Plants feature remarkable developmental plasticity, enabling them to respond to and cope with environmental cues, such as limited availability of phosphate, an essential macronutrient for all organisms. Under this condition, Arabidopsis (Arabidopsis thaliana) roots undergo striking morphological changes, including exhaustion of the primary meristem, impaired unidirectional cell expansion, and elevated density of lateral roots, resulting in shallow root architecture. Here, we show that the activity of two homologous brassinosteroid (BR) transcriptional effectors, BRASSINAZOLE RESISTANT1 (BZR1) and BRASSINOSTEROID INSENSITIVE1-ETHYL METHANESULFONATE-SUPPRESSOR1 (BES1)/BZR2, blocks these responses, consequently maintaining normal root development under low phosphate conditions without impacting phosphate homeostasis. We show that phosphate deprivation shifts the intracellular localization of BES1/BZR2 to yield a lower nucleus-to-cytoplasm ratio, whereas replenishing the phosphate supply reverses this ratio within hours. Phosphate deprivation reduces the expression levels of BR biosynthesis genes and the accumulation of the bioactive BR 28-norcastasterone. In agreement, low and high BR levels sensitize and desensitize root response to this adverse condition, respectively. Hence, we propose that the environmentally controlled developmental switch from deep to shallow root architecture involves reductions in BZR1 and BES1/BZR2 levels in the nucleus, which likely play key roles in plant adaptation to phosphate-deficient environments.

Faculty of Biology Technion Israel Institute of Technology Haifa 3200003 Israel

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Abel S. (2011) Phosphate sensing in root development. Curr Opin Plant Biol 14: 303–309 PubMed

Bai MY, Shang JX, Oh E, Fan M, Bai Y, Zentella R, Sun TP, Wang ZY. (2012) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14: 810–817 PubMed PMC

Chiou TJ, Lin SI. (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62: 185–206 PubMed

Clouse SD. (2011) Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell 23: 1219–1230 PubMed PMC

de Lucas M, Davière JM, Rodríguez-Falcón M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blázquez MA, Titarenko E, Prat S. (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451: 480–484 PubMed

Devaiah BN, Nagarajan VK, Raghothama KG. (2007) Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiol 145: 147–159 PubMed PMC

Fridman Y, Elkouby L, Holland N, Vragović K, Elbaum R, Savaldi-Goldstein S. (2014) Root growth is modulated by differential hormonal sensitivity in neighboring cells. Genes Dev 28: 912–920 PubMed PMC

Fridman Y, Savaldi-Goldstein S. (2013) Brassinosteroids in growth control: how, when and where. Plant Sci 209: 24–31 PubMed

Gallego-Bartolomé J, Minguet EG, Grau-Enguix F, Abbas M, Locascio A, Thomas SG, Alabadí D, Blázquez MA. (2012) Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proc Natl Acad Sci USA 109: 13446–13451 PubMed PMC

González-García MP, Vilarrasa-Blasi J, Zhiponova M, Divol F, Mora-García S, Russinova E, Caño-Delgado AI. (2011) Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development 138: 849–859 PubMed

Hacham Y, Holland N, Butterfield C, Ubeda-Tomas S, Bennett MJ, Chory J, Savaldi-Goldstein S. (2011) Brassinosteroid perception in the epidermis controls root meristem size. Development 138: 839–848 PubMed PMC

He JX, Gendron JM, Sun Y, Gampala SS, Gendron N, Sun CQ, Wang ZY. (2005) BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307: 1634–1638 PubMed PMC

Hothorn M, Belkhadir Y, Dreux M, Dabi T, Noel JP, Wilson IA, Chory J. (2011) Structural basis of steroid hormone perception by the receptor kinase BRI1. Nature 474: 467–471 PubMed PMC

Jiang C, Gao X, Liao L, Harberd NP, Fu X. (2007) Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiol 145: 1460–1470 PubMed PMC

Joo SH, Kim TW, Son SH, Lee WS, Yokota T, Kim SK. (2012) Biosynthesis of a cholesterol-derived brassinosteroid, 28-norcastasterone, in Arabidopsis thaliana. J Exp Bot 63: 1823–1833 PubMed PMC

Kim J, Yi H, Choi G, Shin B, Song PS, Choi G. (2003) Functional characterization of phytochrome interacting factor 3 in phytochrome-mediated light signal transduction. Plant Cell 15: 2399–2407 PubMed PMC

