth (PRG) . LPR1 (At1g23010) and its close paralog LPR2 (At1g71040), encoding multicopper oxidases (MCOs), are major quantitative trait loci (QTLs) associated with Pi deficiency-mediated inhibition of PRG [5, 6]. Loss-of-function mutations in LPR1 and LPR2 affect Pi deficiency-mediated inhibition of PRG . However, unlike Arabidopsis, Pi deficiency either does not exert any significant effect on PRG of taxonomically diverse dicots and monocots [7, 8] or triggeres augmented PRG in rice [9, 10]. These studies suggested that Pi deficiency-mediated inhibition of PRG is not a global response across different plant species. This raised an obvious question about the likely role of homologs of LPR1/2 particularly in species such as rice in which Pi deficiency has a rather contrasting influence on PRG.
Nuclear-localized SIZ1 (At5g60410) encodes a small ubiquitin-like modifier (SUMO) E3 ligase1 and sumoylates transcription factor (TF) PHR1 (At4g28610) in Arabidopsis . PHR1 plays a pivotal role in regulating the expression of Pi 3starvation-responsive (PSR) genes whose promoters are enriched with PHR1-binding sequence (P1BS) motif . PHR1 is a pivotal upstream component of the Pi sensing and signaling cascade comprising miR399s, IPS1 (At3g09922), PHO2 (At2g33770), SPX1 (At5g20150), Pi transporters Pht1;8 (At1g20860),Pht1;9 (At1g76430) and a subset of other PSR genes [13–15]. Interestingly though, promoters of both LPR1 and LPR2 do not have P1BS motif, which suggests a lack of any regulatory influence of PHR1 on the expression of these genes. Therefore, the identification of TFs that regulate LPR1/2 solicits further studies.
Rice, one of the most important cereal crops, feeds over one-third population of the world and sometimes is the only source of calories [16, 17]. Rice is often cultivated in rain-fed system on soils that are poor in Pi availability, which affects its growth and development and consequently the yield potential . Therefore, it is increasingly becoming imperative to decipher the intricacies involved in the maintenance of Pi homeostasis for developing rice with higher Pi use efficiency for the sustainability of agriculture. Pi starvation signal transduction pathway is highly conserved between Arabidopsis and rice . In this context, several homologs of Arabidopsis in rice ie, OsPHR2 [18, 19], OsPHO2 [20, 21], OsSPX1 and OsSPX2  have been functionally characterized and are pivotal components of Pi sensing and signaling cascade . However, the roles of homologs of LPR1/2 in rice during the maintenance of Pi homeostasis have not been elucidated as yet.
In this study, the identification and expression analysis of OsLPR1-5 in rice were carried out. Phylogenetic analysis revealed their grouping into two distinct subclades. Differential expression of these genes under both Pi-replete and Pi-deprived conditions and also under other nutrient deficiencies suggested functional divergence across them. Further, analyses of the relative expression levels of OsLPR3 and OsLPR5 in loss-of-function mutants (ossiz1, osphr2 and ospho2) and transgenic rice overexpressing either OsPHR2 or OsSPX1 provided an insight into their potential roles in Pi sensing and signaling cascade.
Comparative structure analysis of LPRs in Arabidopsis and rice
Phylogenetic analysis of LPR genes
Cu-oxidase domain analysis of LPR proteins in rice
Tissue-specific expression profiles of OsLPRs
Nutrient deficiencies affect the expression profiles of OsLPRs
Phosphite represses OsLPR3/5 responses to Pi deficiency in rice
Short- and long-term effects of Pi deficiency on the expression profiles of OsLPRs in the roots
Split-root experiment revealed the effect of systemic Pi sensing on the relative expression levels of OsLPR3/5
OsLPR3/5 are negatively regulated by OsPHR2 and are influenced by SIZ1/PHO2/SPX1-mediated Pi sensing
Transcript levels of OsSPX1 induced in –P root and stem and also in OsPHR2-Ox plants suggesting the former to be downstream of the latter . Another study demonstrated the inhibition in the activity of OsPHR2 by OsSPX1 in a Pi-dependent manner . Together these studies suggested a negative feedback loop regulation of OsPHR2 by OsSPX1. Since the relative expression levels of OsLPR3 and OsLPR5 were significantly increased in osphr2 under both + P and –P conditions (Fig. 9a), a similar expression pattern was anticipated in SPX1-Ox. Consistent with this assumption, significant increases in the relative expression levels of OsLPR3 and OsLPR5 were observed in SPX1-Ox under both + P and –P conditions compared with their corresponding wild types (Fig. 9c). On the contrary, relative expression levels of OsLPR4 in SPX1-Ox (+P and –P) were comparable with the wild type. This suggested that OsLPR3 and OsLPR5 are part of OsPHR2-OsSPX1-mediated regulation of Pi homeostasis.
