Role of cis-zeatin in root responses to phosphate starvation.
Arabidopsis
ciz-zeatin
phosphate starvation
root hair
root system
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
10 2019
10 2019
Historique:
received:
16
05
2019
accepted:
15
06
2019
pubmed:
24
6
2019
medline:
6
5
2020
entrez:
24
6
2019
Statut:
ppublish
Résumé
Phosphate (Pi) is an essential nutrient for all organisms. Roots are underground organs, but the majority of the root biology studies have been done on root systems growing in the presence of light. Root illumination alters the Pi starvation response (PSR) at different intensities. Thus, we have analyzed morphological, transcriptional and physiological responses to Pi starvation in dark-grown roots. We have identified new genes and pathways regulated by Pi starvation that were not described previously. We also show that Pi-starved plants increase the cis-zeatin (cZ) : trans-zeatin (tZ) ratio. Transcriptomic analyses show that tZ preferentially represses cell cycle and PSR genes, whereas cZ induces genes involved in cell and root hair elongation and differentiation. In fact, cZ-treated seedlings show longer root system as well as longer root hairs compared with tZ-treated seedlings, increasing the total absorbing surface. Mutants with low cZ concentrations do not allocate free Pi in roots during Pi starvation. We propose that Pi-starved plants increase the cZ : tZ ratio to maintain basal cytokinin responses and allocate Pi in the root system to sustain its growth. Therefore, cZ acts as a PSR hormone that stimulates root and root hair elongation to enlarge the root absorbing surface and to increase Pi concentrations in roots.
Substances chimiques
Phosphates
0
Plant Growth Regulators
0
Zeatin
7I6OOJ9GR6
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
242-257Commentaires et corrections
Type : ErratumIn
Informations de copyright
© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.
Références
Ames BN. 1966. Assay of inorganic phosphate, total phosphate and phosphatases. Methods in Enzymology 8: 115-118.
Baek D, Chun HJ, Kang S, Shin G, Su Jung P, Hong H, Chanmin K, Doh Hoon K, Lee SY, Min Chul K et al. 2016. A role for Arabidopsis miR399f in salt, drought, and ABA signaling. Molecules and Cells 39: 111-118.
Baek D, Chun HJ, Yun DJ, Kim MC. 2017. Cross-talk between phosphate starvation and other environmental stress signaling pathways in plants. Molecules and Cells 40: 697-705.
Bari R, Datt Pant B, Stitt M, Scheible W-R. 2006. PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiology 141: 988-999.
Bustos R, Castrillo G, Linhares F, Puga MI, Rubio V, Pérez-Pérez J, Solano R, Leyva A, Paz-Ares J. 2010. A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genetics 6: e1001102.
Catarecha P, Segura MD, Franco-Zorrilla JM, Garcia-Ponce B, Lanza M, Solano R, Paz-Ares J, Leyva A. 2007. A mutant of the Arabidopsis phosphate transporter PHT1;1 displays enhanced arsenic accumulation. Plant Cell 19: 1123-1133.
Chang L, Ramireddy E, Schmülling T. 2015. Cytokinin as a positional cue regulating lateral root spacing in Arabidopsis. Journal of Experimental Botany 66: 4759-4768.
Colon-Carmona A, You R, Haimovitch-Gal T, Doerner P. 1999. Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. The Plant Journal 20: 503-508.
Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S. 2007. Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Current Biology 17: 678-682.
Du Y, Scheres B. 2018. Lateral root formation and the multiple roles of auxin. Journal of Experimental Botany 69: 155-167.
El Yacoubi B, Bailly M, de Crecy-Lagard V. 2012. Biosynthesis and function of posttranscriptional modifications of transfer RNAs. Annual Review of Genetics 46: 69-95.
Franco-Zorrilla JM, Martín AC, Leyva A, Paz-Ares J. 2005. Interaction between phosphate-starvation, sugar, and cytokinin signaling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiology 138: 847-857.
Franco-Zorrilla JM, Martin AC, Solano R, Rubio V, Leyva A, Paz-Ares J. 2002. Mutations at CRE1 impair cytokinin-induced repression of phosphate starvation responses in Arabidopsis. The Plant Journal 32: 353-360.