Kinoshita T, Caño-Delgado A, Seto H, Hiranuma S, Fujioka S, Yoshida S, Chory J. (2005) Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433: 167–171 PubMed

Li QF, Wang C, Jiang L, Li S, Sun SS, He JX. (2012) An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and gibberellins in Arabidopsis. Sci Signal 5: ra72. PubMed

López-Arredondo DL, Leyva-González MA, González-Morales SI, López-Bucio J, Herrera-Estrella L. (2014) Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65: 95–123 PubMed

López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L. (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129: 244–256 PubMed PMC

Niu YF, Chai RS, Jin GL, Wang H, Tang CX, Zhang YS. (2013) Responses of root architecture development to low phosphorus availability: a review. Ann Bot (Lond) 112: 391–408 PubMed PMC

Oh E, Zhu JY, Wang ZY. (2012) Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat Cell Biol 14: 802–809 PubMed PMC

Péret B, Clément M, Nussaume L, Desnos T. (2011) Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci 16: 442–450 PubMed

Rouached H, Stefanovic A, Secco D, Bulak Arpat A, Gout E, Bligny R, Poirier Y. (2011) Uncoupling phosphate deficiency from its major effects on growth and transcriptome via PHO1 expression in Arabidopsis. Plant J 65: 557–570 PubMed

Sánchez-Calderón L, López-Bucio J, Chacón-López A, Cruz-Ramírez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L. (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46: 174–184 PubMed

She J, Han Z, Kim TW, Wang J, Cheng W, Chang J, Shi S, Wang J, Yang M, Wang ZY, et al. (2011) Structural insight into brassinosteroid perception by BRI1. Nature 474: 472–476 PubMed PMC

Sun Y, Fan XY, Cao DM, Tang W, He K, Zhu JY, He JX, Bai MY, Zhu S, Oh E, et al. (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell 19: 765–777 PubMed PMC

Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, Blanchet A, Nussaume L, Desnos T. (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39: 792–796 PubMed

Tang W, Yuan M, Wang R, Yang Y, Wang C, Oses-Prieto JA, Kim TW, Zhou HW, Deng Z, Gampala SS, et al. (2011) PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nat Cell Biol 13: 124–131 PubMed PMC

Thibaud MC, Arrighi JF, Bayle V, Chiarenza S, Creff A, Bustos R, Paz-Ares J, Poirier Y, Nussaume L. (2010) Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J 64: 775–789 PubMed

Ticconi CA, Delatorre CA, Lahner B, Salt DE, Abel S. (2004) Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J 37: 801–814 PubMed

Ticconi CA, Lucero RD, Sakhonwasee S, Adamson AW, Creff A, Nussaume L, Desnos T, Abel S. (2009) ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc Natl Acad Sci USA 106: 14174–14179 PubMed PMC

Tomscha JL, Trull MC, Deikman J, Lynch JP, Guiltinan MJ. (2004) Phosphatase under-producer mutants have altered phosphorus relations. Plant Physiol 135: 334–345 PubMed PMC

Vance CP, Uhde-Stone C, Allan DL. (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157: 423–447 PubMed

Wang ZY, Nakano T, Gendron J, He J, Chen M, Vafeados D, Yang Y, Fujioka S, Yoshida S, Asami T, et al. (2002) Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev Cell 2: 505–513 PubMed

Wang ZY, Seto H, Fujioka S, Yoshida S, Chory J. (2001) BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410: 380–383 PubMed

Yin Y, Vafeados D, Tao Y, Yoshida S, Asami T, Chory J. (2005) A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell 120: 249–259 PubMed

Yin Y, Wang ZY, Mora-Garcia S, Li J, Yoshida S, Asami T, Chory J. (2002) BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109: 181–191 PubMed

Yokota T, Sato T, Takeuchi Y, Nomura T, Uno K, Watanabe T, Takatsuto S. (2001) Roots and shoots of tomato produce 6-deoxo-28-norcathasterone, 6-deoxo-28-nortyphasterol and 6-deoxo-28-norcastasterone, possible precursors of 28-norcastasterone. Phytochemistry 58: 233–238 PubMed

Yu X, Li L, Zola J, Aluru M, Ye H, Foudree A, Guo H, Anderson S, Aluru S, Liu P, et al. (2011) A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant J 65: 634–646 PubMed

Zhang Z, Liao H, Lucas WJ. (2014) Molecular mechanisms underlying phosphate sensing, signaling, and adaptation in plants. J Integr Plant Biol 56: 192–220 PubMed

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