OsPHO2, a signaling component downstream of OsPHR2, plays a key role in regulating the expression of OsPTs and multiple Pi starvation responses thereby influencing Pi utilization in rice [20, 21]. Therefore, the regulatory influence of OsPHO2 on OsLPR3-5 was investigated (Fig. 9d). There were significant increases in the relative expression levels of OsLPR3 in pho2-1 and pho2-2 compared with the wild type. An increased expression of OsSPX1 in the roots of pho2 mutant suggested a negative regulatory influence of OsPHO2 on its downstream OsSPX1 . The accentuated relative expression levels of OsLPR3 in SPX1-Ox (Fig. 9c) and pho2-1 and pho2-2 (Fig. 9d) thus suggested it to be downstream of OsPHR2-OsPHO2-OsSPX1 pathway. On the contrary, significant reductions and no effect on the relative expression levels of OsLPR5 and OsLPR4, respectively in pho2-1 and pho2-2 compared with the wild type (Fig. 9d) highlighted differential roles of the members of OsLPR family in OsPHR2-OsPHO2-OsSPX1-mediated Pi sensing.
Sumoylation is a critical post-translational modification involved in protein-protein interaction, transcriptional activation and localization of proteins . OsSIZ1 and OsSIZ2, homologs of Arabidopsis SIZ1 in rice, partially complemented the morphological phenotype of siz1-2 in Arabidopsis . Further, several genes involved in Pi sensing and signaling were modulated in ossiz1 . Therefore, the effects of OsSIZ1 on the regulation of OsLPR3-5, were assayed (Fig. 9e). Significant reductions were observed in the relative expression levels of OsLPR3 and OsLPR5 in both siz1-1 and siz1-2 compared with the wild-type. Although marginal reductions in the expression levels of OsLPR4 were also detected in these mutants, the values were statistically insignificant. This suggested a post-translational regulatory influence of OsSIZ1 on OsLPR3 and OsLPR5. However, at present it is not known whether OsSIZ1 exerts direct regulatory influence on OsLPR3 and OsLPR5 by sumoylating them or mediated through a target, which is yet to be identified. Functional characterization of OsLPRs could provide an insight into their specific roles in maintaining Pi homeostasis and thus warrants further studies.
This study presented a detailed genome-wide analysis of the gene structure, phylogenetic evolution and tissue-specific expression patterns of LPR family members in rice (OsLPR1- OsLPR5). Phylogenetic analysis revealed their grouping into two distinct subclades. Differential expression of these genes under deficiencies of Pi and other nutrients suggested lack of functional redundancy across them. Further an insight into the likely roles of OsLPR3 and OsLPR5 in the maintenance of Pi homeostasis was gained by assaying their relative expression levels in loss-of-function mutants (ossiz1, osphr2 and ospho2) and transgenic rice overexpressing either OsPHR2 or OsSPX1. The results from this study thus provide a basis for further detailed functional characterization of different members of OsLPR family for elucidation of their specific roles in maintaining homeostasis during deficiency of Pi and/or other nutrients.
