Plant resilience to phosphate limitation: current knowledge and future challenges

References

• Heuer S, Gaxiola R, Schilling R, et al. Improving phosphorus use efficiency: a complex trait with emerging opportunities. Plant J. 2017;90(5):868–885.
   PubMed Web of Science ®Google Scholar
• Poirier Y, Bucher M. Phosphate transport and homeostasis in Arabidopsis. In: Somerville CR, Meyerowitz EM, editors. The Arabidopsis book. Rockville (MD): The American Society of Plant Biologists; 2002.
   Google Scholar
• Rouached H, Arpat AB, Poirier Y. Regulation of phosphate starvation responses in plants: signaling players and cross-talks. Mol Plant. 2010;3(2):288–299.
   PubMed Web of Science ®Google Scholar
• Bouain N, Krouk G, Lacombe B, et al. Getting to the root of plant mineral nutrition: combinatorial nutrient stresses reveal emergent properties. Trends Plant Sci. 2019;24(6):542–552.
   PubMed Web of Science ®Google Scholar
• Müller J, Toev T, Heisters M, et al. Iron-dependent callose deposition adjusts root meristem maintenance to phosphate availability. Dev Cell. 2015;33(2):216–230.
   PubMed Web of Science ®Google Scholar
• Bieleski RL. Phosphate pools, phosphate transport, and phosphate availability. Annu Rev Plant Physiol. 1973;24(1):225–252.
   Google Scholar
• Lu J, Gao X, Dong Z, et al. Improved phosphorus acquisition by tobacco through transgenic expression of mitochondrial malate dehydrogenase from Penicillium oxalicum. Plant Cell Rep. 2012;31(1):49–56.
   PubMed Web of Science ®Google Scholar
• Liang CY, Pineros MA, Tian J, et al. Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils. Plant Physiol. 2013;161(3):1347–1361.
   PubMed Web of Science ®Google Scholar
• Belgaroui N, Berthomieu P, Rouached H, et al. The secretion of the bacterial phytase PHY-US417 by Arabidopsis roots reveals its potential for increasing phosphate acquisition and biomass production during co-growth. Plant Biotechnol J. 2016;14(9):1914–1924.
   PubMed Web of Science ®Google Scholar
• Kisko M, Bouain N, Rouached A, et al. Molecular mechanisms of phosphate and zinc signalling crosstalk in plants: phosphate and zinc loading into root xylem in Arabidopsis. Environ Exp Bot. 2015;114:57–64.
   Web of Science ®Google Scholar
• Balzergue C, Dartevelle T, Godon C, et al. Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation. Nat Commun. 2017;8:15300.
   PubMed Web of Science ®Google Scholar
• Mora-Macias J, Ojeda-Rivera JO, Gutierrez-Alanis D, et al. Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate. Proc Natl Acad Sci USA. 2017;114:3563–3572.
   Web of Science ®Google Scholar
• Bournier M, Tissot N, Mari S, et al. Arabidopsis ferritin 1 (AtFer1) gene regulation by the phosphate starvation response 1 (AtPHR1) transcription factor reveals a direct molecular link between iron and phosphate homeostasis. J Biol Chem. 2013;288(31):22670–22680.
   PubMed Web of Science ®Google Scholar
• Bouain N, Korte A, Satbhai SB, et al. Systems genomics approaches provide new insights into Arabidopsis thaliana root growth regulation under combinatorial mineral nutrient limitation. PLoS Genet. 2019;15(11):e1008392.
   PubMed Web of Science ®Google Scholar
• Gutierrez-Alanis D, Yong-Villalobos L, Jimenez-Sandoval P, et al. Phosphate starvation-dependent iron mobilization induces CLE14 expression to trigger root meristem differentiation through CLV2/PEPR2 signaling. Dev Cell. 2017;41(5):555–570.
   PubMed Web of Science ®Google Scholar
• Zheng Z, Wang Z, Wang X, et al. 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.
   PubMed Web of Science ®Google Scholar
• Medici A, Marshall-Colon A, Ronzier E, et al. AtNIGT1/HRS1 integrates nitrate and phosphate signals at the Arabidopsis root tip. Nat Commun. 2015;6:6274.
   PubMed Web of Science ®Google Scholar
• Cui YN, Li XT, Yuan JZ, et al. Nitrate transporter NPF7.3/NRT1.5 plays an essential role in regulating phosphate deficiency responses in Arabidopsis. Biochem Biophys Res Commun. 2019;508(1):314–319.
