Calcium signaling networks mediate nitrate sensing and responses in Arabidopsis

References

• Wang R, Tischner R, Gutiérrez RA, Hoffman M, Xing X, Chen M, Coruzzi G, Crawford NM. Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol. 2018;136:1–7. doi:10.1104/pp.104.044610.
   Google Scholar
• O’Brien JA, Vega A, Bouguyon E, Krouk G, Gojon A, Coruzzi G, Gutiérrez RA. Nitrate transport, sensing and responses in plants. Mol Plant. 2016;9:837–856. doi:10.1016/j.molp.2016.05.004.
   PubMed Web of Science ®Google Scholar
• Undurraga SF, Ibarra-Henriquez C, Fredes I, Alvarez JM, Gutierrez RA. Nitrate signaling and early responses in Arabidopsis roots. J Exp Bot. 2017;68:2541–2551. doi:10.1093/jxb/erx041.
   PubMed Web of Science ®Google Scholar
• Fredes I, Moreno S, Díaz FP, Gutiérrez RA. Nitrate signaling and the control of Arabidopsis growth and development. Curr Opin Plant Biol. 2018;47:112–118. doi:10.1016/j.pbi.2018.10.004.
   PubMed Web of Science ®Google Scholar
• Ye JY, Tian WH, Zhou M, Zhu QY, Jin CW. Improved plant nitrate status involves in flowering induction by extended photoperiod. Front Plant Sci. 2021:12. doi:10.3389/fpls.2021.629857.
   Web of Science ®Google Scholar
• 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(15):4480–4494. doi:10.1093/jxb/eraa242.
   PubMed Web of Science ®Google Scholar
• Sakuraba Y, Chaganzhana, Mabuchi A, Iba K, Yanagisawa S. Enhanced NRT1.1/NPF6.3 expression in shoots improves growth under nitrogen deficiency stress in arabidopsis. Commun Biol. 2021;4(1). doi:10.1038/s42003-021-01775-1.
   PubMed Web of Science ®Google Scholar
• Ho CH, Lin SH, Hu HC, Tsay YF. CHL1 functions as a nitrate sensor in plants. Cell. 2009;138:1184–1194. doi:10.1016/j.cell.2009.07.004.
   PubMed Web of Science ®Google Scholar
• Bouguyon E, Perrine-Walker F, Pervent M, Rochette J, Cuesta C, Benkova E, Martinière A, Bach L, Krouk G, Gojon A, et al. Nitrate controls root development through post-transcriptional regulation of the NRT1.1/NPF6.3 transporter/sensor. Plant Physiol. 2016;172:1237–1248. doi:10.1104/pp.16.01047.
   PubMed Web of Science ®Google Scholar
• Leran S, Edel KH, Pervent M, Hashimoto K, Corratgé-Faillie C, Offenborn JN, Tillard P, Gojon A, Kudla J, Lacombe B. Nitrate sensing and uptake in Arabidopsis are enhanced by ABI2, a phosphatase inactivated by the stress hormone abscisic acid. Sci Signal. 2015;8:ra43. doi:10.1126/scisignal.aaa4829.
   PubMed Web of Science ®Google Scholar
• Vidal EA, Álvarez JM, Moyano TC, Gutiérrez RA. Transcriptional networks in the nitrate response of Arabidopsis thaliana. Curr Opin Plant Biol. 2015;27:125–132. doi:10.1016/j.pbi.2015.06.010.
   PubMed Web of Science ®Google Scholar
• Konishi M, Yanagisawa S. Arabidopsis NIN-like transcription factors have a central role in nitrate signaling. Nat Commun. 2013;4:1617–1625. doi:10.1038/ncomms2621.
   PubMed Web of Science ®Google Scholar
• 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;4:1713–1721. doi:10.1038/ncomms2650.
   PubMed Web of Science ®Google Scholar
• Guan P, Ripoll JJ, Wang R, Vuong L, Bailey-Steinitz LJ, Ye D, Crawford NM. Interacting TCP and NLP transcription factors control plant responses to nitrate availability. Proc Natl Acad Sci USA. 2017;114:2419–2424. doi:10.1073/pnas.1615676114.
