Nitrate, Auxin and Cytokinin—A Trio to Tango
Abstract
:1. Introduction
2. Nitrate Transport and Signaling
3. The Role of Auxin in Nitrate-Regulated Plant Growth and Development
4. The Role of Cytokinin in Nitrate-Regulated Plant Growth
5. Auxin-Cytokinin Crosstalk in Plant Adaptation to Nitrate Availability
6. Conclusions and Future Directions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Hirel, B.; Le Gouis, J.; Ney, B.; Gallais, A. The challenge of improving nitrogen use efficiency in crop plants: Towards a more central role for genetic variability and quantitative genetics within integrated approaches. J. Exp. Bot. 2007, 58, 2369–2387. [Google Scholar] [CrossRef] [PubMed]
- Hirose, T. Nitrogen use efficiency revisited. Oecologia 2011, 166, 863–867. [Google Scholar] [CrossRef] [PubMed]
- Gruber, N.; Galloway, J.N. An Earth-system perspective of the global nitrogen cycle. Nature 2008, 451, 293–296. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hirel, B.; Tétu, T.; Lea, P.J.; Dubois, F. Improving Nitrogen Use Efficiency in Crops for Sustainable Agriculture. Sustainability 2011, 3, 1452–1485. [Google Scholar] [CrossRef]
- von Wirén, N.; Gazzarrini, S.; Gojon, A.; Frommer, W.B. The molecular physiology of ammonium uptake and retrieval. Curr. Opin. Plant Biol. 2000, 3, 254–261. [Google Scholar] [CrossRef]
- Crawford, N.M.; Glass, A.D.M. Molecular and physiological aspects of nitrate uptake in plants. Trends Plant Sci. 1998, 3, 389–395. [Google Scholar] [CrossRef]
- Näsholm, T.; Kielland, K.; Ganeteg, U. Uptake of organic nitrogen by plants. New Phytol. 2009, 182, 31–48. [Google Scholar] [CrossRef]
- Hänsch, R.; Mendel, R.R. Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr. Opin. Plant Biol. 2009, 12, 259–266. [Google Scholar] [CrossRef]
- Ötvös, K.; Marconi, M.; Vega, A.; O’Brien, J.; Johnson, A.; Abualia, R.; Antonielli, L.; Montesinos, J.C.; Zhang, Y.; Tan, S.; et al. Modulation of plant root growth by nitrogen source-defined regulation of polar auxin transport. EMBO J. 2021, 40, e106862. [Google Scholar] [CrossRef]
- Alvarez, J.M.; Riveras, E.; Vidal, E.A.; Gras, D.E.; Contreras-López, O.; Tamayo, K.P.; Aceituno, F.; Gómez, I.; Ruffel, S.; Lejay, L.; et al. Systems approach identifies TGA1 and TGA4 transcription factors as important regulatory components of the nitrate response of Arabidopsis thaliana roots. Plant J. Cell Mol. Biol. 2014, 80, 1–13. [Google Scholar] [CrossRef]
- Vidal, E.A.; Araus, V.; Lu, C.; Parry, G.; Green, P.J.; Coruzzi, G.M.; Gutiérrez, R.A. Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 2010, 107, 4477–4482. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vidal, E.A.; Álvarez, J.M.; Gutiérrez, R.A. Nitrate regulation of AFB3 and NAC4 gene expression in Arabidopsis roots depends on NRT1.1 nitrate transport function. Plant Signal. Behav. 2014, 9, e28501. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, H.; Forde, B.G. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 1998, 279, 407–409. [Google Scholar] [CrossRef] [PubMed]
- Tian, Q.-Y.; Sun, P.; Zhang, W.-H. Ethylene is involved in nitrate-dependent root growth and branching in Arabidopsis thaliana. New Phytol. 2009, 184, 918–931. [Google Scholar] [CrossRef]
- Li, Q.; Li, B.-H.; Kronzucker, H.J.; Shi, W.-M. Root growth inhibition by NH(4)(+) in Arabidopsis is mediated by the root tip and is linked to NH(4)(+) efflux and GMPase activity. Plant Cell Environ. 2010, 33, 1529–1542. [Google Scholar] [CrossRef]
