Molecular framework integrating nitrate sensing in root and auxin-guided shoot adaptive responses
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
35878040
PubMed Central
PMC9351359
DOI
10.1073/pnas.2122460119
Knihovny.cz E-zdroje
- Klíčová slova
- macronutrient, nitrate, plant development,
- MeSH
- cytokininy metabolismus MeSH
- dusičnany * metabolismus MeSH
- kořeny rostlin metabolismus MeSH
- kyseliny indoloctové * metabolismus MeSH
- půda MeSH
- regulace genové exprese u rostlin MeSH
- signální transdukce MeSH
- výhonky rostlin MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- cytokininy MeSH
- dusičnany * MeSH
- kyseliny indoloctové * MeSH
- půda MeSH
Mineral nutrition is one of the key environmental factors determining plant development and growth. Nitrate is the major form of macronutrient nitrogen that plants take up from the soil. Fluctuating availability or deficiency of this element severely limits plant growth and negatively affects crop production in the agricultural system. To cope with the heterogeneity of nitrate distribution in soil, plants evolved a complex regulatory mechanism that allows rapid adjustment of physiological and developmental processes to the status of this nutrient. The root, as a major exploitation organ that controls the uptake of nitrate to the plant body, acts as a regulatory hub that, according to nitrate availability, coordinates the growth and development of other plant organs. Here, we identified a regulatory framework, where cytokinin response factors (CRFs) play a central role as a molecular readout of the nitrate status in roots to guide shoot adaptive developmental response. We show that nitrate-driven activation of NLP7, a master regulator of nitrate response in plants, fine tunes biosynthesis of cytokinin in roots and its translocation to shoots where it enhances expression of CRFs. CRFs, through direct transcriptional regulation of PIN auxin transporters, promote the flow of auxin and thereby stimulate the development of shoot organs.
Zobrazit více v PubMed
Frink C. R., Waggoner P. E., Ausubel J. H., Nitrogen fertilizer: Retrospect and prospect. Proc. Natl. Acad. Sci. U.S.A. 96, 1175–1180 (1999). PubMed PMC
Crawford N. M., Forde B. G., Molecular and developmental biology of inorganic nitrogen nutrition. Arabidopsis Book 1, e0011 (2002). PubMed PMC
Kiba T., Krapp A., Plant nitrogen acquisition under low availability: Regulation of uptake and root architecture. Plant Cell Physiol. 57, 707–714 (2016). PubMed PMC
O’Brien J. A., et al. , Nitrate transport, sensing, and responses in plants. Mol. Plant 9, 837–856 (2016). PubMed
Bouguyon E., et al. , Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nat. Plants 1, 15015 (2015). PubMed
Ho C.-H., Lin S.-H., Hu H.-C., Tsay Y.-F., CHL1 functions as a nitrate sensor in plants. Cell 138, 1184–1194 (2009). PubMed
Krouk G., et al. , Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell 18, 927–937 (2010). PubMed
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 72, 705–713 (1993). PubMed
Alvarez J. M., et al. , Systems approach identifies TGA1 and TGA4 transcription factors as important regulatory components of the nitrate response of Arabidopsis thaliana roots. Plant J. 80, 1–13 (2014). PubMed
Castaings L., et al. , The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J. 57, 426–435 (2009). PubMed
Guan P., et al. , Interacting TCP and NLP transcription factors control plant responses to nitrate availability. Proc. Natl. Acad. Sci. U.S.A. 114, 2419–2424 (2017). PubMed PMC
Marchive C., et al. , Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nat. Commun. 4, 1713 (2013). PubMed
Rubin G., Tohge T., Matsuda F., Saito K., Scheible W.-R., Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in Arabidopsis. Plant Cell 21, 3567–3584 (2009). PubMed PMC