Database searches, sequence alignment and phylogenetic analysis
Complete genomic sequence and transcripts of OsLPR1-5 were retrieved from Michigan State University (MSU) Rice Genome Annotation Project assembly (v7) (http://rice.plantbiology.msu.edu/). Identification of LPR homologs was performed using tBLASTn program and PLAZA1.0 database (http://bioinformatics.psb.ugent.be/plaza/). LPR homologs were identified in dicots (Arabidopsis thaliana, Capsella rubella, Carica papaya, Cicer arietinum, Cucumis sativus, Fragaria vesca, Glycine max, Lotus japonicus, Malus domestica, Manihot esculenta, Populus trichocarpa, Prunus persica, Ricinus communis, Solanum lycopersicum, Theobroma cacao and Vitis vinifera), monocots (Aegilop stauschii, Brachypodium distachyon, Hordeum vulgare, Oryza sativa, Setaria italica, Sorghum bicolor, Triticum urartu and Zea mays), gymnosperms (Picea sitchensis and Selaginella moellendorffii), bryophytes (Physcomitrella patens) and chlorophyta (Volvox carteri and Chlamydomonas reinhardtii). The unrooted phylogenetic tree of LPR homologs was made using the neighbor-joining method and displayed using the MEGA4.0 program.
Plant materials and growth conditions
In the present study, wild type rice (Oryza sativa) ssp. japonica varieties (Nipponbare, ZH11 and Dongjin), T-DNA insertion mutants (ospho2-1/2 , ossiz1-1/2 , osphr2  in the backgrounds of Nipponbare, Dongjin and ZH11, respectively) and two homozygous overexpresors (OsSPX1-Ox  and OsPHR2-Ox [Gu unpublished work] in Nipponbare background) were used. For OsPHR2 overexpressors, the ORF of OsPHR2 was amplified using the specific primers from Nipponbare cDNA. The PCR product was ligated into the pTCK303 vector as described . By electroporation, the construct was transferred to Agrobacterium tumefaciens strain EHA105 and then transformed into Nipponbare as described . For hydroponic experiments, rice seeds were surface-sterilized for 1 min with 75 % ethanol (v/v) and for 30 min with diluted (1:3, v/v) NaClO followed by thorough rinsing for 30 min with deionized water. Seeds were germinated in dark at 25 °C for 3 d. The hydroponic experiments were carried out in a growth room with a 16-h-light (30 °C)/8-h-dark (22 °C) photoperiod and the relative humidity was maintained at approximately 70 %. Uniformly grown seedlings (7-d-old) were then transferred to complete nutrient solution containing 1.25 mM NH4NO3, 300 μM KH2PO4, 0.35 mM K2SO4, 1 mM CaCl2 · 2H2O, 1 mM MgSO4 · 7H2O, 0.5 mM Na2SiO3 · 9H2O, 20 μM Fe-EDTA, 20 μM H3BO3, 9 μM MnCl2 · 4H2O, 0.32 μM CuSO4 · 5H2O, 0.77 μM ZnSO4 · 7H2O and 0.39 μM Na2MoO4 · 2H2O. For + P (control) and –P media, KH2PO4 concentrations used were 300 μM and 0 μM, respectively. To maintain equimolar concentration of K in + P and –P media, KH2PO4 in + P medium was replaced with K2SO4 in –P medium. For + K (control) and –K media, 300 μM KH2PO4 and 300 μM NaH2PO4 were used, respectively. For + Mg (control) and –Mg media, 1 mM MgSO4 · 7H2O and 1 mM Na2SO4 · 7H2O were used, respectively. For –Fe medium, 20 μM Fe-EDTA was eliminated from + Fe (control) medium. Deionized water was used throughout the experiments and pH of all the nutrient solutions were adjusted to 5.0. For all the experiments, nutrient solutions in the hydroponic set up were refreshed every 3rd d. For Pi split-root experiment, seedlings were prepared and grown in complete nutrient solution for 14 d, and then transferred to split-root container for 14 d. The roots of individual plants were separated into two equal parts, placed into separate containers such that one half received 300 μM Pi, while the other half did not receive any Pi. The controls included a split-root treatment in which both halves of the roots received + Pi (300 μM Pi) and –P (0 μM Pi). For Phi treatment, seedlings were grown in –Pi (0 μM Pi) for 21 d. Uniformly grown seedlings were then transferred to + Pi (300 μM Pi), −Pi (0 μM Pi) and + Phi/–Pi (300 μM Phi, 0 μM Pi) solutions for 3 d.