- Walch-Liu, P.; Ivanov, I.I.; Filleur, S.; Gan, Y.; Remans, T.; Forde, B.G. Nitrogen Regulation of Root Branching. Ann. Bot. 2006, 97, 875–881. [Google Scholar] [CrossRef] [PubMed]
- Takei, K.; Ueda, N.; Aoki, K.; Kuromori, T.; Hirayama, T.; Shinozaki, K.; Yamaya, T.; Sakakibara, H. AtIPT3 is a Key Determinant of Nitrate-Dependent Cytokinin Biosynthesis in Arabidopsis. Plant Cell Physiol. 2004, 45, 1053–1062. [Google Scholar] [CrossRef] [Green Version]
- Poitout, A.; Crabos, A.; Petřík, I.; Novák, O.; Krouk, G.; Lacombe, B.; Ruffel, S. Responses to Systemic Nitrogen Signaling in Arabidopsis Roots Involve trans-Zeatin in Shoots. Plant Cell 2018, 30, 1243–1257. [Google Scholar] [CrossRef] [Green Version]
- Abualia, R.; Ötvös, K.; Novák, O.; Bouguyon, E.; Domanegg, K.; Krapp, A.; Nacry, P.; Gojon, A.; Lacombe, B.; Benková, E. Molecular framework integrating nitrate sensing in root and auxin-guided shoot adaptive responses. Proc. Natl. Acad. Sci. USA 2022, 119, e2122460119. [Google Scholar] [CrossRef]
- Maeda, Y.; Konishi, M.; Kiba, T.; Sakuraba, Y.; Sawaki, N.; Kurai, T.; Ueda, Y.; Sakakibara, H.; Yanagisawa, S. A NIGT1-centred transcriptional cascade regulates nitrate signalling and incorporates phosphorus starvation signals in Arabidopsis. Nat. Commun. 2018, 9, 1376. [Google Scholar] [CrossRef] [Green Version]
- Varala, K.; Marshall-Colón, A.; Cirrone, J.; Brooks, M.D.; Pasquino, A.V.; Léran, S.; Mittal, S.; Rock, T.M.; Edwards, M.B.; Kim, G.J.; et al. Temporal transcriptional logic of dynamic regulatory networks underlying nitrogen signaling and use in plants. Proc. Natl. Acad. Sci. USA 2018, 115, 6494–6499. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alvarez, J.M.; Schinke, A.-L.; Brooks, M.D.; Pasquino, A.; Leonelli, L.; Varala, K.; Safi, A.; Krouk, G.; Krapp, A.; Coruzzi, G.M. Transient genome-wide interactions of the master transcription factor NLP7 initiate a rapid nitrogen-response cascade. Nat. Commun. 2020, 11, 1157. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vega, A.; Fredes, I.; O’Brien, J.; Shen, Z.; Ötvös, K.; Abualia, R.; Benkova, E.; Briggs, S.P.; Gutiérrez, R.A. Nitrate triggered phosphoproteome changes and a PIN2 phosphosite modulating root system architecture. EMBO Rep. 2021, 22, e51813. [Google Scholar] [CrossRef] [PubMed]
- Liu, K.; Niu, Y.; Konishi, M.; Wu, Y.; Du, H.; Sun Chung, H.; Li, L.; Boudsocq, M.; McCormack, M.; Maekawa, S.; et al. Discovery of nitrate–CPK–NLP signalling in central nutrient–growth networks. Nature 2017, 545, 311–316. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gutiérrez, R.A.; Lejay, L.V.; Dean, A.; Chiaromonte, F.; Shasha, D.E.; Coruzzi, G.M. Qualitative network models and genome-wide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis. Genome Biol. 2007, 8, R7. [Google Scholar] [CrossRef] [Green Version]
- Castaings, L.; Camargo, A.; Pocholle, D.; Gaudon, V.; Texier, Y.; Boutet-Mercey, S.; Taconnat, L.; Renou, J.-P.; Daniel-Vedele, F.; Fernandez, E.; et al. The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J. 2009, 57, 426–435. [Google Scholar] [CrossRef]
- Marchive, C.; Roudier, F.; Castaings, L.; Bréhaut, V.; Blondet, E.; Colot, V.; Meyer, C.; Krapp, A. Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nat. Commun. 2013, 4, 1713. [Google Scholar] [CrossRef] [Green Version]
- Liu, K.-H.; Liu, M.; Lin, Z.; Wang, Z.-F.; Chen, B.; Liu, C.; Guo, A.; Konishi, M.; Yanagisawa, S.; Wagner, G.; et al. NIN-like protein 7 transcription factor is a plant nitrate sensor. Science 2022, 377, 1419–1425. [Google Scholar] [CrossRef]