   PubMed Web of Science ®Google Scholar
• Zhong L, Chen D, Min D, Li W, Xu Z, Zhou Y, Li L, Chen M, Ma Y. AtTGA4, a bZIP transcription factor, confers drought resistance by enhancing nitrate transport and assimilation in Arabidopsis thaliana. Biochem Biophys Res Commun. 2015;457:433–439. doi:10.1016/j.bbrc.2015.01.009.
   PubMed Web of Science ®Google Scholar
• Canales J, Contreras-López O, Álvarez JM, Gutiérrez RA. Nitrate induction of root hair density is mediated by TGA1/TGA4 and CPC transcription factors in Arabidopsis thaliana. Plant J. 2017;92:305–316. doi:10.1111/tpj.13656.
   PubMed Web of Science ®Google Scholar
• Guan P, Wang R, Nacry P, Breton G, Kay SA, Pruneda-Paz JL, Davani A, Crawford NM. Nitrate foraging by Arabidopsis roots is mediated by the transcription factor TCP20 through the systemic signaling pathway. Proc Natl Acad Sci USA. 2014;111:15267–15272. doi:10.1073/pnas.1411375111.
   PubMed Web of Science ®Google Scholar
• Alvarez JM, Riveras E, Vidal EA, Gras DE, Contreras-López O, Tamayo KP, 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. 2014;80:1–13. doi:10.1111/tpj.12618.
   PubMed Web of Science ®Google Scholar
• Hepler PK. Calcium: a central regulator of plant growth and development. Plant Cell. 2005;17:2142–2155. doi:10.1105/tpc.105.032508.
   PubMed Web of Science ®Google Scholar
• Clapham DE. Calcium signaling. Cell. 2007;131:1047–1058. doi:10.1016/j.cell.2007.11.028.
   PubMed Web of Science ®Google Scholar
• Batistič O, Kudla J. Analysis of calcium signaling pathways in plants. Biochim Biophys Acta. 2012;1820:1283–1293. doi:10.1016/j.bbagen.2011.10.012.
   PubMed Web of Science ®Google Scholar
• Iwano M, Ito K, Fujii S, Kakita M, Asano-Shimosato H, Igarashi M, Kaothien-Nakayama P, Entani T, Kanatani A, Takehisa M, et al. Calcium signaling mediates self-incompatibility response in the Brassicaceae. Nat Plants. 2015;1:15128. doi:10.1038/nplants.2015.128.
   PubMed Web of Science ®Google Scholar
• Denninger P, Bleckmann A, Lausser A, Vogler F, Ott T, Ehrhardt DW. Male-female communication triggers calcium signatures during fertilization in Arabidopsis. Nat Commun. 2014;5:4645. doi:10.1038/ncomms5645.
   PubMed Web of Science ®Google Scholar
• Charpentier M, Sun J, Vaz Martins T, Radhakrishnan GV, Findlay K, Soumpourou E, Thouin J, Very AA, Sanders D, Morris RJ, et al. Nuclear localized cyclic nucleotide-gated channels mediate symbiotic calcium oscillations. Science. 2016;352:1102–1105. doi:10.1126/science.aae0109.
   PubMed Web of Science ®Google Scholar
• Chaves-Sanjuan A, Sanchez-Barrena MJ, Gonzalez-Rubio JM, Moreno M, Ragel P, Jimenez M, Pardo JM, Martinez-Ripoll M, Quintero FJ, Albert A. Structural basis of the regulatory mechanism of the plant CIPK family of protein kinases controlling ion homeostasis and abiotic stress. Proc Natl Acad Sci USA. 2014;111:4532–4541. doi:10.1073/pnas.1407610111.
   Web of Science ®Google Scholar
• Kudla J, Becker D, Grill E, Hedrich R, Hippler M, Kummer U, Parniske M, Romeis T, Schumacher K. Advances and current challenges in calcium signaling. New Phytol. 2018;218:414–431. doi:10.1111/nph.14966.
