Plant phosphate nutrition: sensing the stress

Viswanathan Satheesh, Ayesha Tahir, Jinkai Li, Mingguang Lei

Stress Biology ›› 2022, Vol. 2 ›› Issue (1) : 16. DOI: 10.1007/s44154-022-00039-0
Review

Plant phosphate nutrition: sensing the stress

Author information +
History +

Abstract

Phosphorus (P) is obtained by plants as phosphate (Pi) from the soil and low Pi levels affects plant growth and development. Adaptation to low Pi condition entails sensing internal and external Pi levels and translating those signals to molecular and morphophysiological changes in the plant. In this review, we present findings related to local and systemin Pi sensing with focus the molecular mechanisms behind root system architectural changes and the impact of hormones and epigenetic mechanisms affecting those changes. We also present some of the recent advances in the Pi sensing and signaling mechanisms focusing on inositol pyrophosphate InsP8 and its interaction with SPX domain proteins to regulate the activity of the central regulator of the Pi starvation response, PHR.

Keywords

Phosphate signaling / Root system architecture / Inositol pyrophosphates / InsP8 / SPX domain / Plant / Human

Cite this article

Download citation ▾
Viswanathan Satheesh, Ayesha Tahir, Jinkai Li, Mingguang Lei. Plant phosphate nutrition: sensing the stress. Stress Biology, 2022, 2(1): 16 https://doi.org/10.1007/s44154-022-00039-0