Gajdosova S, Spichal L, Kaminek M, Hoyerova K, Novak O, Dobrev PI, Galuszka P, Klima P, Gaudinova A, Zizkova E et al. 2011. Distribution, biological activities, metabolism, and the conceivable function of cis-zeatin-type cytokinins in plants. Journal of Experimental Botany 62: 2827-2840.
Gamuyao R, Chin JH, Pariasca-Tanaka J, Pesaresi P, Catausan S, Dalid C, Slamet-Loedin I, Tecson-Mendoza EM, Wissuwa M, Heuer S. 2012. The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488: 535-539.
Giehl RFH, von Wirén N. 2014. Root nutrient foraging. Plant Physiology 166: 509-517.
Goh T, Kasahara H, Mimura T, Kamiya Y, Fukaki H. 2012. Multiple AUX/IAA-ARF modules regulate lateral root formation: the role of Arabidopsis SHY2/IAA3-mediated auxin signalling. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 367: 1461-1468.
Großkinsky DK, Edelsbrunner K, Pfeifhofer H, van der Graaff E, Roitsch T. 2013. Cis- and trans-zeatin differentially modulate plant immunity. Plant Signaling & Behavior 8: e24798.
Gruber BD, Giehl RF, Friedel S, von Wiren N. 2013. Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiology 163: 161-179.
Hamburger D, Rezzonico E, MacDonald-Comber Petétot J, Somerville C, Poirier Y. 2002. Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14: 889-902.
Havlova M, Dobrev PI, Motyka V, Storchova H, Libus J, Dobra J, Malbeck J, Gaudinova A, Vankova R. 2008. The role of cytokinins in responses to water deficit in tobacco plants over-expressing trans-zeatin O-glucosyltransferase gene under 35S or SAG12 promoters. Plant, Cell & Environment 31: 341-353.
Heyl A, Riefler M, Romanov GA, Schmülling T. 2012. Properties, functions and evolution of cytokinin receptors. European Journal of Cell Biology 91: 246-256.
Hsieh LC, Lin SI, Kuo HF, Chiou TJ. 2010. Abundance of tRNA-derived small RNAs in phosphate-starved Arabidopsis roots. Plant Signaling & Behavior 5: 537-539.
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 Physiology 145: 1460-1470.
Jiang CJ, Shimono M, Sugano S, Kojima M, Liu X, Inoue H, Sakakibara H, Takatsuji H. 2013. Cytokinins act synergistically with salicylic acid to activate defense gene expression in rice. Molecular Plant-Microbe Interactions 26: 287-296.
Jurado S, Trivino SD, Abraham Z, Manzano C, Gutierrez C, Del Pozo C. 2008. SKP2A protein, an F-box that regulates cell division, is degraded via the ubiquitin pathway. Plant Signaling & Behavior 3: 810-812.
Kollmer I, Novak O, Strnad M, Schmulling T, Werner T. 2014. Overexpression of the cytosolic cytokinin oxidase/dehydrogenase (CKX7) from Arabidopsis causes specific changes in root growth and xylem differentiation. The Plant Journal 78: 359-371.
Kuiper D, SteingrÖVer E. 1991. Responses of growth, shoot to root ratio and cytokinin concentrations in root tissue of two barley varieties, differing if their salt resistance. In: McMichael BL, Persson H, eds. Developments in agricultural and managed forest ecology. New York, NY, USA: Elsevier, 463-471.
Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M, Nagato Y, Sakakibara H, Kyozuka J. 2007. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445: 652-655.
Kuroha T, Tokunaga H, Kojima M, Ueda N, Ishida T, Nagawa S, Fukuda H, Sugimoto K, Sakakibara H. 2009. Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. Plant Cell 21: 3152-3169.
Laplaze L, Benkova E, Casimiro I, Maes L, Vanneste S, Swarup R, Weijers D, Calvo V, Parizot B, Herrera-Rodriguez MB et al. 2007. Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell 19: 3889-3900.
Li X, Mo X, Shou H, Wu P. 2006. Cytokinin-mediated cell cycling arrest of pericycle founder cells in lateral root initiation of Arabidopsis. Plant and Cell Physiology 47: 1112-1123.
Liu J, Muller B. 2017. Imaging TCSn:GFP, a synthetic cytokinin reporter, in Arabidopsis thaliana. Methods in Molecular Biology 1497: 81-90.
