Reciprocal modulation of responses to nitrate starvation and hypoxia in roots and leaves of Arabidopsis thaliana

References

• Mu X, Chen Y. The physiological response of photosynthesis to nitrogen deficiency. Plant Physiol Biochem. 2021;158:76–7. doi:10.1016/j.plaphy.2020.11.019.
   PubMed Web of Science ®Google Scholar
• Kusano M, Fukushima A, Redestig H, Saito K. Metabolomic approaches toward understanding nitrogen metabolism in plants. J Exp Bot. 2011;62(4):1439–1453. doi:10.1093/jxb/erq417.
   PubMed Web of Science ®Google Scholar
• Anas M, Liao F, Verma KK, Sarwar MA, Mahmood A, Chen ZL, Li Q, Zeng XP, Liu Y, Li YR, et al. Fate of nitrogen in agriculture and environment: agronomic, eco-physiological and molecular approaches to improve nitrogen use efficiency. Biol Res. 2020;53(1):47. doi:10.1186/s40659-020-00312-4.
   PubMed Web of Science ®Google Scholar
• Ezin V, La Pena RD, Ahanchede A. Flooding tolerance of tomato genotypes during vegetative and reproductive stages. Braz J Plant Physiol. 2010;22(2):131–142. doi:10.1590/S1677-04202010000200007.
   Google Scholar
• Kim W, Iizumi T, Hosokawa N, Tanoue M, Hirabayashi Y. Flood impacts on global crop production: advances and limitations. Environ Res Lett. 2023;18(5):54007. doi:10.1088/1748-9326/accd85.
   Web of Science ®Google Scholar
• Voesenek LACJ, Bailey-Serres J. Flood adaptive traits and processes: an overview. New Phytol. 2015;206(1):57–73. doi:10.1111/nph.13209.
   PubMed Web of Science ®Google Scholar
• Diab H, Limami AM. Reconfiguration of N metabolism upon hypoxia stress and recovery: roles of alanine aminotransferase (AlaAT) and glutamate dehydrogenase (GDH). Plants (Basel). 2016;5(2):25. doi:10.3390/plants5020025.
   PubMedGoogle Scholar
• Drew MC. Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annu Rev Plant Physiol Plant Mol Biol. 1997;48(1):223–250. doi:10.1146/annurev.arplant.48.1.223.
   PubMedGoogle Scholar
• Mustroph A, Zanetti ME, Jang CJH, Holtan HE, Repetti PP, Galbraith DW, Girke T, Bailey-Serres J. Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in arabidopsis. Proc Natl Acad Sci U S A. 2009;106(44):18843–18848. doi:10.1073/pnas.0906131106.
   PubMed Web of Science ®Google Scholar
• Giuntoli B, Lee SC, Licausi F, Kosmacz M, Oosumi T, van Dongen JT, Bailey-Serres J, Perata P. A trihelix DNA binding protein counterbalances hypoxia-responsive transcriptional activation in arabidopsis. PLoS Biol. 2014;12(9):e1001950. doi:10.1371/journal.pbio.1001950.
   PubMed Web of Science ®Google Scholar
• Ismond KP, Dolferus R, De Pauw M, Dennis ES, Good AG. Enhanced low oxygen survival in Arabidopsis through increased metabolic flux in the fermentative pathway. Plant Physiol. 2003;132(3):1292–1302. doi:10.1104/pp.103.022244.
   PubMed Web of Science ®Google Scholar
• Hartman S, van Dongen N, Renneberg DMHJ, Welschen-Evertman RAM, Kociemba J, Sasidharan R, Voesenek LACJ. Ethylene differentially modulates hypoxia responses and tolerance across Solanum species. Plants (Basel). 2020;9(8):1022. doi:10.3390/plants9081022.
   PubMedGoogle Scholar
• Liu Z, Hartman S, van Veen H, Zhang H, Leeggangers HACF, Martopawiro S, Bosman F, de Deugd F, Su P, Hummel M, et al. Ethylene augments root hypoxia tolerance via growth cessation and reactive oxygen species amelioration. Plant Physiol. 2022;190(2):1365–1383. doi:10.1093/plphys/kiac245.