- Liu, K.-H.; Diener, A.; Lin, Z.; Liu, C.; Sheen, J. Primary nitrate responses mediated by calcium signalling and diverse protein phosphorylation. J. Exp. Bot. 2020, 71, 4428–4441. [Google Scholar] [CrossRef]
- Krouk, G.; Lacombe, B.; Bielach, A.; Perrine-Walker, F.; Malinska, K.; Mounier, E.; Hoyerova, K.; Tillard, P.; Leon, S.; Ljung, K.; et al. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell 2010, 18, 927–937. [Google Scholar] [CrossRef]
- Maghiaoui, A.; Bouguyon, E.; Cuesta, C.; Perrine-Walker, F.; Alcon, C.; Krouk, G.; Benková, E.; Nacry, P.; Gojon, A.; Bach, L. The Arabidopsis NRT1.1 transceptor coordinately controls auxin biosynthesis and transport to regulate root branching in response to nitrate. J. Exp. Bot. 2020, 71, 4480–4494. [Google Scholar] [CrossRef] [PubMed]
- Mounier, E.; Pervent, M.; Ljung, K.; Gojon, A.; Nacry, P. Auxin-mediated nitrate signalling by NRT1.1 participates in the adaptive response of Arabidopsis root architecture to the spatial heterogeneity of nitrate availability. Plant Cell Environ. 2014, 37, 162–174. [Google Scholar] [CrossRef] [PubMed]
- Signora, L.; De Smet, I.; Foyer, C.H.; Zhang, H. ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis. Plant J. Cell Mol. Biol. 2001, 28, 655–662. [Google Scholar] [CrossRef] [Green Version]
- Kiba, T.; Krapp, A. Plant Nitrogen Acquisition Under Low Availability: Regulation of Uptake and Root Architecture. Plant Cell Physiol. 2016, 57, 707–714. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vidal, E.A.; Alvarez, J.M.; Araus, V.; Riveras, E.; Brooks, M.D.; Krouk, G.; Ruffel, S.; Lejay, L.; Crawford, N.M.; Coruzzi, G.M.; et al. Nitrate in 2020: Thirty Years from Transport to Signaling Networks. Plant Cell 2020, 32, 2094–2119. [Google Scholar] [CrossRef]
- O’Brien, J.A.; Vega, A.; Bouguyon, E.; Krouk, G.; Gojon, A.; Coruzzi, G.; Gutiérrez, R.A. Nitrate Transport, Sensing, and Responses in Plants. Mol. Plant 2016, 9, 837–856. [Google Scholar] [CrossRef] [Green Version]
- Krapp, A.; David, L.C.; Chardin, C.; Girin, T.; Marmagne, A.; Leprince, A.-S.; Chaillou, S.; Ferrario-Méry, S.; Meyer, C.; Daniel-Vedele, F. Nitrate transport and signalling in Arabidopsis. J. Exp. Bot. 2014, 65, 789–798. [Google Scholar] [CrossRef]
- Noguero, M.; Lacombe, B. Transporters Involved in Root Nitrate Uptake and Sensing by Arabidopsis. Front. Plant Sci. 2016, 7, 1391. [Google Scholar] [CrossRef] [Green Version]
- Morgan, M.A.; Volk, R.J.; Jackson, W.A. Simultaneous Influx and Efflux of Nitrate during Uptake by Perennial Ryegrass 1. Plant Physiol. 1973, 51, 267–272. [Google Scholar] [CrossRef] [Green Version]
- Hanson, J.B. Application of the Chemiosmotic Hypothesis to Ion Transport Across the Root. Plant Physiol. 1978, 62, 402–405. [Google Scholar] [CrossRef] [Green Version]
- Filleur, S.; Dorbe, M.F.; Cerezo, M.; Orsel, M.; Granier, F.; Gojon, A.; Daniel-Vedele, F. An arabidopsis T-DNA mutant affected in Nrt2 genes is impaired in nitrate uptake. FEBS Lett. 2001, 489, 220–224. [Google Scholar] [CrossRef] [Green Version]
- Filleur, S.; Daniel-Vedele, F. Expression analysis of a high-affinity nitrate transporter isolated from Arabidopsis thaliana by differential display. Planta 1999, 207, 461–469. [Google Scholar] [CrossRef]
- Trueman, L.J.; Richardson, A.; Forde, B.G. Molecular cloning of higher plant homologues of the high-affinity nitrate transporters of Chlamydomonas reinhardtii and Aspergillus nidulans. Gene 1996, 175, 223–231. [Google Scholar] [CrossRef] [PubMed]