Lomin SN, Krivosheev DM, Steklov M, Osolodkin DI, Romanov GA. 2012. Receptor properties and features of cytokinin signaling. Acta Naturae 4: 31-45.
Lopez-Bucio J, Cruz-Ramirez A, Herrera-Estrella L. 2003. The role of nutrient availability in regulating root architecture. Current Opinion in Plant Biology 6: 280-287.
Lynch JP, Brown KM. 2001. Topsoil foraging - an architectural adaptation of plants to low phosphorus availability. Plant and Soil 237: 225-237.
Manzano C, Pallero-Baena M, Silva-Navas J, Navarro Neila S, Casimiro I, Casero P, Garcia-Mina JM, Baigorri R, Rubio L, Fernandez JA et al. 2017. A light-sensitive mutation in Arabidopsis LEW3 reveals the important role of N-glycosylation in root growth and development. Journal of experimental botany 68: 5103-5116.
Manzano C, Ramirez-Parra E, Casimiro I, Otero S, Desvoyes B, De Rybel B, Beeckman T, Casero P, Gutierrez C, Del Pozo JC. 2012. Auxin and epigenetic regulation of SKP2B, an F-box that represses lateral root formation. Plant Physiology 160: 749-762.
Martin AC, del Pozo JC, Iglesias J, Rubio V, Solano R, de la Pena A, Leyva A, Paz-Ares J. 2000. Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. The Plant Journal 24: 559-567.
Megel C, Morelle G, Lalande S, Duchêne A-M, Small I, Maréchal-Drouard L. 2015. Surveillance and cleavage of eukaryotic tRNAs. International Journal of Molecular Sciences 16: 1873-1893.
Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N et al. 2005. A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proceedings of the National Academy of Sciences, USA 102: 11934-11939.
Miyawaki K, Tarkowski P, Matsumoto-Kitano M, Kato T, Sato S, Tarkowska D, Tabata S, Sandberg G, Kakimoto T. 2006. Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proceedings of the National Academy of Sciences, USA 103: 16598-16603.
Mora-Macias J, Ojeda-Rivera JO, Gutierrez-Alanis D, Yong-Villalobos L, Oropeza-Aburto A, Raya-Gonzalez J, Jimenez-Dominguez G, Chavez-Calvillo G, Rellan-Alvarez R, Herrera-Estrella L. 2017. Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate. Proceedings of the National Academy of Sciences, USA 114: E3563-E3572.
Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C. 2004. Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16: 1365-1377.
Nussaume L, Kanno S, Javot H, Marin E, Pochon N, Ayadi A, Nakanishi TM, Thibaud M-C. 2011. Phosphate import in plants: focus on the PHT1 transporters. Frontiers in Plant Science 2: 83.
Park EJ, Kim T-H. 2018. Fine-tuning of gene expression by tRNA-derived fragments during abiotic stress signal transduction. International Journal of Molecular Sciences 19: 518.
Peret B, Clement M, Nussaume L, Desnos T. 2011. Root developmental adaptation to phosphate starvation: better safe than sorry. Trends in Plant Science 16: 442-450.
Perez-Torres C-A, Lopez-Bucio J, Cruz-Ramirez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L. 2008. Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20: 3258-3272.
Raghothama KG. 1999. Phosphate acquisition. Annual Review of Plant Physiology and Plant Molecular Biology 50: 665-693.
Romanov GA, Lomin SN, Schmulling T. 2006. Biochemical characteristics and ligand-binding properties of Arabidopsis cytokinin receptor AHK3 compared to CRE1/AHK4 as revealed by a direct binding assay. Journal of Experimental Botany 57: 4051-4058.
Rouached H, Arpat AB, Poirier Y. 2010. Regulation of phosphate starvation responses in plants: signaling players and cross-talks. Molecular Plant 3: 288-299.
Ruan W, Guo M, Cai L, Hu H, Li C, Liu Y, Wu Z, Mao C, Yi K, Wu P et al. 2015. Genetic manipulation of a high-affinity PHR1 target cis-element to improve phosphorous uptake in Oryza sativa L. Plant Molecular Biology 87: 429-440.
Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, Leyva A, Paz-Ares J. 2001. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes & Development 15: 2122-2133.