References

[1]
Adepoju O, Williams SP, Craige B, Cridland CA, Sharpe AK, Brown AM, Land E, Perera IY, Mena D, Sobrado P, Gillaspy GE (2019) Inositol trisphosphate kinase and Diphosphoinositol Pentakisphosphate kinase enzymes constitute the inositol pyrophosphate synthesis pathway in plants. bioRxiv. https://doi.org/10.1101/724914
[2]
Al-BabiliS, BouwmeesterHJ. Strigolactones a novel carotenoid-derived plant hormone. Annu Rev Plant Biol, 2015, 66: 161-186
CrossRef Google scholar
[3]
AzevedoC, SaiardiA. Eukaryotic phosphate homeostasis: the inositol pyrophosphate perspective. Trends Biochem Sci, 2017, 42(3):219-231
CrossRef Google scholar
[4]
BalzergueC, DartevelleT, GodonC, LaugierE, MeisrimlerC, TeulonJM, CreffA, BisslerM, BrouchoudC, HagègeA, MüllerJ, ChiarenzaS, JavotH, Becuwe-LinkaN, DavidP, PéretB, DelannoyE, ThibaudMC, ArmengaudJ, AbelS, PellequerJL, NussaumeL, DesnosT. Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation. Nat Commun, 2017, 8(1):15300
CrossRef Google scholar
[5]
BergwitzC, JüppnerH. Regulation of phosphate homeostasis by PTH, vitamin D, and FGF23. Annu Rev Med, 2010, 61: 91-104
CrossRef Google scholar
[6]
BerridgeMJ, IrvineRF. Inositol phosphates and cell signalling. Nature, 1989, 341: 197-205
CrossRef Google scholar
[7]
BeveridgeCA, SymonsGM, MurfetIC, RossJJ, RameauC. The rms1 mutant of pea has elevated indole-3-acetic acid levels andreduced root-sap zeatin riboside content but increased branching con-trolled by graft-transmissible signal(s). Plant Physiol, 1997, 115: 1251-1258
CrossRef Google scholar
[8]
BhosaleR, GiriJ, PandeyBK, GiehlRFH, HartmannA, TrainiR, et al.. A mechanistic framework for auxin dependent Arabidopsis root hair elongation to low external phosphate. Nat Commun, 2018, 9: 1409
CrossRef Google scholar
[9]
BorchK, BoumaTJ, LynchJP, BrownKM. Ethylene: a regulator of root architectural responses to soil phosphorus availability. Plant Cell Environ, 1999, 22(4):425-431
CrossRef Google scholar
[10]
BustosR, CastrilloG, LinharesF, PugaMI, RubioV, Pérez-PérezJ, SolanoR, LeyvaA, Paz-AresJ. A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet, 2010, 6(9):e1001102
CrossRef Google scholar
[11]
CaiXT, XuP, ZhaoPX, LiuR, YuLH, XiangCB. Arabidopsis ERF109 mediates cross-talk between jasmonic acid and auxin biosynthesis during lateral root formation. Nat Commun, 2014, 5(1):5833
CrossRef Google scholar
[12]
CampoS, San SegundoB. Systemic induction of phosphatidylinositol-based signaling in leaves of arbuscular mycorrhizal rice plants. Sci Rep, 2020, 10(1):1-17
CrossRef Google scholar
[13]
CastrilloG, TeixeiraPJPL, ParedesSH, LawTF, de LorenzoL, FeltcherME, FinkelOM, BreakfieldNW, MieczkowskiP, JonesCD, Paz-AresJ, DanglJL. Root microbiota drive direct integration of phosphate stress and immunity. Nature, 2017, 543: 513-518
CrossRef Google scholar
[14]
ChakrabortyA, KimS, SnyderSH. Inositol pyrophosphates as mammalian cell signals. Sci Signal, 2011, 4(188):re1
CrossRef Google scholar
[15]
ChandrikaNN, SundaravelpandianK, YuSM, SchmidtW. ALFIN-LIKE 6 is involved in root hair elongation during phosphate deficiency in Arabidopsis. New Phytol, 2013, 198(3):709-720
CrossRef Google scholar
[16]
ChenCY, WuK, SchmidtW. The histone deacetylase HDA19 controls root cell elongation and modulates a subset of phosphate starvation responses in Arabidopsis. Sci Rep, 2015, 5(1):15708
CrossRef Google scholar
[17]
ChiouT-J, LinS-I. Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol, 2011, 62: 185-206
CrossRef Google scholar
[18]
ConradM, SchothorstJ, KankipatiHN, Van ZeebroeckG, Rubio-TexeiraM, TheveleinJM. Nutrient sensing and signaling in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev, 2014, 38: 254-299
CrossRef Google scholar
[19]
DebS, SankaranarayananS, WewalaG, WiddupE, SamuelMA. The S-Domain Receptor Kinase Arabidopsis Receptor Kinase2 and the U Box/Armadillo Repeat-Containing E3 Ubiquitin Ligase9 module mediates lateral root development under phosphate starvation in Arabidopsis. Plant Physiol, 2014, 165: 1647-1656
CrossRef Google scholar
[20]
Desai M, Rangarajan P, Donahue JL, et al (2014) Two inositol hexakisphosphate kinases drive inositol pyrophosphate synthesis in plants. Plant Journal 80:642–653. https://doi.org/10.1111/tpj.12669
[21]
DesfougèresY, GerasimaitëRU, JessenHJ, MayerA. Vtc5, a novel subunit of the vacuolar transporter chaperone complex, regulates polyphosphate synthesis and phosphate homeostasis in yeast. J Biol Chem., 2016, 291: 22262-22275
CrossRef Google scholar
[22]
DesfougèresY, WilsonMS, LahaD, MillerGJ, SaiardiA. ITPK1 mediates the lipid-independent synthesis of inositol phosphates controlled by metabolism. Proc Natl Acad Sci, 2019, 116(49):24551-24561
CrossRef Google scholar
[23]
DesmariniD, LevS, FurkertD, CrossettB, SaiardiA, Kaufman-FrancisK, LiC, SorrellTC, Wilkinson-WhiteL, MatthewsJ, FiedlerD, DjordjevicJT. IP(7)-SPX domain interaction controls fungal virulence by stabilizing phosphate signaling machinery. mBio, 2020, 11(5):e01920