Total RNAs from various tissues were isolated using Trizol reagent (Invitrogen) and first-strand cDNA was synthesized with an oligo (dT)-18 primer and reverse transcriptase. OsActin (accession no. AB047313) was used as an internal control for qRT-PCR analysis. qRT-PCR analysis was performed using SYBR green master mix (Vazyme) and ABI StepOnePlus Sequence Detection System (Applied Biosystems), from biological triplicates. Primers used for qRT-PCR are listed in Additional file 8.
Measurements of Pi and total P concentrations in plants
To measure Pi concentration in plants, about 0.5 g Fresh sample was used for the quantification of Pi concentration in plants as described . Total P concentration was quantified by digesting dry sample (0.05 g) with H2SO4-H2O2 at 280 °C followed by assay with molybdenum blue as described .
Data were analyzed by analysis of variance (ANOVA) using the SPSS 13 program. Different letters or asterisks on the histograms between the mutants and the WT and/or different treatments indicate their statistically significant difference using Duncan multiple range test at P < 0.05.
AREB1, ABSCISIC ACID-RESPONSIVE ELEMENT BINDING PROTEIN1; Fe, iron; FFRL, feed-forward regulatory loop; K, Potassium; LTN1, LEAF TIP NECROSIS1; LPR1, low phosphate root1; lpsi, local phosphate sensing impaired; Mg, magnesium; MCOs, multicopper oxidases; MSU, Michigan State University; N, nitrogen; NAC016, NAM/ATAF1/2/CUC2016; NAP, NAC-LIKE, ACTIVATED BY AP3/PI; NCBI, National Center for Biotechnology Information; Ox, overexpressing; P, phosphorus; Pi, phosphate; Phi, phosphite; −P, Pi deficiency; P1BS, PHR1-binding sequence; PSR, Pi starvation-responsive; PRG, primary root growth; PAP, purple acid phosphatase; SUMO, small ubiquitin-like modifier; qRT-PCR, quantitative real-time PCR; QTLs, quantitative trait loci; SI, sequence identity; TF, transcription factor; TNC, trinuclear Cu cluster; UTR, untranslated region
This work was supported by the Chinese National Natural Science Foundation (31172014), the National Program on R&D of Transgenic Plants (2014ZX08 009-003-005, 2014ZX0800931B and 2016ZX08009-003-005), the Jiangsu Provincial Natural Science Foundation (BK20141367), the Innovative Research Team Development Plan of the Ministry of Education (IRT1256) and the 111 Project (number 12009). We also thank the Ministry of Science and Technology, Department of Biotechnology, Government of India for awarding Ramalingaswamy Fellowship to A.J. [BT/HRD/35/02/26/2009]. We also acknowledge Viswanathan Satheesh for his valuable suggestions and correction during the preparation and revision of this manuscript.
Availability of data and materials
All the data supporting the present findings is contained within the manuscript.
YC participated in planning and conducting the experiments, did bioinformatics analysis and helped in writing the manuscript. HA carried out some experiments. AJ participated in analysis of the data, and helped in writing the manuscript. XW, LZ and WP participated in carrying out different experiments. AC helped in bioinformatics analysis. GX participated in planning the study. SS conceived the study, participated in planning and analysis of the data, and helped in writing the manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
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- Raghothama KG. Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol. 1999;50:665–93.View ArticlePubMedGoogle Scholar
- Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ, et al. Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol. 2012;195:306–20.View ArticlePubMedGoogle Scholar