Varala K., et al. , Temporal transcriptional logic of dynamic regulatory networks underlying nitrogen signaling and use in plants. Proc. Natl. Acad. Sci. U.S.A. 115, 6494–6499 (2018). PubMed PMC
Wang J.-W., Czech B., Weigel D., miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138, 738–749 (2009). PubMed
Ruffel S., Gojon A., Systemic nutrient signalling: On the road for nitrate. Nat. Plants 3, 17040 (2017). PubMed
Chen X., et al. , Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition. Curr. Biol. 26, 640–646 (2016). PubMed
Ohkubo Y., Tanaka M., Tabata R., Ogawa-Ohnishi M., Matsubayashi Y., Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition. Nat. Plants 3, 17029 (2017). PubMed
Ota R., Ohkubo Y., Yamashita Y., Ogawa-Ohnishi M., Matsubayashi Y., Shoot-to-root mobile CEPD-like 2 integrates shoot nitrogen status to systemically regulate nitrate uptake in Arabidopsis. Nat. Commun. 11, 641 (2020). PubMed PMC
Poitout A., et al. , responses to systemic nitrogen signaling in Arabidopsis roots involve trans-zeatin in shoots. Plant Cell 30, 1243–1257 (2018). PubMed PMC
Ruffel S., et al. , 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. U.S.A. 108, 18524–18529 (2011). PubMed PMC
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. 58, 226–229 (2016). PubMed
Tabata R., et al. , Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346, 343–346 (2014). PubMed
Bouguyon E., Gojon A., Nacry P., Nitrate sensing and signaling in plants. Semin. Cell Dev. Biol. 23, 648–654 (2012). PubMed
Krouk G., Hormones and nitrate: A two-way connection. Plant Mol. Biol. 91, 599–606 (2016). PubMed
Landrein B., et al. , Nitrate modulates stem cell dynamics in Arabidopsis shoot meristems through cytokinins. Proc. Natl. Acad. Sci. U.S.A. 115, 1382–1387 (2018). PubMed PMC
Lee Z. H., Hirakawa T., Yamaguchi N., Ito T., The roles of plant hormones and their interactions with regulatory genes in determining meristem activity. Int. J. Mol. Sci. 20, 4065 (2019). PubMed PMC
Murray J. A. H., Jones A., Godin C., Traas J., Systems analysis of shoot apical meristem growth and development: Integrating hormonal and mechanical signaling. Plant Cell 24, 3907–3919 (2012). PubMed PMC
Wang R., et al. , Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol. 136, 2512–2522 (2004). PubMed PMC
Vidal E. A., Gutiérrez R. A., A systems view of nitrogen nutrient and metabolite responses in Arabidopsis. Curr. Opin. Plant Biol. 11, 521–529 (2008). PubMed
Little D. Y., et al. , The putative high-affinity nitrate transporter NRT2.1 represses lateral root initiation in response to nutritional cues. Proc. Natl. Acad. Sci. U.S.A. 102, 13693–13698 (2005). PubMed PMC
López-Bucio J., Cruz-Ramírez A., Herrera-Estrella L., The role of nutrient availability in regulating root architecture. Curr. Opin. Plant Biol. 6, 280–287 (2003). PubMed
Ötvös K., et al. , Modulation of plant root growth by nitrogen source-defined regulation of polar auxin transport. EMBO J. 40, e106862 (2021). PubMed PMC
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 6, 1136–1145 (2020). PubMed
Medici A., et al. , AtNIGT1/HRS1 integrates nitrate and phosphate signals at the Arabidopsis root tip. Nat. Commun. 6, 6274 (2015). PubMed PMC
Gan Y., Bernreiter A., Filleur S., Abram B., Forde B. G., Overexpressing the ANR1 MADS-box gene in transgenic plants provides new insights into its role in the nitrate regulation of root development. Plant Cell Physiol. 53, 1003–1016 (2012). PubMed
Benková E., et al. , Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602 (2003). PubMed
Friml J., Wiśniewska J., Benková E., Mendgen K., Palme K., Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806–809 (2002). PubMed
Friml J., et al. , Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147–153 (2003). PubMed