- Li, W.; Wang, Y.; Okamoto, M.; Crawford, N.M.; Siddiqi, M.Y.; Glass, A.D.M. Dissection of the AtNRT2.1:AtNRT2.2 inducible high-affinity nitrate transporter gene cluster. Plant Physiol. 2007, 143, 425–433. [Google Scholar] [CrossRef] [Green Version]
- Miller, A.J.; Fan, X.; Orsel, M.; Smith, S.J.; Wells, D.M. Nitrate transport and signalling. J. Exp. Bot. 2007, 58, 2297–2306. [Google Scholar] [CrossRef]
- Liu, K.-H.; Tsay, Y.-F. Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J. 2003, 22, 1005–1013. [Google Scholar] [CrossRef] [Green Version]
- Tsay, Y.-F. Plant science: How to switch affinity. Nature 2014, 507, 44–45. [Google Scholar] [CrossRef]
- Tsay, Y.F.; Schroeder, J.I.; Feldmann, K.A.; Crawford, N.M. The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 1993, 72, 705–713. [Google Scholar] [CrossRef] [PubMed]
- Liu, K.H.; Huang, C.Y.; Tsay, Y.F. CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 1999, 11, 865–874. [Google Scholar] [CrossRef]
- Huang, N.C.; Chiang, C.S.; Crawford, N.M.; Tsay, Y.F. CHL1 encodes a component of the low-affinity nitrate uptake system in Arabidopsis and shows cell type-specific expression in roots. Plant Cell 1996, 8, 2183–2191. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, R.; Liu, D.; Crawford, N.M. The Arabidopsis CHL1 protein plays a major role in high-affinity nitrate uptake. Proc. Natl. Acad. Sci. USA 1998, 95, 15134–15139. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ho, C.-H.; Lin, S.-H.; Hu, H.-C.; Tsay, Y.-F. CHL1 functions as a nitrate sensor in plants. Cell 2009, 138, 1184–1194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kotur, Z.; Mackenzie, N.; Ramesh, S.; Tyerman, S.D.; Kaiser, B.N.; Glass, A.D.M. Nitrate transport capacity of the Arabidopsis thaliana NRT2 family members and their interactions with AtNAR2.1. New Phytol. 2012, 194, 724–731. [Google Scholar] [CrossRef] [PubMed]
- Cerezo, M.; Tillard, P.; Filleur, S.; Muños, S.; Daniel-Vedele, F.; Gojon, A. Major Alterations of the Regulation of Root NO3−Uptake Are Associated with the Mutation of Nrt2.1 and Nrt2.2 Genes in Arabidopsis. Plant Physiol. 2001, 127, 262–271. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Little, D.Y.; Rao, H.; Oliva, S.; Daniel-Vedele, F.; Krapp, A.; Malamy, J.E. The putative high-affinity nitrate transporter NRT2.1 represses lateral root initiation in response to nutritional cues. Proc. Natl. Acad. Sci. USA 2005, 102, 13693–13698. [Google Scholar] [CrossRef] [Green Version]
- Remans, T.; Nacry, P.; Pervent, M.; Girin, T.; Tillard, P.; Lepetit, M.; Gojon, A. A Central Role for the Nitrate Transporter NRT2.1 in the Integrated Morphological and Physiological Responses of the Root System to Nitrogen Limitation in Arabidopsis. Plant Physiol. 2006, 140, 909–921. [Google Scholar] [CrossRef] [Green Version]
- Lejay, L.; Gojon, A. Chapter Six-Root Nitrate Uptake. In Advances in Botanical Research; Maurel, C., Ed.; Membrane Transport in Plants; Academic Press: Cambridge, MA, USA, 2018; Volume 87, pp. 139–169. [Google Scholar]
- Zhao, Y. Auxin biosynthesis: A simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Mol. Plant 2012, 5, 334–338. [Google Scholar] [CrossRef] [Green Version]
- Benková, E.; Michniewicz, M.; Sauer, M.; Teichmann, T.; Seifertová, D.; Jürgens, G.; Friml, J. Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation. Cell 2003, 115, 591–602. [Google Scholar] [CrossRef] [Green Version]