CrossRef Google scholar
[24]
DevaiahBN, MadhuvanthiR, KarthikeyanAS, RaghothamaKG. Phosphate starvation responses and gibberellic acid biosynthesis are regulated by the MYB62 transcription factor in Arabidopsis. Mol Plant, 2009, 2(1):43-58
CrossRef Google scholar
[25]
do NascimentoC, PagliariP, SchmittD, et al.. Phosphorus concentrations in sequentially fractionated soil samples as affected by digestion methods. Sci Rep, 2015, 5: 17967
CrossRef Google scholar
[26]
DollinsDE, BaiW, FridyPC, OttoJC, NeubauerJL, GattisSG, MehtaKPM, YorkJD. Vip1 is a kinase and pyrophosphatase switch that regulates inositol diphosphate signaling. Proc Natl Acad Sci U S A, 2020, 117: 9356-9364
CrossRef Google scholar
[27]
DongJ, MaG, SuiL, WeiM, SatheeshV, ZhangR, GeS, LiJ, ZhangT-E, WittwerC, JessenHJ, ZhangH, AnGY, ChaoDY, LiuD, LeiM. Inositol pyrophosphate InsP8 acts as an intracellular phosphate signal in Arabidopsis. Mol Plant, 2019, 12(11):1463-1473
CrossRef Google scholar
[28]
DuY, ScheresB. Lateral root formation and the multiple roles of auxin. J Exp Bot, 2018, 69(2):155-167
CrossRef Google scholar
[29]
DuanK, YiK, DangL, HuangH, WuW, WuP. Characterization of a sub-family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation. Plant J, 2008, 54(6):965-975
CrossRef Google scholar
[30]
FooE, TurnbullCG, BeveridgeCA. Long-distance signaling and the control of branching in the rms1 mutant of pea. Plant Physiol, 2001, 126: 203-209
CrossRef Google scholar
[31]
Franco-ZorrillaJM, MartinAC, SolanoR, RubioV, LeyvaA, Paz-AresJ. Mutations at CRE1 impair cytokinin-induced repression ofphosphate starvation responses in Arabidopsis. Plant J, 2002, 32: 353-360
CrossRef Google scholar
[32]
FreedC, AdepojuO, GillaspyG. Can inositol pyrophosphates inform strategies for developing low phytate crops?. Plants, 2020, 9: 115
CrossRef Google scholar
[33]
FurkertD, HostachyS, Nadler-HollyM, FiedlerD. Triplexed affinity reagents to sample the mammalian inositol pyrophosphate interactome. Cell Chem Biol, 2020, 27: 1097-1108
CrossRef Google scholar
[34]
Funkhouser EA, Loewus FA (1975) Purification of myo-Inositol 1-Phosphate Synthase from rice cell culture by affinity chromatography. Plant Physiol 56:786–90. https://doi.org/10.1104/pp.56.6.786
[35]
GaoY-Q, BuL-H, HanM-L, WangY-L, LiZ-Y, LiuH-T, ChaoD-Y. Long-distance blue light signalling regulates phosphate deficiency-induced primary root growth inhibition. Mol Plant, 2021, 14(9):1539-1553
CrossRef Google scholar
[36]
GerasimaiteR, PavlovicI, CapolicchioS, HoferA, SchmidtA, JessenHJ, MayerA. Inositol pyrophosphate specificity of the SPX-dependent polyphosphate polymerase VTC. ACS Chem Biol, 2017, 12: 648-653
CrossRef Google scholar
[37]
GiotsF, DonatonMCV, TheveleinJM. Inorganic phosphate is sensed by specific phosphate carriers and acts in concert with glucose as a nutrient signal for activation of the protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol Microbiol, 2003, 47: 1163-1181
CrossRef Google scholar
[38]
GiriJ, BhosaleR, HuangG, PandeyBK, ParkerH, ZappalaS, YangJ, DievartA, BureauC, LjungK, PriceA, RoseT, LarrieuA, MairhoferS, SturrockCJ, WhiteP, DupuyL, HawkesfordM, PerinC, LiangW, PeretB, HodgmanCT, LynchJ, WissuwaM, ZhangD, PridmoreT, MooneySJ, GuiderdoniE, SwarupR, BennettMJ. The rice auxin influx carrier OsAUX1 is required to facilitate root hair elongation in response to low external phosphate. Nat Commun, 2018, 9(1):1408
CrossRef Google scholar
[39]
GodonC, MercierC, WangX, DavidP, RichaudP, NussaumeL, LiuD, DesnosT. Under phosphate starvation conditions, Fe and Al trigger accumulation of the transcription factor STOP1 in the nucleus of Arabidopsis root cells. Plant J, 2019, 99(5):937-949
CrossRef Google scholar
[40]
GokhaleNA, ZarembaA, ShearsSB. Receptor-dependent compartmentalization of PPIP5K1, a kinase with a cryptic polyphosphoinositide binding domain. Biochem J, 2011, 434: 415-426
CrossRef Google scholar
[41]
GuC, NguyenHN, GaniniD, ChenZ, JessenHJ, GuZ, WangH, ShearsSB. KO of 5-InsP7 kinase activity transforms the HCT116 colon cancer cell line into a hypermetabolic, growth-inhibited phenotype. Proc Natl Acad Sci U S A, 2017, 2017(114):11968-11973
CrossRef Google scholar
[42]
GuC, NguyenH-N, HoferA, JessenHJ, DaiXWH, et al.. The significance of the bifunctional kinase/phosphatase activities of PPIP5Ks for coupling inositol pyrophosphate cell-signaling to cellular phosphate homeostasis. J Biol Chem, 2017, 292(11):4544-4555
CrossRef Google scholar
[43]
GuC, WilsonMSC, JessenHJ, SaiardiA, ShearsSB. Inositol pyrophosphate profiling of two HCT116 cell lines uncovers variation in InsP8 levels. PLoS One, 2016, 11(10):e0165286
CrossRef Google scholar
[44]
Gutierrez-AlanisD, Yong-VillalobosL, Jimenez-SandovalP, Alatorre-CobosF, Oropeza-AburtoA, Mora-MaciasJ, Sanchez-RodriguezF, Cruz-RamirezA, Herrera-EstrellaL. Phosphate starvation-dependent iron mobilization induces CLE14 expression to trigger root meristem differentiation through CLV2/PEPR2 signaling. Dev Cell, 2017, 41: 555-570.e3