   PubMed Web of Science ®Google Scholar
• Matthus E, Wilkins KA, Swarbreck SM, et al. Phosphate starvation alters abiotic-stress-induced cytosolic free calcium increases in roots. Plant Physiol. 2019;179(4):1754–1767.
   PubMed Web of Science ®Google Scholar
• Giovannetti M, Göschl C, Dietzen C, et al. Identification of novel genes involved in phosphate accumulation in Lotus japonicus through Genome Wide Association mapping of root system architecture and anion content. PLoS Genet. 2019;15(12):e1008126.
   PubMed Web of Science ®Google Scholar
• Sakuraba Y, Kanno S, Mabuchi A, et al. A phytochrome-B-mediated regulatory mechanism of phosphorus acquisition. Nat Plants. 2018;4(12):1089–1101.
   PubMed Web of Science ®Google Scholar
• Rouached H. Red light means on for phosphorus. Nat Plants. 2018;4(12):983–984.
   PubMed Web of Science ®Google Scholar
• Nussaume L, Kanno S, Javot H, et al. Phosphate import in plants: focus on the PHT1 transporters. Front Plant Sci. 2011;2:83.
   PubMed Web of Science ®Google Scholar
• Liao YY, Li JL, Pan RL, et al. Structure-function analysis reveals amino acid residues of arabidopsis phosphate transporter AtPHT1;1 crucial for its activity. Front Plant Sci. 2019;10:1158.
   PubMed Web of Science ®Google Scholar
• Kisko M, Bouain N, Safi A, et al. LPCAT1 controls phosphate homeostasis in a zinc-dependent manner. Elife. 2018;7:e32077.
   PubMed Web of Science ®Google Scholar
• Młodzińska E, Zboińska M. Phosphate uptake and allocation - a closer look at Arabidopsis thaliana L. and Oryza sativa L. Front Plant Sci. 2016;7:1198.
   PubMed Web of Science ®Google Scholar
• Fabiańska I, Bucher M, Häusler RE. Intracellular phosphate homeostasis - a short way from metabolism to signaling. Plant Sci. 2019;286:57–67.
   PubMed Web of Science ®Google Scholar
• Zhao LM, Versaw WK, Liu JY, et al. A phosphate transporter from Medicago truncatula is expressed in the photosynthetic tissues of the plant and located in the chloroplast envelop. New Phytol. 2003;157(2):291–302.
   PubMed Web of Science ®Google Scholar
• Versaw WK, Harrison MJ. A chloroplast phosphate transporter, PHT2;1, influences allocation of phosphate within the plant and phosphate-starvation responses. Plant Cell. 2002;14(8):1751–1766.
   PubMed Web of Science ®Google Scholar
• Pratt J, Boisson AM, Gout E, et al. Phosphate (Pi) starvation effect on the cytosolic Pi concentration and Pi exchanges across the tonoplast in plant cells: an in vivo 31P-nuclear magnetic resonance study using methylphosphonate as a Pi analog. Plant Physiol. 2009;151(3):1646–1657.
   PubMed Web of Science ®Google Scholar
• Zhu W, Miao Q, Sun D, et al. The mitochondrial phosphate transporters modulate plant responses to salt stress via affecting ATP and gibberellin metabolism in Arabidopsis thaliana. PLoS One. 2012;7(8):e43530.
   PubMed Web of Science ®Google Scholar
• Guo B, Jin Y, Wussler C, et al. Functional analysis of the Arabidopsis PHT4 family of intracellular phosphate transporters. New Phytol. 2008;177(4):889–898.
   PubMed Web of Science ®Google Scholar
• Liu J, Yang L, Luan M, et al. A vacuolar phosphate transporter essential for phosphate homeostasis in Arabidopsis. Proc Natl Acad Sci U S A. 2015;112(47):6571–6578.
   PubMed Web of Science ®Google Scholar
• Liu TY, Huang TK, Yang SY, et al. Identification of plant vacuolar transporters mediating phosphate storage. Nat Commun. 2016;7:11095.
   PubMed Web of Science ®Google Scholar
• Ding G, Lei GJ, Yamaji N, et al. Vascular cambium-localized AtSPDT mediates xylem-to-phloem transfer of phosphorus for its preferential distribution in Arabidopsis. Mol Plant. 2020;13(1):99–111.
   PubMed Web of Science ®Google Scholar
• Vogiatzaki E, Baroux C, Jung JY, et al. PHO1 exports phosphate from the chalazal seed coat to the embryo in developing arabidopsis seeds. Curr Biol. 2017;27(19):2893–2900.