   PubMed Web of Science ®Google Scholar
• Choi WG, Hilleary R, Swanson SJ, Kim SH, Gilroy S. Rapid, long-distance electrical and calcium signaling in plants. Annu Rev Plant Biol. 2016;67:287–307. doi:10.1146/annurev-arplant-043015-112130.
   PubMed Web of Science ®Google Scholar
• Costa A, Kudla J. Colorful insights: advances in imaging drive novel breakthroughs in Ca2+ signaling. Mol Plant. 2015;8:352–355. doi:10.1016/j.molp.2014.11.020.
   PubMed Web of Science ®Google Scholar
• Guo H, Feng P, Chi W, Sun X, Xu X, Li Y, Ren D, Lu C, David Rochaix J, Leister D, et al. Plastid-nucleus communication involves calcium-modulated MAPK signalling. Nat Commun. 2016;7:12173. doi:10.1038/ncomms12173.
   PubMed Web of Science ®Google Scholar
• Edel KH, Kudla J. Increasing complexity and versatility: how the calcium signaling toolkit was shaped during plant land colonization. Cell Calcium. 2015;57:231–246. doi:10.1016/j.ceca.2014.10.013.
   PubMed Web of Science ®Google Scholar
• Sakakibara H, Kobayashi K, Deji A, Sugiyama T. Partial characterization of the signaling pathway for the nitrate-dependent expression of genes for nitrogen-assimilatory enzymes using detached maize leaves. Plant Cell Physiol. 1997;38:837–843. doi:10.1093/oxfordjournals.pcp.a029242.
   Web of Science ®Google Scholar
• Sueyoshi K, Mitsuyama T, Sugimoto T, Kleinhofs A, Warner RL, Oji Y. Effects of inhibitors for signaling components on the expression of the genes for nitrate reductase and nitrite reductase in excised barley leaves. Soil Sci Plant Nutr. 1999;45:1015–1019. doi:10.1080/00380768.1999.10414353.
   Web of Science ®Google Scholar
• Riveras E, Alvarez JM, Vidal EA, Oses C, Vega A, Gutiérrez RA. The calcium ion is a second messenger in the nitrate signaling pathway of Arabidopsis. Plant Physiol. 2015;169:1397–1404. doi:10.1104/pp.15.00961.
   PubMed Web of Science ®Google Scholar
• Gao QF, Gu LL, Wang HQ, Fei CF, Fang X, Hussain J, Sun SJ, Dong JY, Liu H, Wang YF. Cyclic nucleotide-gated channel 18 is an essential Ca2+ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis. Proc Natl Acad Sci USA. 2016;113:3096–3101. doi:10.1073/pnas.1524629113.
   PubMed Web of Science ®Google Scholar
• Zhang S, Pan Y, Tian W, Dong M, Zhu H, Luan S, Li L. Arabidopsis CNGC14 mediates calcium influx required for tip growth in root hairs. Mol Plant. 2017;10:1004–1006. doi:10.1016/j.molp.2017.02.007.
   PubMed Web of Science ®Google Scholar
• Tian W, Hou C, Ren J, Wang C, Zhao F, Dahlbeck D, Hu S, Zhang L, Niu Q, Li L, et al. A calmodulin-gated calciumchannel links pathogen patterns to plant immunity. Nature. 2019;572:131–135. doi:10.1038/s41586-019-1413-y.
   PubMed Web of Science ®Google Scholar
• Liu KH, Tsay YF. Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J. 2003;22:1005–1013. doi:10.1093/emboj/cdg118.
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1038/nplants.2015.15.
   PubMed Web of Science ®Google Scholar
• Wang X, Feng C, Tian L, Hou C, Tian W, Hu B, Zhang Q, Ren ZJ, Niu Q, Song JL, et al. A transceptor-channel complex couples nitrate sensing to calcium signaling in Arabidopsis. Mol Plant. 2021;14:774–786. doi:10.1016/j.molp.2021.02.005.