CrossRef Google scholar
[45]
HamBK, LucasWJ. Phloem-mobile RNAs as systemic signaling agents. Annu Rev Plant Biol, 2017, 68: 173-195
CrossRef Google scholar
[46]
HatchAJ, YorkJD. SnapShot: inositol phosphates. Cell, 2010, 143(6):1030-1030.e1
CrossRef Google scholar
[47]
HolfordICR. Soil phosphorus: its measurement, and its uptake by plants. Aust J Soil Res, 1997, 35: 227-239
CrossRef Google scholar
[48]
HothornM, NeumannH, LenherrED, WehnerM, RybinV, HassaPO, UttenweilerA, ReinhardtM, SchmidtA, SeilerJ, LadurnerAG, HerrmannC, ScheffzekK, MayerA. Catalytic core of a membrane-associated eukaryotic polyphosphate polymerase. Science, 2009, 324(5926):513-516
CrossRef Google scholar
[49]
HuangKL, MaGJ, ZhangML, XiongH, WuH, ZhaoCZ, LiuCS, JiaHX, ChenL, RenF. The ARF7 and ARF19 transcription factors positively regulate PHOSPHATE STARVATION RESPONSE1 in Arabidopsis roots. Plant Physiol, 2018, 178: 413-427
CrossRef Google scholar
[50]
HuangS, JefferyDA, AnthonyMD, O’SheaEK. Functional analysis of the cyclin-dependent kinase inhibitor Pho85p protein kinase, in the transduction pathway of pi signals in Saccharomyces cerevisiae. Mol Cell Biol, 2001, 15: 997-1004
[51]
JiaH, ZhangS, WangL, YangY, ZhangH, CuiH, ShaoH, XuG. OsPht1;8, a phosphate transporter, is involved in auxin and phosphate starvation response in rice. J Exp Bot, 2017, 68(18):5057-5068
CrossRef Google scholar
[52]
JiangC, GaoX, LiaoL, HarberdNP, FuX. Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin–DELLA signaling pathway in Arabidopsis. Plant Physiol, 2007, 145: 1460-1470
CrossRef Google scholar
[53]
KaffmanA, HerskowitzI, TjianR, O’SheaEK. Phosphorylation of the transcription factor PHO4 by a cyclin-CDK complex, PHO80-PHO85. Science, 1994, 263: 1153-1156
CrossRef Google scholar
[54]
KapulnikY, DelauxPM, ResnickN, Mayzlish-GatiE, WiningerS, BhattacharyaC, Séjalon-DelmasN, CombierJP, BécardG, BelausovE, BeeckmanT, DorE, HershenhornJ, KoltaiH. Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta, 2011, 233(1):209-216
CrossRef Google scholar
[55]
Kim S-I, Tai TH (2011) Identification of genes necessary for wild-type levels of seed phytic acid in Arabidopsis thaliana using a reverse genetics approach. Mol Genet Genomics 286(2):119–133
[56]
KochianLV, HoekengaOA, PineroMA. How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorus efficiency. Annu Rev Plant Biol, 2004, 55(1):459-493
CrossRef Google scholar
[57]
KuiperD, SteingrÖVerE. McMichaelBL, PerssonH. Responses of growth, shoot to root ratio and Cytokinin concentrations in root tissue of two barley varieties, differing if their salt resistance. Developments in agricultural and managed forest ecology, 1991 NY, USA Elsevier 463-471
[58]
KuoHF, ChangTY, ChiangSF, WangWD, CharngYY, ChiouTJ. Arabidopsis inositol pentakisphosphate 2-kinase, AtIPK1, is required for growth and modulates phosphate homeostasis at the transcriptional level. Plant J, 2014, 80: 503-515
CrossRef Google scholar
[59]
KuoHF, HsuYY, LinWC, ChenKY, MunnikT, BrearleyCA, ChiouTJ. Arabidopsis inositol phosphate kinases IPK1 and ITPK1 constitute a metabolic pathway in maintaining phosphate homeostasis. Plant J, 2018, 95: 613-630
CrossRef Google scholar
[60]
LahaD, JohnenP, AzevedoC, DynowskiM, WeissM, CapolicchioS, MaoH, IvenT, SteenbergenM, FreyerM, et al.. VIH2 regulates the synthesis of inositol pyrophosphate InsP8 and jasmonate-dependent defenses in Arabidopsis. Plant Cell, 2015, 27: 1082-1097
CrossRef Google scholar
[61]
LahaD, ParvinN, HoferA, GiehlRF, Fernandez-RebolloN, von Wire’nN, SaiardiA, JessenHJ, SchaafG. Arabidopsis ITPK1 and ITPK2 have an evolutionarily conserved phytic acid kinase activity. ACS Chem Biol, 2019, 14: 2127-2133
CrossRef Google scholar
[62]
LeeB, ParkSJ, HongS, KimK, KimS. Inositol polyphosphate multikinase signaling: multifaceted functions in health and disease. Mol Cells, 2021, 44: 187
CrossRef Google scholar
[63]
LeeS, KimMG, AhnH, KimS. Inositol pyrophosphates: signaling molecules with pleiotropic actions in mammals. Molecules, 2020, 25(9):2208
CrossRef Google scholar
[64]
LeeY-S, HuangK, QuiochoFA, O’SheaEK. Molecular basis of cyclin-CDK-CKI regulation by reversible binding of an inositol pyrophosphate. Nat Chem Biol, 2008, 4(1):25-32
CrossRef Google scholar
[65]
LeeY-S, MuluguS, YorkJD, O’SheaEK. Regulation of a cyclin-CDK-CDK inhibitor complex by inositol pyrophosphates. Science, 2007, 316: 109-112
CrossRef Google scholar
[66]
LeiM, ZhuC, LiuY, KarthikeyanAS, BressanRA, RaghothamaKG, et al.. Ethylene signalling is involved in regulation of phosphate starvation-induced gene expression and production of acid phosphatases and anthocyanin in Arabidopsis. New Phytol, 2011, 189: 1084-1095
CrossRef Google scholar
[67]
LevyS, KafriM, CarmiM, BarkaiN. The competitive advantage of a dual-transporter system. Science, 2011, 334: 1408-1412