   PubMed Web of Science ®Google Scholar
• Hartman S. Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress. Nat Commun. 2019;10(1):4020. doi:10.1038/s41467-019-12045-4.
   PubMedGoogle Scholar
• Gibbs DJ, Lee SC, Md Isa N, Gramuglia S, Fukao T, Bassel GW, Correia CS, Corbineau F, Theodoulou FL, Bailey-Serres J, et al. Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature. 2011;479(7373):415–418. doi:10.1038/nature10534.
   PubMed Web of Science ®Google Scholar
• Licausi F, Kosmacz M, Weits DA, Giuntoli B, Giorgi FM, Voesenek LACJ, Perata P, van Dongen JT. Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature. 2011;479(7373):419–422. doi:10.1038/nature10536.
   PubMed Web of Science ®Google Scholar
• Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol. 2004;134(4):1683–1696. doi:10.1104/pp.103.033431.
   PubMed Web of Science ®Google Scholar
• Limami AM, Diab H, Lothier J. Nitrogen metabolism in plants under low oxygen stress. Planta. 2014;239(3):531–541. doi:10.1007/s00425-013-2015-9.
   PubMed Web of Science ®Google Scholar
• Narsai R, Rocha M, Geigenberger P, Whelan J, van Dongen JT. Comparative analysis between plant species of transcriptional and metabolic responses to hypoxia. New Phytol. 2011;190(2):472–487. doi:10.1111/j.1469-8137.2010.03589.x.
   PubMed Web of Science ®Google Scholar
• Oliveira HC, Sodek L. Effect of oxygen deficiency on nitrogen assimilation and amino acid metabolism of soybean root segments. Amino Acids. 2013;44(2):743–755. doi:10.1007/s00726-012-1399-3.
   PubMed Web of Science ®Google Scholar
• Rocha M, Licausi F, Araújo WL, Nunes-Nesi A, Sodek L, Fernie AR, van Dongen JT. Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of lotus japonicus. Plant Physiol. 2010;152(3):1501–1513. doi:10.1104/pp.109.150045.
   PubMed Web of Science ®Google Scholar
• Manoli A, Begheldo M, Genre A, Lanfranco L, Trevisan S, Quaggiotti S. NO homeostasis is a key regulator of early nitrate perception and root elongation in maize. J Exp Bot. 2014;65(1):185–200. doi:10.1093/jxb/ert358.
   PubMed Web of Science ®Google Scholar
• Trevisan S, Manoli A, Quaggiotti S. NO signaling is a key component of the root growth response to nitrate in zea mays L. Plant Signal Behav. 2014;9(3):e28290. doi:10.4161/psb.28290.
   PubMedGoogle Scholar
• Liu B, Rennenberg H, Kreuzwieser J. Hypoxia induces stem and leaf nitric oxide (NO) emission from poplar seedlings. Planta. 2015;241(3):579–89. doi:10.1007/s00425-014-2198-8.
   PubMed Web of Science ®Google Scholar
• Norén H, Svensson P, Andersson B. A convenient and versatile hydroponic cultivation system for Arabidopsis thaliana. Physiol Plant. 2004;121(3):343–348. doi:10.1111/j.0031-9317.2004.00350.x.
   Web of Science ®Google Scholar
• Balazadeh S, Schildhauer J, Araújo WL, Munné-Bosch S, Fernie AR, Proost S, Humbeck K, Mueller-Roeber B. Reversal of senescence by N resupply to N-starved Arabidopsis thaliana: transcriptomic and metabolomic consequences. J Exp Bot. 2014;65(14):3975–3992. doi:10.1093/jxb/eru119.
   PubMed Web of Science ®Google Scholar
• Arteca RN, Arteca JM. A novel method for growing Arabidopsis thaliana plantshydroponically. Physiol Plant. 2000;108(2):188–193. doi:10.1034/j.1399-3054.2000.108002188.x.
   Web of Science ®Google Scholar
• Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2010;3(6):1101–1108. PMID: 18546601. doi: 10.1038/nprot.2008.73.