   PubMed Web of Science ®Google Scholar
• Mao J, Manik S, Shi S, Chao J, Jin Y, Wang Q, Liu H. Mechanisms and physiological roles of the cbl-cipk networking system in Arabidopsis thaliana. Genes. 2016;7(9):62. doi:10.3390/genes7090062.
   Web of Science ®Google Scholar
• Saito S, Uozumi N. Calcium-regulated phosphorylation systems controlling uptake and balance of plant nutrients. Front Plant Sci. 2020:11. doi:10.3389/fpls.2020.00044.
   PubMed Web of Science ®Google Scholar
• Hashimoto K, Kudla J. Calcium decoding mechanisms in plants. Biochimie. 2011;93:2054–2059. doi:10.1016/j.biochi.2011.05.019.
   PubMed Web of Science ®Google Scholar
• Dong QY, Bai B, Almutairi BO, Kudla J. Emerging roles of the cbl-cipk calcium signaling network as key regulatory hub in plant nutrition. J Plant Physiol. 2021;257:153335. doi:10.1016/j.jplph.2020.153335.
   PubMed Web of Science ®Google Scholar
• Ma Q, Tang RJ, Zheng XJ, Wang SM, Luan S. The calcium sensor CBL7 modulates plant responses to low nitrate in Arabidopsis. Biochem Biophys Res Commun. 2015;468:59–65. doi:10.1016/j.bbrc.2015.10.164.
   PubMed Web of Science ®Google Scholar
• Yang J, Deng X, Wang X, Wang JZ, Du SY, Li YS. The calcium sensor oscbl1 modulates nitrate signaling to regulate seedling growth in rice. PLoS ONE. 2019;14(11):e0224962. doi:10.1371/journal.pone.0224962.
   PubMed Web of Science ®Google Scholar
• Krouk G. Nitrate signaling: calcium bridges the nitrate gap. Nat Plants. 2017;3:17095. doi:10.1038/nplants.2017.95.
   PubMed Web of Science ®Google Scholar
• Vert G, Chory J. A toggle switch in plant nitrate uptake. Cell. 2009;138:1064–1066. doi:10.1016/j.cell.2009.09.005.
   PubMed Web of Science ®Google Scholar
• Hu HC, Wang YY, Tsay YF. AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J. 2009;57:264–278. doi:10.1111/j.1365-313X.2008.03685.x.
   PubMed Web of Science ®Google Scholar
• Tuteja N, Sopory SK. Plant signaling in stress: g-protein coupled receptors, heterotrimeric G-proteins and signal coupling via phospholipases. Plant Signal Behav. 2008:379–386. doi:10.4161/psb.3.2.5303.
   Google Scholar
• Rupwate SD, Rajasekharan R. Plant phosphoinositide-specific phospholipase C: an insight. Plant Signal Behav. 2012;7:1281–1283. doi:10.4161/psb.21436.
   PubMed Web of Science ®Google Scholar
• Singh A, Bhatnagar N, Pandey A, Pandey GK. Plant phospholipase C family: regulation and functional role in lipid signaling. Cell Calcium. 2015;58:139–146. doi:10.1016/j.ceca.2015.04.003.
   PubMed Web of Science ®Google Scholar
• Schulz P, Herde M, Romeis T. Calcium-dependent protein kinases: hubs in plant stress signaling and development. Plant Physiol. 2013;163(2):523–530. doi:10.1104/pp.113.222539.
   PubMed Web of Science ®Google Scholar
• Kudla J, Batistic O, Hashimoto K. Calcium signals: the lead currency of plant information processing. Plant Cell. 2010;22:541–563. doi:10.1105/tpc.109.072686.
   PubMed Web of Science ®Google Scholar
• Boudsocq M, Sheen J. CDPKs in immune and stress signaling. Trends Plant Sci. 2013;18(1):30–40. doi:10.1016/j.tplants.2012.08.008.