CrossRef Google scholar
[68]
LiX, GuC, HostachyS, SahuS, WittwerC, JessenHJ, ShearsSB. Control of XPR1-dependent cellular phosphate efflux by InsP8 is an exemplar for functionally-exclusive inositol pyrophosphate signaling. Proc Natl Acad Sci, 2020, 117(7):3568-3574
CrossRef Google scholar
[69]
LiuD. Root developmental responses to phosphorus nutrition. J Int Plant Biol, 2021, 63(6):1065-1090
CrossRef Google scholar
[70]
LiuF, WangZ, RenH, et al.. OsSPX1 suppresses the function of OsPHR2 in the regulation of expression of OsPT2 and phosphate homeostasis in shoots of rice. Plant J, 2010, 62: 508-517
CrossRef Google scholar
[71]
LiuN, ShangW, LiC, JiaL, WangX, XingG, ZhengW. Evolution of the SPX gene family in plants and its role in the response mechanism to phosphorus stress. Open Biol, 2018, 8(1):170231
CrossRef Google scholar
[72]
LiuY, XieY, WangH, MaX, YaoW, WangH. Light and ethylene coordinately regulate the phosphate starvation response through transcriptional regulation of PHOSPHATE STARVATION RESPONSE1. Plant Cell, 2017, 29(9):2269-2284
CrossRef Google scholar
[73]
LoewusFA, MurthyPP. Myo-inositol metabolism in plants. Plant Sci, 2000, 150(1):1-19
CrossRef Google scholar
[74]
LonettiA, SzijgyartoZ, BoschD, LossO, AzevedoC, SaiardiA. Identification of an evolutionarily conserved family of inorganic polyphosphate endopolyphosphatases. J Biol Chem, 2011, 286(37):31966-31974
CrossRef Google scholar
[75]
López-ArredondoDL, Leyva-GonzálezMA, González-MoralesSI, López-BucioJ, Herrera-EstrellaL. Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol, 2014, 65: 95-123
CrossRef Google scholar
[76]
Lopez-BucioJ, Hernandez-AbreuE, Sanchez-CalderonL, Nieto-JacoboM, SimpsonJ, Herrera-EstrellaL. Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol, 2002, 129: 244-256
CrossRef Google scholar
[77]
Lopez-ObandoM, LigerotY, BonhommeS, BoyerFD, RameauC. Strigolactone biosynthesis and signaling in plant development. Development, 2015, 142: 3615-3619
CrossRef Google scholar
[78]
Lorenzo-Orts L, Couto D, Hothorn M (2020) Identity and functions of inorganic and inositol polyphosphates in plants. New Phytol 225:637–652. https://doi.org/10.1111/nph.16129
[79]
LuM, ChengZ, ZhangX-M, et al.. Spatial divergence of PHR-PHT1 modules maintains phosphorus homeostasis in soybean nodules. Plant Physiol, 2020, 184: 236-250
CrossRef Google scholar
[80]
LvQ, ZhongY, WangY, WangZ, ZhangL, ShiJ, WuZ, LiuY, MaoC, YiK, WuP. SPX4 negatively regulates phosphate signaling and homeostasis through its interaction with PHR2 in Rice. Plant Cell, 2014, 26(4):1586-1597
CrossRef Google scholar
[81]
MaZ, BaskinTI, BrownKM, LynchJP. Regulation of root elongation under phosphorus stress involves changes in ethylene responsiveness. Plant Physiol, 2003, 131: 1381-1390
CrossRef Google scholar
[82]
MachkalyanG, TrieuP, PétrinD, HébertTE. Miller GJ PPIP5K1 interacts with the exocyst complex through a C-terminal intrinsically disordered domain and regulates cell motility. Cell Signal, 2016, 28: 401-411
CrossRef Google scholar
[83]
MagbanuaJP, FujisawaK, OgawaN, OshimaY. The homeodomain protein Pho2p binds at an A/T-rich segment flanking the binding site of the basic-helix-loop-helix protein Pho4p in the yeast PHO promoters. Yeast, 1997, 13: 1299-1308
CrossRef Google scholar
[84]
MagbanuaJP, OgawaN, HarashimaS, OshimaY. The transcriptional activators of the PHO regulon, Pho4p and Pho2p, interact directly with each other and with components of the basal transcription machinery in Saccharomyces cerevisiae. J Biochem, 1997, 121: 1182-1189
CrossRef Google scholar
[85]
MailerRK, AllendeM, HeestermansM, SchweizerM, DeppermannC, FryeM, PulaG, OdebergJ, GelderblomM, Rose-JohnS, SickmannA, BlankenbergS, HuberTB, KubischC, MaasC, GambaryanS, FirsovD, StavrouEX, ButlerLM, RennéT. Xenotropic and polytropic retrovirus receptor 1 regulates procoagulant platelet polyphosphate. Blood, 2021, 137(10):1392-1405
CrossRef Google scholar
[86]
MarschnerP. Marschner’s mineral nutrition of higher plants, 2012 3 Cambridge Academic Press 649
[87]
MartinAC, del PozoJC, IglesiasJ, RubioV, SolanoR, de La PenaA, et al.. Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J, 2000, 24: 559-567
CrossRef Google scholar
[88]
Mora-MacíasJ, Ojeda-RiveraJO, Gutiérrez-AlanísD, Yong-VillalobosL, Oropeza-AburtoA, Raya-GonzálezJ, Jiménez-DomínguezG, Chávez-CalvilloG, Rellán-ÁlvarezR, Herrera-EstrellaL. Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate. Proc Natl Acad Sci, 2017, 114: E3563-E3572
CrossRef Google scholar
[89]
MorcuendeR, BariR, GibonY, ZhengW, PantBD, BläsingO, UsadelB, CzechowskiT, UdvardiMK, StittM, ScheibleWR. Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ, 2007, 30: 85-112
CrossRef Google scholar
[90]
MoritohY, AbeSI, AkiyamaH, KobayashiA, KoyamaR, HaraR, KasaiS, WatanabeM. The enzymatic activity of inositol hexakisphosphate kinase controls circulating phosphate in mammals. Nat Commun, 2021, 12(1):4847