- López-Arredondo DL, Leyva-González MA, González-Morales SI, López-Bucio J, Herrera-Estrella L. Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol. 2014;65:95–123.View ArticlePubMedGoogle Scholar
- Sánchez-Calderón L, López-Bucio J, Chacón-López A, Cruz-Ramírez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L. Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol. 2005;46:174–84.View ArticlePubMedGoogle Scholar
- Reymond M, Svistoonoff S, Loudet O, Nussaume L, Desnos T. Identification of QTL controlling root growth response to phosphate starvation in Arabidopsis thaliana. Plant Cell Environ. 2006;29:115–25.View ArticlePubMedGoogle Scholar
- Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, Blanchet A, Laurent Nussaume L, Thierry DT. Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet. 2007;39:792–6.View ArticlePubMedGoogle Scholar
- Narayanan A, Reddy BK. Effect of phosphorus deficiency on the form of plant root system. In: Scaife A, editor. Plant nutrition, vol. 2. Slough: Commonwealth Agricultural Bureau; 1982. p. 412–7.Google Scholar
- Mollier A, Pellerin S. Maize root system growth and development as influenced by phosphorus deficiency. J Exp Bot. 1999;50:487–97.View ArticleGoogle Scholar
- Shimizu A, Yanagihara S, Kawasaki S, Ikehashi H. Phosphorus deficiency-induced root elongation and its QTL in rice (Oryza sativa L.). Theor Appl Genet. 2004;109:1361–8.View ArticlePubMedGoogle Scholar
- Yi KK, Wu ZC, Zhou J, Du LM, Guo LB, Wu YR, Wu P. OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiol. 2005;138:2087–96.View ArticlePubMedPubMed CentralGoogle Scholar
- Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, et al. The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci U S A. 2005;102:7760–5.View ArticlePubMedPubMed CentralGoogle Scholar
- Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, Leyva A, Paz-Ares J. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Gene Dev. 2001;15:2122–33.View ArticlePubMedPubMed CentralGoogle Scholar
- Bari R, Pant BD, Stitt M, Scheible WR. PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 2006;141:988–99.View ArticlePubMedPubMed CentralGoogle Scholar
- Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, García JA, Javier Paz-Ares J. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet. 2007;39:1033–7.View ArticlePubMedGoogle Scholar
- Puga MI, Mateosa I, Charukesi R, Wang ZY, Franco-Zorrilla JM, de Lorenzo L, Irigoyen ML, Masiero S, Bustos R, Rodríguez J, et al. SPX1 is a phosphate-dependent inhibitor of phosphate starvation response1 in Arabidopsis. Proc Natl Acad Sci U S A. 2014;111:14947–52.View ArticlePubMedPubMed CentralGoogle Scholar
- Gamuyao R, Chin JH, Pariasca-Tanaka J, Pesaresi P, Catausan S, Dalid C, Slamet-Loedin I, Tecson-Mendoza EM, Wissuwa M, Heuer S. The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature. 2012;488:535–9.View ArticlePubMedGoogle Scholar
- Wu P, Shou HX, Xu GH, Lian XM. Improvement of phosphorus efficiency in rice on the basis of understanding phosphate signaling and homeostasis. Curr Opin Plant Biol. 2013;16:205–12.View ArticlePubMedGoogle Scholar
- Zhou J, Jiao FC, Wu ZC, Li YY, Wang XM, He XW, Zhong WQ, Wu P. OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol. 2008;146:1673–86.View ArticlePubMedPubMed CentralGoogle Scholar
- Guo MN, Ruan WY, Li CY, Huang FL, Zeng M, Liu YY, Yu YN, Ding XM, Wu YR, Wu ZC, et al. Integrative comparison of the role of the phosphate responses1 subfamily in phosphate signaling and homeostasis in rice. Plant Physiol. 2015;168:1762–76.View ArticlePubMedPubMed CentralGoogle Scholar