   Web of Science ®Google Scholar
• Arvidsson S, Kwasniewski M, Riaño-Pachón DM, Mueller-Roeber B. QuantPrime–a flexible tool for reliable high-throughput primer design for quantitative PCR. BMC Bioinform. 2008;9(1):465. doi:10.1186/1471-2105-9-465.
   PubMedGoogle Scholar
• Park BS, Song JT, Seo HS. Arabidopsis nitrate reductase activity is stimulated by the E3 SUMO ligase AtSIZ1. Nat Commun. 2011;2(1):400. doi:10.1038/ncomms1408.
   PubMedGoogle Scholar
• Zheng D, Han X, An YI, Guo H, Xia X, Yin W. The nitrate transporter NRT2.1 functions in the ethylene response to nitrate deficiency in arabidopsis. Plant, Cell & Environ. 2013;36(7):1328–1337. doi:10.1111/pce.12062.
   PubMed Web of Science ®Google Scholar
• Hinz M, Wilson IW, Yang J, Buerstenbinder K, Llewellyn D, Dennis ES, Sauter M, Dolferus R. Arabidopsis RAP2.2: an ethylene response transcription factor that is important for hypoxia survival. Plant Physiol. 2010;153(2):757–772. doi:10.1104/pp.110.155077.
   PubMed Web of Science ®Google Scholar
• Safavi-Rizi V, Herde M, Stöhr C. RNA-Seq reveals novel genes and pathways associated with hypoxia duration and tolerance in tomato root. Sci Rep. 2020;10(1):1692. doi:10.1038/s41598-020-57884-0.
   PubMed Web of Science ®Google Scholar
• Giuntoli B, Licausi F, van Veen H, Perata P. Functional balancing of the hypoxia regulators RAP2.12 and HRA1 takes place in vivo in Arabidopsis thaliana plants. Front Plant Sci. 2017;8:591. doi:10.3389/fpls.2017.00591.
   PubMed Web of Science ®Google Scholar
• Licausi F, Van Dongen JT, Giuntoli B, Novi G, Santaniello A, Geigenberger P, Perata P. HRE1 and HRE2, two hypoxia-inducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana. Plant J. 2010;62(2):302–315. doi:10.1111/j.1365-313X.2010.04149.x.
   PubMed Web of Science ®Google Scholar
• Wang R, Xing X, Crawford N. Nitrite acts as a transcriptome signal at micromolar concentrations in Arabidopsis roots. Plant Physiol. 2007;145(4):1735–1745. doi:10.1104/pp.107.108944.
   PubMed Web of Science ®Google Scholar
• Dordas C, Hasinoff BB, Igamberdiev AU, Manac’h N, Rivoal J, Hill RD. Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. Plant J. 2003;35(6):763–770. doi:10.1046/j.1365-313X.2003.01846.x.
   PubMed Web of Science ®Google Scholar
• Hebelstrup KH, van Zanten M, Mandon J, Voesenek LACJ, Harren FJM, Cristescu SM, Møller IM, Mur LAJ. Haemoglobin modulates NO emission and hyponasty under hypoxia-related stress in Arabidopsis thaliana. J Exp Bot. 2012;63(15):5581–5591. doi:10.1093/jxb/ers210.
   PubMed Web of Science ®Google Scholar
• Igamberdiev AU. Nitrate, NO and haemoglobin in plant adaptation to hypoxia: an alternative to classic fermentation pathways. J Exp Bot. 2004;55(408):2473–2482. doi:10.1093/jxb/erh272.
   PubMed Web of Science ®Google Scholar
• Hunt PW, Klok EJ, Trevaskis B, Watts RA, Ellis MH, Peacock WJ, Dennis ES. Increased level of hemoglobin 1 enhances survival of hypoxic stress and promotes early growth in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2002;99(26):17197–17202. doi:10.1073/pnas.212648799.
   PubMed Web of Science ®Google Scholar
• Mira MM, Hill RD, Stasolla C. Phytoglobins improve hypoxic root growth by alleviating apical meristem cell death. Plant Physiol. 2016;172(3):2044–2056. doi:10.1104/pp.16.01150.
   PubMed Web of Science ®Google Scholar