   PubMed Web of Science ®Google Scholar
• Wissuwa M, Ae N. Genotypic variation for tolerance to phosphorus deficiency in rice and the potential for its exploitation in rice improvement. Plant Breed. 2001;120(1):43–48.
   Web of Science ®Google Scholar
• Gamuyao R, Chin JH, Pariasca-Tanaka J, et al. The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature. 2012;488(7412):535–539.
   PubMed Web of Science ®Google Scholar
• Yang SY, Lu WC, Ko SS, et al. Upstream open reading frame and phosphate-regulated expression of rice OsNLA1 controls phosphate transport and reproduction . Plant Physiol. 2020; 182(1):393–407.
   PubMed Web of Science ®Google Scholar
• Lin WY, Huang TK, Chiou TJ. Nitrogen limitation adaptation, a target of microRNA827, mediates degradation of plasma membrane-localized phosphate transporters to maintain phosphate homeostasis in Arabidopsis. Plant Cell. 2013;25(10):4061–4074.
   PubMed Web of Science ®Google Scholar
• Yue W, Ying Y, Wang C, et al. OsNLA1, a RING-type ubiquitin ligase, maintains phosphate homeostasis in Oryza sativa via degradation of phosphate transporters. Plant J. 2017;90(6):1040–1051.
   PubMed Web of Science ®Google Scholar
• Hu B, Jiang Z, Wang W, et al. al. Nitrate-NRT1.1B-SPX4 cascade integrates nitrogen and phosphorus signalling networks in plants. Nat Plants. 2019;5(4):401–413.
   PubMed Web of Science ®Google Scholar
• Puga MI, Mateos I, Charukesi R, et al. SPX1 is a phosphate-dependent inhibitor of PHOSPHATE STARVATION RESPONSE 1 in Arabidopsis. Proc Natl Acad Sci USA. 2014;111(41):14947–14952.
   PubMed Web of Science ®Google Scholar
• Wang Z, Ruan W, Shi J, et al. Rice SPX1 and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner. Proc Natl Acad Sci USA. 2014;111(41):14953–14958.
   PubMed Web of Science ®Google Scholar
• Wild R, Gerasimaite R, Jung JY, et al. Control of eukaryotic phosphate homeostasis by inositol polyphosphate sensor domains. Science. 2016;352(6288):986–990.
   PubMed Web of Science ®Google Scholar
• Briat JF, Rouached H, Tissot N, et al. Integration of P, S, Fe, and Zn nutrition signals in Arabidopsis thaliana: potential involvement of PHOSPHATE STARVATION RESPONSE 1 (PHR1). Front Plant Sci. 2015;6:290.
   PubMed Web of Science ®Google Scholar
• Rubio V, Linhares F, Solano R, 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.
   PubMed Web of Science ®Google Scholar
• Aung K, Lin SI, Wu CC, et al. Pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol. 2006;141(3):1000–1011.
   PubMed Web of Science ®Google Scholar
• Bari R, Datt Pant B, Stitt M, et al. PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 2006;141(3):988–999.
   PubMed Web of Science ®Google Scholar
• Ajmera I, Shi J, Giri J, et al. Regulatory feedback response mechanisms to phosphate starvation in rice. NPJ Syst Biol Appl. 2018;4:4.
   PubMed Web of Science ®Google Scholar
• Rouached H, Stefanovic A, Secco D, et al. Uncoupling phosphate deficiency from its major effects on growth and transcriptome via PHO1 expression in Arabidopsis. Plant J. 2011;65(4):557–570.
   PubMed Web of Science ®Google Scholar
• Medici A, Szponarski W, Dangeville P, et al. Identification of molecular integrators shows that nitrogen actively controls the phosphate starvation response in plants. Plant Cell. 2019;31(5):1171–1184.
   PubMed Web of Science ®Google Scholar
• Rouached H, Rhee SY. System-level understanding of plant mineral nutrition in the big data era. Curr Opin Syst Biol. 2017;4:71–77.
   Google Scholar
• Finkel OM, Salas-González I, Castrillo G, et al. The effects of soil phosphorous content on microbiota are driven by the plant phosphate starvation response. BioRxiv. 2019;608133.
   Google Scholar
• Castrillo G, Teixeira PJPL, Paredes SH, et al. Root microbiota drive direct integration of phosphate stress and immunity. Nature. 2017;543(7646):513–518.
   PubMed Web of Science ®Google Scholar