- Friml, J.; Vieten, A.; Sauer, M.; Weijers, D.; Schwarz, H.; Hamann, T.; Offringa, R.; Jürgens, G. Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis. Nature 2003, 426, 147–153. [Google Scholar] [CrossRef]
- Reinhardt, D.; Pesce, E.-R.; Stieger, P.; Mandel, T.; Baltensperger, K.; Bennett, M.; Traas, J.; Friml, J.; Kuhlemeier, C. Regulation of phyllotaxis by polar auxin transport. Nature 2003, 426, 255–260. [Google Scholar] [CrossRef]
- Chapman, E.J.; Estelle, M. Mechanism of auxin-regulated gene expression in plants. Annu. Rev. Genet. 2009, 43, 265–285. [Google Scholar] [CrossRef] [Green Version]
- Rademacher, E.H.; Lokerse, A.S.; Schlereth, A.; Llavata-Peris, C.I.; Bayer, M.; Kientz, M.; Freire Rios, A.; Borst, J.W.; Lukowitz, W.; Jürgens, G.; et al. Different Auxin Response Machineries Control Distinct Cell Fates in the Early Plant Embryo. Dev. Cell 2012, 22, 211–222. [Google Scholar] [CrossRef] [Green Version]
- Bargmann, B.O.R.; Vanneste, S.; Krouk, G.; Nawy, T.; Efroni, I.; Shani, E.; Choe, G.; Friml, J.; Bergmann, D.C.; Estelle, M.; et al. A map of cell type-specific auxin responses. Mol. Syst. Biol. 2013, 9, 688. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fendrych, M.; Akhmanova, M.; Merrin, J.; Glanc, M.; Hagihara, S.; Takahashi, K.; Uchida, N.; Torii, K.U.; Friml, J. Rapid and reversible root growth inhibition by TIR1 auxin signalling. Nat. Plants 2018, 4, 453–459. [Google Scholar] [CrossRef] [PubMed]
- Kubeš, M.; Napier, R. Non-canonical auxin signalling: Fast and curious. J. Exp. Bot. 2019, 70, 2609–2614. [Google Scholar] [CrossRef]
- Lin, W.; Zhou, X.; Tang, W.; Takahashi, K.; Pan, X.; Dai, J.; Ren, H.; Zhu, X.; Pan, S.; Zheng, H.; et al. TMK-based cell-surface auxin signalling activates cell-wall acidification. Nature 2021, 599, 278–282. [Google Scholar] [CrossRef] [PubMed]
- Li, L.; Verstraeten, I.; Roosjen, M.; Takahashi, K.; Rodriguez, L.; Merrin, J.; Chen, J.; Shabala, L.; Smet, W.; Ren, H.; et al. Antagonistic cell surface and intracellular auxin signalling regulate plasma membrane H+-fluxes for root growth. Nature 2021, 599, 273. [Google Scholar] [CrossRef]
- Friml, J.; Gallei, M.; Gelová, Z.; Johnson, A.; Mazur, E.; Monzer, A.; Rodriguez, L.; Roosjen, M.; Verstraeten, I.; Živanović, B.D.; et al. ABP1–TMK auxin perception for global phosphorylation and auxin canalization. Nature 2022, 609, 575–581. [Google Scholar] [CrossRef]
- Cambridge, A.P.; Morris, D.A. Transfer of exogenous auxin from the phloem to the polar auxin transport pathway in pea (Pisum sativum L.). Planta 1996, 199, 583–588. [Google Scholar] [CrossRef]
- Adamowski, M.; Friml, J. PIN-dependent auxin transport: Action, regulation, and evolution. Plant Cell 2015, 27, 20–32. [Google Scholar] [CrossRef] [Green Version]
- Abualia, R.; Benkova, E.; Lacombe, B. Transporters and Mechanisms of Hormone Transport in Arabidopsis. Adv. Bot. Res. 2018, 87, 342. [Google Scholar] [CrossRef]
- Barbez, E.; Kubeš, M.; Rolčík, J.; Béziat, C.; Pěnčík, A.; Wang, B.; Rosquete, M.R.; Zhu, J.; Dobrev, P.I.; Lee, Y.; et al. A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature 2012, 485, 119–122. [Google Scholar] [CrossRef] [Green Version]
- Okada, K.; Ueda, J.; Komaki, M.K.; Bell, C.J.; Shimura, Y. Requirement of the Auxin Polar Transport System in Early Stages of Arabidopsis Floral Bud Formation. Plant Cell 1991, 3, 677–684. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bennett, M.J.; Marchant, A.; Green, H.G.; May, S.T.; Ward, S.P.; Millner, P.A.; Walker, A.R.; Schulz, B.; Feldmann, K.A. Arabidopsis AUX1 Gene: A Permease-Like Regulator of Root Gravitropism. Science 1996, 273, 948–950. [Google Scholar] [CrossRef]