Sakakibara H. 2006. Cytokinins: activity, biosynthesis, and translocation. Annual Review of Plant Biology 57: 431-449.
Sanchez-Calderon L, Lopez-Bucio J, Chacon-Lopez A, Cruz-Ramirez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L. 2005. Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant and Cell Physiology 46: 174-184.
Schäfer M, Brütting C, Meza-Canales ID, Großkinsky DK, Vankova R, Baldwin IT, Meldau S. 2015. The role of cis-zeatin-type cytokinins in plant growth regulation and mediating responses to environmental interactions. Journal of Experimental Botany 66: 4873-4884.
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B. 2012. Fiji: an open-source platform for biological-image analysis. Nature methods 9: 676-682.
Secco D, Whelan J. 2014. Toward deciphering the genome-wide transcriptional responses of rice to phosphate starvation and recovery. Plant Signaling & Behavior 9: e28319.
Shen C, Yue R, Yang Y, Zhang L, Sun T, Tie S, Wang H. 2014. OsARF16 is involved in cytokinin-mediated inhibition of phosphate transport and phosphate signaling in rice (Oryza sativa L.). PLoS ONE 9: e112906.
Silva-Navas J, Moreno-Risueno MA, Manzano C, Pallero-Baena M, Navarro-Neila S, Téllez-Robledo B, Garcia-Mina JM, Baigorri R, Javier Gallego F, del Pozo JC. 2015. D-Root: a system to cultivate plants with the root in darkness or under different light conditions. The Plant Journal 84: 244-255.
Silva-Navas J, Moreno-Risueno MA, Manzano C, Téllez-Robledo B, Navarro-Neila S, Carrasco V, Pollmann S, Gallego FJ, del Pozo JC. 2016. Flavonols mediate root phototropism and growth through regulation of proliferation to-differentiation transition. Plant Cell 28: 1372-1387.
Stolz A, Riefler M, Lomin SN, Achazi K, Romanov GA, Schmulling T. 2011. The specificity of cytokinin signalling in Arabidopsis thaliana is mediated by differing ligand affinities and expression profiles of the receptors. The Plant Journal 67: 157-168.
Swain T, Hillis WE. 1959. The phenolic constituents of Prunus domestica. I.-The quantitative analysis of phenolic constituents. Journal of the Science of Food and Agriculture 10: 63-68.
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. Proceedings of the National Academy of Sciences, USA 106: 14174-14179.
Vyroubalova S, Vaclavikova K, Tureckova V, Novak O, Smehilova M, Hluska T, Ohnoutkova L, Frebort I, Galuszka P. 2009. Characterization of new maize genes putatively involved in cytokinin metabolism and their expression during osmotic stress in relation to cytokinin levels. Plant Physiology 151: 433-447.
Wang L, Dong J, Gao Z, Liu D. 2012. The Arabidopsis gene HYPERSENSITIVE TO PHOSPHATE STARVATION 3 encodes ETHYLENE OVERPRODUCTION 1. Plant and Cell Physiology 53: 1093-1105.
Wang X, Yi K, Tao Y, Wang F, Wu Z, Jiang D, Chen X, Zhu L, Wu P. 2006. Cytokinin represses phosphate-starvation response through increasing of intracellular phosphate level. Plant, Cell & Environment 29: 1924-1935.
Ward JT, Lahner B, Yakubova E, Salt DE, Raghothama KG. 2008. The effect of iron on the primary root elongation of Arabidopsis during phosphate deficiency. Plant Physiology 147: 1181-1191.
Werner T, Holst K, Pörs Y, Guivarc'h A, Mustroph A, Chriqui D, Grimm B, Schmülling T. 2008. Cytokinin deficiency causes distinct changes of sink and source parameters in tobacco shoots and roots. Journal of Experimental Botany 59: 2659-2672.
Woo J, MacPherson CR, Liu J, Wang H, Kiba T, Hannah MA, Wang XJ, Bajic VB, Chua NH. 2012. The response and recovery of the Arabidopsis thaliana transcriptome to phosphate starvation. BMC Plant Biology 12: 62.
Yeh C-M, Kobayashi K, Fujii S, Fukaki H, Mitsuda N, Ohme-Takagi M. 2017. Blue light negatively regulates tolerance to phosphate deficiency in Arabidopsis. bioRxiv. doi: 10.1101/235952