Reinhardt D., Vascular patterning: More than just auxin? Curr. Biol. 13, R485–R487 (2003). PubMed
Maeda Y., et al. , A NIGT1-centred transcriptional cascade regulates nitrate signalling and incorporates phosphorus starvation signals in Arabidopsis. Nat. Commun. 9, 1376 (2018). PubMed PMC
Guenot B., et al. , Pin1-independent leaf initiation in Arabidopsis. Plant Physiol. 159, 1501–1510 (2012). PubMed PMC
Sawchuk M. G., Edgar A., Scarpella E., Patterning of leaf vein networks by convergent auxin transport pathways. PLoS Genet. 9, e1003294 (2013). PubMed PMC
Bennett T., et al. , Connective auxin transport in the shoot facilitates communication between shoot apices. PLoS Biol. 14, e1002446 (2016). PubMed PMC
Šimášková M., et al. , Cytokinin response factors regulate PIN-FORMED auxin transporters. Nat. Commun. 6, 8717 (2015). PubMed
Raines T., et al. , The cytokinin response factors modulate root and shoot growth and promote leaf senescence in Arabidopsis. Plant J. 85, 134–147 (2016). PubMed
Yu L.-H., et al. , Overexpression of Arabidopsis NLP7 improves plant growth under both nitrogen-limiting and -sufficient conditions by enhancing nitrogen and carbon assimilation. Sci. Rep. 6, 27795 (2016). PubMed PMC
Sakakibara H., Cytokinin biosynthesis and transport for systemic nitrogen signaling. Plant J. 105, 421–430 (2021). PubMed
Takei K., et al. , AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis. Plant Cell Physiol. 45, 1053–1062 (2004). PubMed
Kiba T., Takei K., Kojima M., Sakakibara H., Side-chain modification of cytokinins controls shoot growth in Arabidopsis. Dev. Cell 27, 452–461 (2013). PubMed
Kudo T., Kiba T., Sakakibara H., Metabolism and long-distance translocation of cytokinins. J. Integr. Plant Biol. 52, 53–60 (2010). PubMed
Naulin P. A., et al. , Nitrate Induction of Primary Root Growth Requires Cytokinin Signaling in Arabidopsis thaliana. Plant Cell Physiol. 61, 342–352 (2020). PubMed
Gutiérrez R. A., et al. , Insights into the genomic nitrate response using genetics and the Sungear Software System. J. Exp. Bot. 58, 2359–2367 (2007). PubMed
Ma W., et al. , Auxin biosynthetic gene TAR2 is involved in low nitrogen-mediated reprogramming of root architecture in Arabidopsis. Plant J. 78, 70–79 (2014). PubMed
Maghiaoui A., et al. , The Arabidopsis NRT1.1 transceptor coordinately controls auxin biosynthesis and transport to regulate root branching in response to nitrate. J. Exp. Bot. 71, 4480–4494 (2020). PubMed
Alvarez J. M., et al. , Transient genome-wide interactions of the master transcription factor NLP7 initiate a rapid nitrogen-response cascade. Nat. Commun. 11, 1157 (2020). PubMed PMC
Liu K. H., et al. , Discovery of nitrate-CPK-NLP signalling in central nutrient-growth networks. Nature 545, 311–316 (2017). PubMed PMC
Horiguchi G., Fujikura U., Ferjani A., Ishikawa N., Tsukaya H., Large-scale histological analysis of leaf mutants using two simple leaf observation methods: Identification of novel genetic pathways governing the size and shape of leaves. Plant J. 48, 638–644 (2006). PubMed
Turnbull C. G. N., Booker J. P., Leyser H. M. O., Micrografting techniques for testing long-distance signalling in Arabidopsis. Plant J. 32, 255–262 (2002). PubMed
Kurihara D., Mizuta Y., Sato Y., Higashiyama T., ClearSee: A rapid optical clearing reagent for whole-plant fluorescence imaging. Development 142, 4168–4179 (2015). PubMed PMC
Svačinová J., et al. , A new approach for cytokinin isolation from Arabidopsis tissues using miniaturized purification: Pipette tip solid-phase extraction. Plant Methods 8, 17 (2012). PubMed PMC
Antoniadi I., et al. , Cell-type-specific cytokinin distribution within the Arabidopsis primary root apex. Plant Cell 27, 1955–1967 (2015). PubMed PMC