CrossRef Google scholar
[91]
MouillonJ-M, PerssonBL. New aspects on phosphate sensing and signalling in Saccharomyces cerevisiae. FEMS Yeast Res, 2006, 6: 171-176
CrossRef Google scholar
[92]
MüllerJ, ToevT, HeistersM, TellerJ, MooreKL, HauseG, DineshDC, BürstenbinderK, AbelS. Iron-dependent Callose deposition adjusts root meristem maintenance to phosphate availability. Dev Cell, 2015, 33: 216-230
CrossRef Google scholar
[93]
NacryP, CanivencG, MullerB, et al.. A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiol, 2005, 138: 2061-2074
CrossRef Google scholar
[94]
NariseT, KobayashiK, BabaS, ShimojimaM, MasudaS, FukakiH, et al.. Involvement of auxin signaling mediated by IAA14 and ARF7/19 in membrane lipid remodeling during phosphate starvation. Plant Mol Biol, 2010, 72: 533-544
CrossRef Google scholar
[95]
O’NeillEM, KaffmanA, JollyER, O’SheaEK. Regulation of PHO4 nuclear localization by the PHO80–PHO85 cyclin-CDK complex. Science, 1996, 271(5246):209-212
CrossRef Google scholar
[96]
OgawaN, NoguchiK, SawaiH, YamashitaY, YompakudeeC, OshimaY. Functional domains of Pho81p, an inhibitor of the Pho85p protein kinase, in the transduction pathway for pi signals in Saccharomyces cerevisiae. Mol Cell Biol, 1995, 15: 997-1004
CrossRef Google scholar
[97]
OkushimaY, OvervoordePJ, ArimaK, AlonsoJM, ChanA, ChangC, EckerJR, HughesB, LuiA, NguyenD, OnoderaC, QuachH, SmithA, YuG, TheologisA. Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell, 2005, 17: 444-463
CrossRef Google scholar
[98]
OsorioMB, NgS, BerkowitzO, et al.. SPX4 acts on PHR1-dependent and -independent regulation of shoot phosphorus status in Arabidopsis. Plant Physiol, 2019, 181: 332-352
CrossRef Google scholar
[99]
PandeyBK, VermaL, PrustyA, SinghAP, BennettMJ, TyagiAK, GiriJ, MehraP. OsJAZ11 regulates phosphate starvation responses in rice. Planta, 2021, 254: 8
CrossRef Google scholar
[100]
ParkBS, SeoJS, ChuaNH. Nitrogen limitation adaptation recruits phosphate2 to target the phosphate transporter pt2 for degradation during the regulation of Arabidopsis phosphate homeostasis. Plant Cell, 2014, 26(1):454-464
CrossRef Google scholar
[101]
ParkSJ, LeeS, ParkSE, KimS. Inositol pyrophosphates as multifaceted metabolites in the regulation of mammalian signaling networks. Animal Cells Syst, 2018, 22: 1-6
CrossRef Google scholar
[102]
Perez-TorresCA, Lopez-BucioJ, Cruz-RamirezA, Ibarra-LacletteE, DharmasiriS, EstelleM, Herrera-EstrellaL. Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell, 2008, 20: 3258-3272
CrossRef Google scholar
[103]
PugaMI, MateosI, CharukesiR, WangZ, Franco-ZorrillaJM, de LorenzoL, IrigoyenML, MasieroS, BustosW, RodríguezJ, LeyvaA, RubioV, SommerH, Paz-AresJ. SPX1 is a phosphate-dependent inhibitor of phosphate starvation response 1 in Arabidopsis. Proc Natl Acad Sci U S A, 2014, 111(41):14947-14952
CrossRef Google scholar
[104]
RaboyV. Seeds for a better future: “low phytate” grains help to overcome malnutrition and reduce pollution. Trends Plant Sci, 2001, 6: 458-462
CrossRef Google scholar
[105]
RiedMK, WildR, ZhuJ, PipercevicJ, SturmK, BrogerL, et al.. Inositol pyrophosphates promote the interaction of SPX domains with the coiled-coil motif of PHR transcription factors to regulate plant phosphate homeostasis. Nat Commun, 2021, 12: 384
CrossRef Google scholar
[106]
RiemerE, QiuD, LahaD, et al.. ITPK1 is an InsP6/ADP pohsphotransferase that controls phosphate signaling in Arabidopsis. Mol Plant, 2021, 14: 1864-1880
CrossRef Google scholar
[107]
RubioV, LinharesF, SolanoR, MartinAC, IglesiasJ, LeyvaA, et al.. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev, 2001, 15(16):2122-2133
CrossRef Google scholar
[108]
SabbaghY. Phosphate as a sensor and signaling molecule. Clin Nephrol, 2013, 79: 57-65
CrossRef Google scholar
[109]
SamynDR, Van der VekenJ, Van ZeebroeckG, PerssonBL, KarlssonBC. Key residues and phosphate release routes in the Saccharomyces cerevisiae Pho84 transceptor. J Biol Chem, 2016, 291(51):26388-26398
CrossRef Google scholar
[110]
SchneiderKR, SmithRL, O’SheaEK. Phosphate-regulated inactivation of the kinase PHO80–PHO85 by the CDK inhibitor PHO81. Science, 1994, 266: 122-126
CrossRef Google scholar
[111]
SeccoD, WangC, ArpatBA, WangZ, PoirierY, TyermanSD, WuP, ShouH, WhelanJ. The emerging importance of the SPX domain-containing proteins in phosphate homeostasis. New Phytol, 2012, 193(4):842-851
CrossRef Google scholar
[112]
SeccoD, WangC, ShouH, SchultzMD, ChiarenzaS, NussaumeL, EckerJR, WhelanJ, ListerR. Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. Elife, 2015, 4: e09343
CrossRef Google scholar
[113]
SeccoD, WhelanJ, RouachedH, ListerR. Nutrient stress-induced chromatin changes in plants. Curr Opin Plant Biotech, 2017, 39: 1-7
CrossRef Google scholar
[114]
SeguelA, CummingJ, Klugh-StewartK, CornejoP, BorieP. The role of arbuscular mycorrhizas in decreasing aluminium phytotoxicity in acidic soils: a review. Mycorrhiza., 2013, 23: 167-183