- Ye, L.; Liu, L.; Xing, A.; Kang, D. Characterization of a dwarf mutant allele of Arabidopsis MDR-like ABC transporter AtPGP1 gene. Biochem. Biophys. Res. Commun. 2013, 441, 782–786. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Avery, G.S.; Pottorf, L. Auxin and Nitrogen Relationships in Green Plants. Am. J. Bot. 1945, 32, 666–669. [Google Scholar] [CrossRef]
- Caba, J.M.; Centeno, M.L.; Fernández, B.; Gresshoff, P.M.; Ligero, F. Inoculation and nitrate alter phytohormone levels in soybean roots: Differences between a supernodulating mutant and the wild type. Planta 2000, 211, 98–104. [Google Scholar] [CrossRef]
- Tian, Q.; Chen, F.; Liu, J.; Zhang, F.; Mi, G. Inhibition of maize root growth by high nitrate supply is correlated with reduced IAA levels in roots. J. Plant Physiol. 2008, 165, 942–951. [Google Scholar] [CrossRef] [PubMed]
- Meier, M.; Liu, Y.; Lay-Pruitt, K.S.; Takahashi, H.; von Wirén, N. Auxin-mediated root branching is determined by the form of available nitrogen. Nat. Plants 2020, 6, 1136–1145. [Google Scholar] [CrossRef]
- Ma, W.; Li, J.; Qu, B.; He, X.; Zhao, X.; Li, B.; Fu, X.; Tong, Y. Auxin biosynthetic gene TAR2 is involved in low nitrogen-mediated reprogramming of root architecture in Arabidopsis. Plant J. Cell Mol. Biol. 2014, 78, 70–79. [Google Scholar] [CrossRef]
- Bouguyon, E.; Brun, F.; Meynard, D.; Kubeš, M.; Pervent, M.; Leran, S.; Lacombe, B.; Krouk, G.; Guiderdoni, E.; Zažímalová, E.; et al. Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nat. Plants 2015, 1, 15015. [Google Scholar] [CrossRef] [PubMed]
- Porco, S.; Larrieu, A.; Du, Y.; Gaudinier, A.; Goh, T.; Swarup, K.; Swarup, R.; Kuempers, B.; Bishopp, A.; Lavenus, J.; et al. Lateral root emergence in Arabidopsis is dependent on transcription factor LBD29 regulation of auxin influx carrier LAX3. Development 2016, 143, 3340–3349. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lay-Pruitt, K.S.; Takahashi, H. Integrating N signals and root growth: The role of nitrate transceptor NRT1.1 in auxin-mediated lateral root development. J. Exp. Bot. 2020, 71, 4365–4368. [Google Scholar] [CrossRef] [PubMed]
- Lee, H.; Ganguly, A.; Baik, S.; Cho, H.-T. Calcium-dependent protein kinase 29 modulates PIN-FORMED polarity and Arabidopsis development via its own phosphorylation code. Plant Cell 2021, 33, 3513–3531. [Google Scholar] [CrossRef]
- Mok, D.W.; Mok, M.C. Cytokinin Metabolism and Action. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001, 52, 89–118. [Google Scholar] [CrossRef]
- El-Showk, S.; Ruonala, R.; Helariutta, Y. Crossing paths: Cytokinin signalling and crosstalk. Dev. Camb. Engl. 2013, 140, 1373–1383. [Google Scholar] [CrossRef] [Green Version]
- Gajdosová, S.; Spíchal, L.; Kamínek, M.; Hoyerová, K.; Novák, O.; Dobrev, P.I.; Galuszka, P.; Klíma, P.; Gaudinová, A.; Zizková, E.; et al. Distribution, biological activities, metabolism, and the conceivable function of cis-zeatin-type cytokinins in plants. J. Exp. Bot. 2011, 62, 2827–2840. [Google Scholar] [CrossRef] [Green Version]
- Silva-Navas, J.; Conesa, C.M.; Saez, A.; Navarro-Neila, S.; Garcia-Mina, J.M.; Zamarreño, A.M.; Baigorri, R.; Swarup, R.; del Pozo, J.C. Role of cis-zeatin in root responses to phosphate starvation. New Phytol. 2019, 224, 242–257. [Google Scholar] [CrossRef]