   PubMed Web of Science ®Google Scholar
• Shi S, Li S, Muhammad A, Mao J, Xu D, Ullah Z, Liu GS, Wang Q, Liu HB. The Arabidopsis calcium-dependent protein kinases (CDPKs) and their roles in plant growth regulation and abiotic stress responses. Int J Mol Sci. 2018;19(7):1900. doi:10.3390/ijms19071900.
   Web of Science ®Google Scholar
• Liu KH, Niu Y, Konishi M, Wu Y, Du H, Sun CH, Li L. Discovery of nitrate-cpk-nlp signalling in central nutrient-growth networks. Nature. 2017;545(7654):311–316. doi:10.1038/nature22077.
   PubMed Web of Science ®Google Scholar
• Zhang H, Forde BG. An arabidopsis mads box gene that controls nutrient-induced changes in root architecture. Science. 1998;279(5349):407–409. doi:10.1126/science.279.5349.407.
   PubMed Web of Science ®Google Scholar
• Gan Y, Bernreiter A, Filleur S, Abram B, Forde BG. 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. 2012;53(6):1003–1016. doi:10.1093/pcp/pcs050.
   PubMed Web of Science ®Google Scholar
• Zhang X, Cui Y, Yu M, Su B, Gong W, Baluška F, Komis G, Šamaj J, Shan X, Lin J. Phosphorylation-mediated dynamics of nitrate transceptor NRT1.1 regulate auxin flux and nitrate signaling in lateral root growth. Plant Physiol. 2019;181:480–498. doi:10.1104/pp.19.00346.
   PubMed Web of Science ®Google Scholar
• Wang C, Zhang W, Li Z, Li Z, Bi Y, Crawford NM, Wang Y. FIP1 plays an important role in nitrate signaling and regulates cipk8 and cipk23 expression in Arabidopsis. Front Plant Sci. 2018;9:593. doi:10.3389/fpls.2018.00593.
   PubMed Web of Science ®Google Scholar
• Dodd AN, Kudla J, Sanders D. The language of calcium signaling. Annu Rev Plant Biol. 2010;61:593–620. doi:10.1146/annurev-arplant-070109-104628.
   PubMed Web of Science ®Google Scholar
• Mossaid I, Fahrenkrog B. Complex commingling: nucleoporins and the spindle assembly checkpoint. Cells. 2015;4(4):706–725. doi:10.3390/cells4040706.
   PubMed Web of Science ®Google Scholar
• Ristova D, Carré C, Pervent M, Medici A, Kim GJ, Scalia D, Ruffel S, Birnbaum KD, Lacombe B, Busch W, et al. Combinatorial interaction network of transcriptomic and phenotypic responses to nitrogen and hormones in the Arabidopsis thaliana root. Sci Sig. 2016;9:rs13. doi:10.1126/scisignal.aaf2768.
   PubMed Web of Science ®Google Scholar
• Edel KH, Kudla. Integration of calcium and ABA signaling. Curr Opin in Plant Biol. 2016;33:83–91. doi:10.1016/j.pbi.2016.06.010.
   PubMed Web of Science ®Google Scholar
• Efeyan A, Comb WC, Sabatini DM. Nutrient-sensing mechanisms and pathways. Nature. 2015;517:302. doi:10.1038/nature14190.
   PubMed Web of Science ®Google Scholar
• Sheen J. Ca2+-dependent protein kinases and stress signal transduction in plants. Science. 1996;274:1900–1902. doi:10.1126/science.274.5294.1900.
   PubMed Web of Science ®Google Scholar
• Wang W, Hu B, Li A, Chu C. NRT1.1s in plants: functions beyond nitrate transport. Front Plant Sci. 2020;71(15):4373–4379. doi:10.1093/jxb/erz554.
   Google Scholar
• Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, Mounier E, Hoyerova K, Tillard P, Leon S, Ljung K. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev Cell. 2010;18:927–937. doi:10.1016/j.devcel.2010.05.008.
   PubMed Web of Science ®Google Scholar