CrossRef Google scholar
[115]
SengottaiyanP, PetrlovaJ, LagerstedtJO, Ruiz-PavonL, BudamaguntaMS, VossJC, PerssonBL. Characterization of the biochemical and biophysical properties of the Saccharomyces cerevisiae phosphate transporter Pho89. Biochem Biophys Res Commun, 2011, 436: 551-556
CrossRef Google scholar
[116]
ShaoD, et al.. Interaction of Saccharomyces cerevisiae Pho2 with Pho4 increases the accessibility of the activation domain of Pho4. Mol Gen Genet, 1996, 251(3):358-364
[117]
Shears SB (2018) Intimate connections: Inositol pyrophosphates at the interface of metabolic regulation and cell signaling. J Cell Physiol 233:1897–1912. https://doi.org/10.1002/jcp.26017
[118]
ShenC, WangS, ZhangS, XuY, QianQ, QiY, et al.. OsARF16, a transcription factor, is required for auxin and phosphate starvation response in rice (Oryza sativaL.). Plant Cell Environ, 2013, 36: 607-620
CrossRef Google scholar
[119]
ShiJ, HuH, ZhangK, et al.. The paralogous SPX3 and SPX5 genes redundantly modulate pi homeostasis in rice. J Exp Bot, 2014, 65: 859-870
CrossRef Google scholar
[120]
ShiJ, WangH, HazebroekJ, ErtlDS, HarpT. The maize low-phytic acid 3 encodes a myo-inositol kinase that plays a role in phytic acid biosynthesis in developing seeds. Plant J, 2005, 42(5):708-719
CrossRef Google scholar
[121]
Silva-NavasJ, ConesaCM, SaezA, Navarro-NeilaS, Garcia-MinaJM, ZamarreñoAM, BaigorriR, SwarupR, del PozoJC. Role of cis-zeatin in root responses to phosphate starvation. New Phytol, 2019, 224(1):242-257
CrossRef Google scholar
[122]
SmithAP, JainA, DealRB, NagarajanVK, PolingMD, RaghothamaKG, MeagherRB. Histone H2A.Z regulates the expression of several classes of phosphate starvation response genes but not as a transcriptional activator. Plant Physiol, 2010, 152(1):217-225
CrossRef Google scholar
[123]
SongL, YuH, DongJ, CheX, JiaoY, LiuD. The molecular mechanism of ethylene-mediated root hair development induced by phosphate starvation. PLoS Genet, 2016, 12(7):e1006194
CrossRef Google scholar
[124]
SorefanK, BookerJ, HaurogneK, GoussotM, BainbridgeK, FooE, et al.. MAX4 and RMS1 are orthologous dioxygenase-like genesthat regulate shoot branching in Arabidopsis and pea. Genes Dev, 2003, 17: 1469-1474
CrossRef Google scholar
[125]
Stevenson-PaulikJ, OdomAR, YorkJD. Molecular and biochemical characterization of two plant inositol polyphosphate 6−/3−/5-kinases. J Biol Chem, 2002, 277: 42711-42718
CrossRef Google scholar
[126]
SvistoonoffS, CreffA, ReymondM, Sigoillot-ClaudeC, RicaudL, BlanchetA, NussaumeL, DesnosT. Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet, 2007, 39(6):792-796
CrossRef Google scholar
[127]
ThibaudMC, ArrighiJF, BayleV, ChiarenzaS, CreffA, BustosR, et al.. Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J, 2010, 64: 775-789
CrossRef Google scholar
[128]
TianWH, YeJY, CuiMQ, ChangJB, LiuY, LiGX, WuYR, XuJM, HarberdNP, MaoCZ, JinCW, DingZJ, ZhengSJ. A transcription factor STOP1-centered pathway coordinates ammonium and phosphate acquisition in Arabidopsis. Mol Plant, 2021, 14(9):1554-1568
CrossRef Google scholar
[129]
TicconiCA, LuceroRD, SakhonwaseeS, AdamsonAW, CreffA, NussaumeL, DesnosT, AbelS. ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc Natl Acad Sci U S A, 2009, 106: 14174-14179
CrossRef Google scholar
[130]
Toh-eA, TanakaK, UesonoY, WicknerRB. PHO85, a negative regulator of the PHO system, is a homolog of the protein kinase gene, CDC28, of Saccharomyces cerevisiae. Mol Gen Genet, 1988, 214: 162-164
CrossRef Google scholar
[131]
UmeharaM, HanadaA, YoshidaS, AkiyamaK, AriteT, Takeda-KamiyaN, et al.. Inhibition of shoot branching by new terpenoid plant hormones. Nature, 2008, 455: 195-200
CrossRef Google scholar
[132]
WangC, YueW, YingY, WangS, SeccoD, LiuY, WhelanJ, TyermanSD, ShouH. Rice SPX-major facility Superfamily3, a vacuolar phosphate efflux transporter, is involved in maintaining phosphate homeostasis in Rice. Plant Physiol, 2015, 169(4):2822-2831
[133]
WangH, DeroseEF, LondonRE, ShearsSB. IP6K structure and the molecular determinants of catalytic specificity in an inositol phosphate kinase family. Nat Commun, 2014, 5: 4178
CrossRef Google scholar
[134]
WangH, FalckJR, HallTMT, ShearsSB. Structural basis for an inositol pyrophosphate kinase surmounting phosphate crowding. Nat Chem Biol, 2012, 8: 111-116
CrossRef Google scholar
[135]
WangJ, SunJ, MiaoJ, et al.. A phosphate starvation response regulator ta-PHR1 is involved in phosphate signalling and increases grain yield in wheat. Ann Bot, 2013, 111: 1139-1153
CrossRef Google scholar
[136]
WangS, IchiiM, TaketaS, XuL, XiaK, ZhouX. Lateral root formation in rice (Oryza sativa): promotion effect of jasmonic acid. J Plant Physiol, 2002, 159(8):827-832
CrossRef Google scholar
[137]
WangS, ZhangS, SunC, XuY, ChenY, YuC, QianQ, JiangDA, QiYH. Auxin response factor (OsARF12), a novel regulator for phosphate homeostasis in rice (Oryza sativa). New Phytol, 2014, 201(1):91-103