- Hu B, Zhu CG, Li F, Tang JY, Wang YQ, Lin AH, Liu LC, Che RH, Chu CC. LEAF TIP NECROSIS1 plays a pivotal role in the regulation of multiple phosphate starvation responses in rice. Plant Physiol. 2011;156:1101–15.View ArticlePubMedPubMed CentralGoogle Scholar
- Cao Y, Yan Y, Zhang F, Wang HD, Gu M, Wu XR, Sun SB, Xu GH. Fine characterization of OsPHO2 knockout mutants reveals its key role in Pi utilization in rice. J Plant Physiol. 2014;171:340–8.View ArticlePubMedGoogle Scholar
- Wang ZY, Ruan WY, Shi J, Zhang L, Xiang D, Yang C, Li CY, Wu ZC, Liu Y, Yu YA, et al. Rice SPX1 and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner. Proc Natl Acad Sci U S A. 2014;111:14953–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Solomon EI, Augustine AJ, Yoon J. O2 reduction to H2O by the multicopper oxidases. Dalton Trans. 2008;30:3921–32.View ArticlePubMedGoogle Scholar
- Müller J, Toev T, Heisters M, Teller J, Moore KL, Hause G, Dinesh DC, Bürstenbinder K, Abel S. Iron-dependent callose deposition adjusts root meristem maintenance to phosphate availability. Dev Cell. 2015;33:216–30.View ArticlePubMedGoogle Scholar
- Coudert Y, Périn C, Courtois B, Khong NG, Gantet P. Genetic control of root development in rice, the model cereal. Trends Plant Sci. 2010;15:219–26.View ArticlePubMedGoogle Scholar
- Zheng L, Huang F, Narsai R, Wu J, Giraud E, He F, Cheng L, Wang F, Wu P, Whelan J, et al. Physiological and transcriptome analysis of iron and phosphorus interaction in rice seedlings. Plant Physiol. 2009;151:262–74.View ArticlePubMedPubMed CentralGoogle Scholar
- Wang Z, Hu H, Huang HJ, Duan K, Wu ZC, Wu P. Regulation of OsSPX1 and OsSPX3 on expression of OsSPX domain genes and Pi-starvation signaling in rice. J Integr Plant Biol. 2009;51:663–74.View ArticlePubMedGoogle Scholar
- Lv Qd, Zhong Yj, Wang Yg, Wang Zy, Zhang L, Shi J, Wu Zc, Liu Y, Mao Cz, Yi Kk, Wu P. SPX4 negatively regulates phosphate signaling and homeostasis through Its interaction with PHR2 in rice. Plant Cell. 2014;26:1586–97.View ArticlePubMedPubMed CentralGoogle Scholar
- Qin L, Guo YX, Chen LY, Liang RK, Gu M, Xu GH, Zhao J, Walk T, Liao H. Functional characterization of 14 Pht1 family genes in yeast and their expressions in response to nutrient starvation in soybean. PLoS One. 2012;7, e47726.View ArticlePubMedPubMed CentralGoogle Scholar
- Wang YH, Garvin DF, Kochian LV. Rapid induction of regulatory and transporter genes in response to phosphorus, potassium, and iron deficiencies in tomato roots: evidence for cross talk and root/rhizosphere-mediated signals. Plant Physiol. 2002;130:1361–70.View ArticlePubMedPubMed CentralGoogle Scholar
- Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N, et al. A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci U S A. 2005;102:11934–9.View ArticlePubMedPubMed CentralGoogle Scholar
- Ward JT, Lahner B, Yakubova E, Salt DE, Raghothama KG. The effect of iron on the primary root elongation of Arabidopsis during phosphate deficiency. Plant Physiol. 2008;147:1181–91.View ArticlePubMedPubMed CentralGoogle Scholar
- Rai V, Sanagala R, Sinilal B, Yadav S, Sarkar AK, Dantu PK, Jain A. Iron availability affects phosphate deficiency-mediated responses, and evidence of cross-talk with auxin and zinc in Arabidopsis. Plant Cell Physiol. 2015;56:1107–23.View ArticlePubMedGoogle Scholar
- Cai HM, Xie WB, Lian XM. Comparative analysis of differentially expressed genes in rice under nitrogen and phosphorus starvation stress conditions. Plant Mol Biol Rep. 2013;31:160–73.View ArticleGoogle Scholar