- Bhargava, A.; Clabaugh, I.; To, J.P.; Maxwell, B.B.; Chiang, Y.-H.; Schaller, G.E.; Loraine, A.; Kieber, J.J. Identification of Cytokinin-Responsive Genes Using Microarray Meta-Analysis and RNA-Seq in Arabidopsis. Plant Physiol. 2013, 162, 272–294. [Google Scholar] [CrossRef] [Green Version]
- Hirose, N.; Takei, K.; Kuroha, T.; Kamada-Nobusada, T.; Hayashi, H.; Sakakibara, H. Regulation of cytokinin biosynthesis, compartmentalization and translocation. J. Exp. Bot. 2008, 59, 75–83. [Google Scholar] [CrossRef] [Green Version]
- Sakakibara, H. Cytokinins: Activity, biosynthesis, and translocation. Annu. Rev. Plant Biol. 2006, 57, 431–449. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hirose, N.; Makita, N.; Yamaya, T.; Sakakibara, H. Functional characterization and expression analysis of a gene, OsENT2, encoding an equilibrative nucleoside transporter in rice suggest a function in cytokinin transport. Plant Physiol. 2005, 138, 196–206. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kieber, J.J.; Schaller, G.E. Cytokinins. Arab. Book 2014, 12, e0168. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zürcher, E.; Liu, J.; di Donato, M.; Geisler, M.; Müller, B. Plant development regulated by cytokinin sinks. Science 2016, 353, 1027–1030. [Google Scholar] [CrossRef] [Green Version]
- Durán-Medina, Y.; Díaz-Ramírez, D.; Marsch-Martínez, N. Cytokinins on the Move. Front. Plant Sci. 2017, 8, 146. [Google Scholar] [CrossRef] [Green Version]
- Ko, D.; Kang, J.; Kiba, T.; Park, J.; Kojima, M.; Do, J.; Kim, K.Y.; Kwon, M.; Endler, A.; Song, W.-Y.; et al. Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. Proc. Natl. Acad. Sci. USA 2014, 111, 7150–7155. [Google Scholar] [CrossRef] [Green Version]
- Zhang, K.; Novak, O.; Wei, Z.; Gou, M.; Zhang, X.; Yu, Y.; Yang, H.; Cai, Y.; Strnad, M.; Liu, C.-J. Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins. Nat. Commun. 2014, 5, 3274. [Google Scholar] [CrossRef] [Green Version]
- Rahayu, Y.S.; Walch-Liu, P.; Neumann, G.; Römheld, V.; von Wirén, N.; Bangerth, F. Root-derived cytokinins as long-distance signals for NO3−-induced stimulation of leaf growth. J. Exp. Bot. 2005, 56, 1143–1152. [Google Scholar] [CrossRef] [Green Version]
- Wang, R.; Okamoto, M.; Xing, X.; Crawford, N.M. Microarray Analysis of the Nitrate Response in Arabidopsis Roots and Shoots Reveals over 1,000 Rapidly Responding Genes and New Linkages to Glucose, Trehalose-6-Phosphate, Iron, and Sulfate Metabolism. Plant Physiol. 2003, 132, 556–567. [Google Scholar] [CrossRef] [Green Version]
- Ruffel, S.; Krouk, G.; Ristova, D.; Shasha, D.; Birnbaum, K.D.; Coruzzi, G.M. Nitrogen economics of root foraging: Transitive closure of the nitrate–cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc. Natl. Acad. Sci. USA 2011, 108, 18524–18529. [Google Scholar] [CrossRef] [Green Version]
- Sakakibara, H. Cytokinin biosynthesis and transport for systemic nitrogen signaling. Plant J. 2021, 105, 421–430. [Google Scholar] [CrossRef] [PubMed]
- Ruffel, S.; Poitout, A.; Krouk, G.; Coruzzi, G.M.; Lacombe, B. Long-distance nitrate signaling displays cytokinin dependent and independent branches. J. Integr. Plant Biol. 2016, 58, 226–229. [Google Scholar] [CrossRef] [PubMed]
- Roy, S. Nitrate Ahoy! Shoot Cytokinin Signals Integrate Growth Responses with Nitrogen Availability[OPEN]. Plant Cell 2018, 30, 1169–1170. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rashotte, A.M.; Mason, M.G.; Hutchison, C.E.; Ferreira, F.J.; Schaller, G.E.; Kieber, J.J. A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proc. Natl. Acad. Sci. USA 2006, 103, 11081–11085. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, Z.-B.; Liu, G.; Liu, J.; Zhang, B.; Meng, W.; Müller, B.; Hayashi, K.-I.; Zhang, X.; Zhao, Z.; De Smet, I.; et al. Synergistic action of auxin and cytokinin mediates aluminum-induced root growth inhibition in Arabidopsis. EMBO Rep. 2017, 18, 1213–1230. [Google Scholar] [CrossRef] [PubMed]