CrossRef Google scholar
[138]
WangX, BaiJ, LiuH, SunY, ShiX, RenZ. Overexpression of a maize transcription factor ZmPHR1 improves shoot inorganic phosphate content and growth of Arabidopsis under low-phosphate conditions. Plant Mol Biol Rep, 2013, 31(3):665-677
CrossRef Google scholar
[139]
WangX, YiK, TaoY, WangF, WuZ, JiangD, et al.. Cytokinin represses phosphate-starvation response through increasing of intracellular phosphate level. Plant Cell Environ, 2006, 29(10):1924-1935
CrossRef Google scholar
[140]
WangZ, HuH, HuangH, DuanK, WuZ, WuP. Regulation of OsSPX1 and OsSPX3 on expression of OsSPX domain genes and pi-starvation signaling in rice. J Integr Plant Biol, 2009, 51: 663-674
CrossRef Google scholar
[141]
WangZ, KuoHF, ChiouTJ. Intracellular phosphate sensing and regulation of phosphate transport systems in plants. Plant Physiol, 2021, 187(4):2043-2055
CrossRef Google scholar
[142]
WangZ, RuanW, ShiJ, ZhangL, XiangD, YangC, et al.. RiceSPX1 and SPX2 inhibit phosphate starvation responses through inter-acting with PHR2 in a phosphate-dependent manner. Proc Natl Acad Sci U S A, 2014, 111: 14953-14958
CrossRef Google scholar
[143]
WildR, GerasimaiteR, JungJY, TruffaultV, PavlovicI, SchmidtA, SaiardiA, JessenHJ, PoirierY, HothornM, MayerA. Control of eukaryotic phosphate homeostasis by inositol polyphosphate sensor domains. Science, 2016, 352: 986-990
CrossRef Google scholar
[144]
WuP, ShouH, XuG, LianX. Improvement of phosphorus efficiency in rice on the basis of understanding phosphate signaling and homeostasis. Curr Opin Plant Biol, 2013, 16: 205-212
CrossRef Google scholar
[145]
WykoffDD, GrossmanAR, WeeksDP, et al.. Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. PNAS, 1999, 96: 15336-15341
CrossRef Google scholar
[146]
WykoffDD, RizviAH, RaserJM, MargolinB, O'SheaEK. Positive feedback regulates switching of phosphate transporters in S. cerevisiae. Mol Cell, 2007, 27: 1005-1013
CrossRef Google scholar
[147]
XuJM, WangZQ, WangJY, LiPF, JinJF, ChenWW, FanW, KochianLV, ZhengSJ, YangJL. Low phosphate represses histone deacetylase complex1 to regulate root system architecture remodeling in Arabidopsis. New Phytol, 2020, 225: 1732-1745
CrossRef Google scholar
[148]
XuL, JinL, LongL, LiuL, HeX, GaoW, ZhuL, ZhangX. Overexpression ofGbWRKY1 positively regulates the pi starvation response by alterationof auxin sensitivity in Arabidopsis. Plant Cell Rep, 2012, 31(12):2177-2188
CrossRef Google scholar
[149]
YoneyamaK, KisugiT, XieX, YoneyamaK. de BruijnFJ. Chemistry of strigolactones: why and how do plants produce so many strigolactones?. Molecular microbial ecology of the rhizosphere, 2013 Hoboken, NJ John Wiley & Sons, Inc.
[150]
Yong-VillalobosL, Gonzalez-MoralesSI, WrobelK, Gutierrez-AlanisD, Cervantes-PerezSA, Hayano-KanashiroC, Oropeza-AburtoA, Cruz-RamirezA, MartinezO, Herrera-EstrellaL. Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation. Proc Natl Acad Sci U S A, 2015, 112(52):E7293-EE730
CrossRef Google scholar
[151]
ZhangK, ZhouZ, LiJ, WangJ, YuL, LinS. SPX-related genes regulate phosphorus homeostasis in the marine phytoplankton, Phaeodactylum tricornutum. Commun Biol, 2021, 4(1):797
CrossRef Google scholar
[152]
ZhangYJ, LynchJP, BrownKM. Ethylene and phosphorus availability have interacting yet distinct effects on root hair development. J Exp Bot, 2003, 54: 2351-2361
CrossRef Google scholar
[153]
ZhangZL, ZhengY, HamBK, ChenJY, YoshidaA, KochianLV, FeiZJ, LucasWJ. Vascular-mediated signalling involved in early phosphate stress response in plants. Nat Plants, 2016, 2(4):16033
CrossRef Google scholar
[154]
ZhengZ, WangZ, WangX, LiuD. Blue light-triggered chemical reactions underlie phosphate deficiency-induced inhibition of root elongation of Arabidopsis seedlings grown in petri dishes. Mol Plant, 2019, 12(11):1515-1523
CrossRef Google scholar
[155]
ZhouJ, HuQ, XiaoX, YaoD, GeS, YeJ, LiH, CaiR, et al.. Mechanism of phosphate sensing and signaling revealed by rice SPX1-PHR2 complex structure. Nat Commun, 2021, 12(1):7040
CrossRef Google scholar
[156]
ZhouJ, JiaoFC, WuZ, et al.. OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol, 2008, 146: 1673-1686
CrossRef Google scholar
[157]
ZhouX, O’SheaEK. Integrated approaches reveal determinants of genome-wide binding and function of the transcription factor Pho4. Mol Cell, 2011, 42(6):826-836
CrossRef Google scholar
[158]
ZhuJ, LauK, PuschmannR, HarmelRK, ZhangY, PriesV, GauglerP, BrogerL, DuttaAK, JessenHJ, et al.. Two bifunctional inositol pyrophosphate kinases/phosphatases control plant phosphate homeostasis. ELife, 2019, 8: 1-25
CrossRef Google scholar
[159]
ZhuangQ, XueY, YaoZ, et al.. Phosphate starvation responsive GmSPX5 mediates nodule growth through interaction with GmNF-YC4 in soybean (Glycine max). Plant J, 2021, 108: 1422-1438
CrossRef Google scholar

Accesses

Citations

Detail

Sections
Recommended

/