- Kant S, Peng M, Rothstein SJ. Genetic regulation by NLA and MicroRNA827 for maintaining nitrate-dependent phosphate homeostasis in Arabidopsis. PLoS Genet. 2011;7, e1002021.View ArticlePubMedPubMed CentralGoogle Scholar
- Cerutti T, Delatorre CA. Nitrogen and phosphorus interaction and cytokinin: responses of the primary root of Arabidopsis thaliana and the pdr1 mutant. Plant Sci. 2013;198:91–7.View ArticlePubMedGoogle Scholar
- Medici A, Marshall-Colon A, Ronzier E, Szponarski W, Wang R, Gojon A, Crawford NM, Ruffel S, Coruzzi GM, Krouk G. AtNIGT1/HRS1 integrates nitrate and phosphate signals at the Arabidopsis root tip. Nat Commun. 2015;6:6274–84.View ArticlePubMedPubMed CentralGoogle Scholar
- Schachtman DP, Shin R. Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol. 2007;58:47–69.View ArticlePubMedGoogle Scholar
- Ticconi CA, Delatorre CA, Abel S. Attenuation of phosphate starvation responses by phosphite in Arabidopsis. Plant Physiol. 2001;127:963–72.View ArticlePubMedPubMed CentralGoogle Scholar
- Varadarajan DK, Karthikeyan AS, Matilda PD, Raghothama KG. Phosphite, an analog of phosphate, suppresses the coordinated expression of genes under phosphate starvation. Plant Physiol. 2002;129:1232–40.View ArticlePubMedPubMed CentralGoogle Scholar
- Jost R, Pharmawati M, Lapis-Gaza HR, Rossig C, Berkowitz O, Lambers H, Finnegan PM. Differentiating phosphate-dependent and phosphate-independent systemic phosphate-starvation response networks in Arabidopsis thaliana through the application of phosphite. J Exp Bot. 2015;66:2501–14.View ArticlePubMedPubMed CentralGoogle Scholar
- Hou XL, Wu P, Jiao FC, Jia QJ, Chen HM, Yu J, Song XW, Yi KK. Regulation of the expression of OsIPS1 and OsIPS2 in rice via systemic and local Pi signalling and hormones. Plant Cell Environ. 2005;28:353–64.View ArticleGoogle Scholar
- Secco D, Jabnoune M, Walker H, Shou H, Wu P, Poirier Y, Whelan J. Spatio-temporal transcript profiling of rice roots and shoots in response to phosphate starvation and recovery. Plant Cell. 2013;25:4285–304.View ArticlePubMedPubMed CentralGoogle Scholar
- Ai PH, Sun SB, Zhao JN, Fan XR, Xin WJ, Guo Q, Yu L, Shen QR, Wu P, Miller AJ, et al. Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation. Plant J. 2009;57:798–809.View ArticlePubMedGoogle Scholar
- Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May ST, Rahn C, Swarup R, Woolaway KE, White PJ. Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol. 2003;132:578–96.View ArticlePubMedPubMed CentralGoogle Scholar
- Shin H, Shin HS, Dewbre GR, Harrison MJ. Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J. 2004;39:629–42.View ArticlePubMedGoogle Scholar
- Bariola PA, Howard CJ, Taylor CB, Verburg MT, Jaglan VD, Green PJ. The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant J. 1994;6:673–85.View ArticlePubMedGoogle Scholar
- Yu B, Xu CC, Benning C. Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proc Natl Acad Sci U S A. 2002;99:5732–7.View ArticlePubMedPubMed CentralGoogle Scholar
- Cruz-Ramírez A, Oropeza-Aburto A, Razo-Hernández F, Ramírez-Chávez E, Herrera-Estrella L. Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc Natl Acad Sci U S A. 2006;103:6765–70.View ArticlePubMedPubMed CentralGoogle Scholar
- Sun SB, Gu M, Cao Y, Huang XP, Zhang X, Ai PH, Zhao JN, Fan XR, Xu GH. A constitutive expressed phosphate transporter, OsPht1;1, modulates phosphate uptake and translocation in phosphate-replete rice. Plant Physiol. 2012;159:1571–81.View ArticlePubMedPubMed CentralGoogle Scholar
- Wang XF, Wang YF, Piñeros MA, Wang Z, Wang W, Li C, Wu Z, Kochian LV, Wu P. Phosphate transporters OsPHT1;9 and OsPHT1;10 are involved in phosphate uptake in rice. Plant Cell Environ. 2014;37:1159–70.View ArticlePubMedGoogle Scholar