- Schlereth, A.; Möller, B.; Liu, W.; Kientz, M.; Flipse, J.; Rademacher, E.H.; Schmid, M.; Jürgens, G.; Weijers, D. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 2010, 464, 913–916. [Google Scholar] [CrossRef]
- Dello Ioio, R.; Nakamura, K.; Moubayidin, L.; Perilli, S.; Taniguchi, M.; Morita, M.T.; Aoyama, T.; Costantino, P.; Sabatini, S. A genetic framework for the control of cell division and differentiation in the root meristem. Science 2008, 322, 1380–1384. [Google Scholar] [CrossRef] [Green Version]
- Ruzicka, K.; Simásková, M.; Duclercq, J.; Petrásek, J.; Zazímalová, E.; Simon, S.; Friml, J.; Van Montagu, M.C.E.; Benková, E. Cytokinin regulates root meristem activity via modulation of the polar auxin transport. Proc. Natl. Acad. Sci. USA 2009, 106, 4284–4289. [Google Scholar] [CrossRef] [Green Version]
- Šimášková, M.; O’Brien, J.A.; Khan, M.; Van Noorden, G.; Ötvös, K.; Vieten, A.; De Clercq, I.; Van Haperen, J.M.A.; Cuesta, C.; Hoyerová, K.; et al. Cytokinin response factors regulate PIN-FORMED auxin transporters. Nat. Commun. 2015, 6, 8717. [Google Scholar] [CrossRef] [Green Version]
- Marhavý, P.; Bielach, A.; Abas, L.; Abuzeineh, A.; Duclercq, J.; Tanaka, H.; Pařezová, M.; Petrášek, J.; Friml, J.; Kleine-Vehn, J.; et al. Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis. Dev. Cell 2011, 21, 796–804. [Google Scholar] [CrossRef]
- Marhavý, P.; Duclercq, J.; Weller, B.; Feraru, E.; Bielach, A.; Offringa, R.; Friml, J.; Schwechheimer, C.; Murphy, A.; Benková, E. Cytokinin controls polarity of PIN1-dependent auxin transport during lateral root organogenesis. Curr. Biol. CB 2014, 24, 1031–1037. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ristova, D.; Carré, C.; Pervent, M.; Medici, A.; Kim, G.J.; Scalia, D.; Ruffel, S.; Birnbaum, K.D.; Lacombe, B.; Busch, W.; et al. Combinatorial interaction network of transcriptomic and phenotypic responses to nitrogen and hormones in the Arabidopsis thaliana root. Sci. Signal. 2016, 9, rs13. [Google Scholar] [CrossRef] [PubMed]
- Bruex, A.; Kainkaryam, R.M.; Wieckowski, Y.; Kang, Y.H.; Bernhardt, C.; Xia, Y.; Zheng, X.; Wang, J.Y.; Lee, M.M.; Benfey, P.; et al. A Gene Regulatory Network for Root Epidermis Cell Differentiation in Arabidopsis. PLoS Genet. 2012, 8, e1002446. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hawkesford, M.J.; Griffiths, S. Exploiting genetic variation in nitrogen use efficiency for cereal crop improvement. Curr. Opin. Plant Biol. 2019, 49, 35. [Google Scholar] [CrossRef] [PubMed]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Abualia, R.; Riegler, S.; Benkova, E. Nitrate, Auxin and Cytokinin—A Trio to Tango. Cells 2023, 12, 1613. https://doi.org/10.3390/cells12121613
Abualia R, Riegler S, Benkova E. Nitrate, Auxin and Cytokinin—A Trio to Tango. Cells. 2023; 12(12):1613. https://doi.org/10.3390/cells12121613
Chicago/Turabian StyleAbualia, Rashed, Stefan Riegler, and Eva Benkova. 2023. "Nitrate, Auxin and Cytokinin—A Trio to Tango" Cells 12, no. 12: 1613. https://doi.org/10.3390/cells12121613
APA StyleAbualia, R., Riegler, S., & Benkova, E. (2023). Nitrate, Auxin and Cytokinin—A Trio to Tango. Cells, 12(12), 1613. https://doi.org/10.3390/cells12121613