- Li YT, Zhang J, Zhang X, Fan HM, Gu M, Qu HY, Xu GH. Phosphate transporter OsPht1;8 in rice plays an important role in phosphorus redistribution from source to sink organs and allocation between embryo and endosperm of seeds. Plant Sci. 2015;230:23–32.View ArticlePubMedGoogle Scholar
- Zhang F, Sun YF, Pei WX, Jain A, Sun R, Cao Y, Wu XR, Jiang TT, Zhang L, Fan XR, et al. Involvement of OsPht1;4 in phosphate acquisition and mobilization facilitates embryo development in rice. Plant J. 2015;82:556–69.View ArticlePubMedGoogle Scholar
- Burleigh SH, Harrison MJ. The down-Regulation of Mt4-Like genes by phosphate fertilization occurs systemically and involves phosphate translocation to the shoots. Plant Physiol. 1999;119:241–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Thibaud MC, Arrighi JF, Bayle V, Chiarenza S, Creff A, Bustos R, Paz-Ares J, Poirier Y, Nussaume L. Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J. 2010;64:775–89.View ArticlePubMedGoogle Scholar
- Jain A, Nagarajan VK, Raghothama KG. Transcriptional regulation of phosphate acquisition by higher plants. Cell Mol Life Sci. 2012;69:3207–24.View ArticlePubMedGoogle Scholar
- Sakuraba Y, Kim YS, Han SH, Lee BD, Paek NC. The Arabidopsis transcription Factor NAC016 promotes drought stress responses by repressing AREB1 transcription through a trifurcate feed-forward regulatory loop involving NAP. Plant Cell. 2015;27:1771–87.View ArticlePubMedPubMed CentralGoogle Scholar
- Ross CA, Liu Y, Shen QJ. The WRKY gene family in rice (Oryza sativa). J Integr Plant Biol. 2007;49:827–42.View ArticleGoogle Scholar
- Dai XY, Wang YY, Zhang WH. OsWRKY74, a WRKY transcription factor, modulates tolerance to phosphate starvation in rice. J Exp Bot. 2015;67:947–60.View ArticlePubMedPubMed CentralGoogle Scholar
- Wang C, Ying S, Huang HJ, Li K, Wu P, Shou HX. Involvement of OsSPX1 in phosphate homeostasis in rice. Plant J. 2009;57:895–904.View ArticlePubMedGoogle Scholar
- Miura K, Hasegawa PM. Sumoylation and other ubiquitin-like post-translational modifications in plants. Trends Cell Biol. 2010;20:223–32.View ArticlePubMedGoogle Scholar
- Park HC, Kim H, Koo SC, Park HJ, Cheong MS, Hong H, Baek D, Chung WS, Kim DH, Bressan RA, et al. Functional characterization of the SIZ/PIAS-type SUMO E3 ligases, OsSIZ1 and OsSIZ2 in rice. Plant Cell Environ. 2010;33:1923–34.View ArticlePubMedGoogle Scholar
- Wang HD, Sun R, Cao Y, Pei WX, Sun YF, Zhou H, Wu XN, Zhang F, Luo L, Shen QR, et al. OsSIZ1, a SUMO E3 ligase gene, is involved in the regulation of the responses to phosphate and nitrogen in rice. Plant Cell Physiol. 2015;56:2381–95.View ArticlePubMedGoogle Scholar
- Chen JY, Liu Y, Ni J, Wang YF, Bai YH, Shi J, Gan J, Wu ZC, Wu P. OsPHF1 regulates the plasma membrane localization of low-and high-affinity inorganic phosphate transporters and determines inorganic phosphate uptake and translocation in rice. Plant Physiol. 2011;157:269–78.View ArticlePubMedPubMed CentralGoogle Scholar
- Upadhyaya NM, Surin B, Ramm K, Gaudron J, Schunmann PHD, Taylor W, Waterhouse PM, Wang MB. Agrobacterium-mediated transformation of Australian rice cultivars Jarrah and Amaroo using modified promoters and selectable markers. Aust J Plant Physiol. 2000;27:201–10.Google Scholar
- Jia HF, Ren HY, Gu M, Zhao JN, Sun SB, Zhang X, Chen JY, Wu P, Xu GH. The phosphate transporter gene OsPht1;8 is involved in phosphate homeostasis in rice. Plant Physiol. 2011;156:1164–75.View ArticlePubMedPubMed CentralGoogle Scholar