Nitrate transporter NRT1.1 and anion channel SLAH3 form a functional unit to regulate nitrate-dependent alleviation of ammonium toxicity.
NRT1.1
SLAH3
ammonium toxicity
nitrate
rhizosphere acidification
Journal
Journal of integrative plant biology
ISSN: 1744-7909
Titre abrégé: J Integr Plant Biol
Pays: China (Republic : 1949- )
ID NLM: 101250502
Informations de publication
Date de publication:
Apr 2022
Apr 2022
Historique:
received:
15
01
2022
accepted:
27
02
2022
pubmed:
2
3
2022
medline:
20
4
2022
entrez:
1
3
2022
Statut:
ppublish
Résumé
Ammonium (NH
Substances chimiques
Ammonium Compounds
0
Anion Transport Proteins
0
Anions
0
Arabidopsis Proteins
0
Ion Channels
0
NRT1.1 protein, Arabidopsis
0
Nitrate Transporters
0
Nitrates
0
Plant Proteins
0
SLAH3 protein, Arabidopsis
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
942-957Subventions
Organisme : National Natural Science Foundation of China
Organisme : 111 Project
Organisme : Fundamental Research Funds for the Central Universities
Informations de copyright
© 2022 The Authors. Journal of Integrative Plant Biology published by John Wiley & Sons Australia, Ltd on behalf of Institute of Botany, Chinese Academy of Sciences.
Références
Bittsanszky, A., Pilinszky, K., Gyulai, G., and Komives, T. (2015). Overcoming ammonium toxicity. Plant Sci. 231: 184-190.
Bloom, A.J., Burger, M., Asensio, J.S.R., and Cousins, A.B. (2010). Carbon dioxide enrichment inhibits nitrate assimilation in wheat and Arabidopsis. Science 328: 899-903.
Bouguyon, E., Brun, F., Meynard, D., Kubes, M., Pervent, M., Leran, S., Lacombe, B., Krouk, G., Guiderdoni, E., Zazimalova, E., Hoyerova, K., Nacry, P., and Gojon, A. (2015). Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nat. Plants 1: 15015.
Breemen, N.V., Driscoll, C.T., and Mulder, J. (1984). Acidic deposition and internal proton sources in acidification of soils and waters. Nature 307: 599-604.
Britto, D.T., and Kronzucker, H.J. (2002). NH4+ toxicity in higher plants: A critical review. J. Plant Physiol. 159: 567-584.
Britto, D.T., Siddiqi, M.Y., Glass, A.D.M., and Kronzucker, H.J. (2001). Futile transmembrane NH4+ cycling: A cellular hypothesis to explain ammonium toxicity in plants. Proc. Natl. Acad. Sci. U.S.A 98: 4255-4258.
Chen, L., and Liao, H. (2017). Engineering crop nutrient efficiency for sustainable agriculture. J. Integr. Plant Biol. 59: 710-735.
Coleto, I., Bejarano, I., Marin-Pena, A.J., Medina, J., Rioja, C., Burow, M., and Marino, D. (2021). Arabidopsis thaliana transcription factors MYB28 and MYB29 shape ammonium stress responses by regulating Fe homeostasis. New Phytol. 229: 1021-1035.
Du, W., Zhang, Y., Si, J., Zhang, Y., Fan, S., Xia, H., and Kong, L. (2021). Nitrate alleviates ammonium toxicity in wheat (Triticum aestivum L.) by regulating tricarboxylic acid cycle and reducing rhizospheric acidification and oxidative damage. Plant Signal. Behav. 9: 1991687.
Escobar, M.A., Geisler, D.A., and Rasmusson, A.G. (2006). Reorganization of the alternative pathways of the Arabidopsis respiratory chain by nitrogen supply: Opposing effects of ammonium and nitrate. Plant J. 45: 775-788.
Esteban, R., Ariz, I., Cruz, C., and Moran, J.F. (2016). Mechanisms of ammonium toxicity and the quest for tolerance. Plant Sci. 248: 92-101.
Fan, W., Lou, H.Q., Gong, Y.L., Liu, M.Y., Cao, M.J., Liu, Y., Yang, J.L., and Zheng, S.J. (2015). Characterization of an inducible C2H2-type zinc finger transcription factor VuSTOP1 in rice bean (Vigna umbellata) reveals differential regulation between low pH and aluminum tolerance mechanisms. New Phytol. 208: 456-468.
Fang, X.Z., Tian, W.H., Liu, X.X., Lin, X.Y., Jin, C.W., and Zheng, S.J. (2016). Alleviation of proton toxicity by nitrate uptake specifically depends on nitrate transporter 1.1 in Arabidopsis. New Phytol. 211: 149-158.
Gazzarrini, S., Lejay, L., Gojon, A., Ninnemann, O., Frommer, W.B., and von Wirén, N. (1999). Three functional transporters for constitutive, diurnally regulated, and starvation-induced uptake of ammonium into Arabidopsis roots. Plant Cell 11: 937-948.
Gerendás, J., Zhu, Z., Bendixen, R., Ratcliffe, R.G., and Sattelmacher, B. (1997). Physiological and biochemical processes related to ammonium toxicity in higher plants. J. Plant Nutr. Soil Sci. 160: 239-251.
Hachiya, T., Inaba, J., Wakazaki, M., Sato, M., Toyooka, K., Miyagi, A., Kawai-Yamada, M., Sugiura, D., Nakagawa, T., Kiba, T., Gojon, A., and Sakakibara, H. (2021). Excessive ammonium assimilation by plastidic glutamine synthetase causes ammonium toxicity in Arabidopsis thaliana. Nat. Commun. 12: 4944.
Hachiya, T., Mizokami, Y., Miyata, K., Tholen, D., Watanabe, C.K., and Noguchi, K. (2011). Evidence for a nitrate-independent function of the nitrate sensor NRT1.1 in Arabidopsis thaliana. J. Plant Res. 124: 425-430.
Hachiya, T., and Noguchi, K. (2011). Mutation of NRT1.1 enhances ammonium/low pH-tolerance in Arabiopsis thaliana. Plant Signal. Behav. 6: 706-708.
Hachiya, T., Watanabe, C.K., Fujimoto, M., Ishikawa, T., Takahara, K., Kawai-Yamada, M., Uchimiya, H., Uesono, Y., Terashima, I., and Noguchi, K. (2012). Nitrate addition alleviates ammonium toxicity without lessening ammonium accumulation, organic acid depletion and inorganic cation depletion in Arabidopsis thaliana shoots. Plant Cell Physiol. 53: 577-591.
Ho, C.H., Lin, S.H., Hu, H.C., and Tsay, Y.F. (2009). CHL1 functions as a nitrate sensor in plants. Cell 138: 1184-1194.
Hoffmann, A., Milde, S., Desel, C., Hümpel, A., Kaiser, H., Hammes, E., Piippo, M., Soitamo, A., Aro, E.M., and Gerendás, J. (2007). N form-dependent growth retardation of Arabidopsis thaliana seedlings as revealed from physiological and microarray studies. J. Plant Nutr. Soil Sci. 170: 87-97.
Huang, N.C., Chiang, C.S., Crawford, N.M., and Tsay, Y.F. (1996). CHL1 encodes a component of the low-affinity nitrate uptake system in Arabidopsis and shows cell type-specific expression in roots. Plant Cell 8: 2183-2191.
Iuchi, S., Koyama, H., Iuchi, A., Kobayashi, Y., Kitabayashi, S., Kobayashi, Y., Ikka, T., Hirayama, T., Shinozaki, K., and Kobayashi, M. (2007). Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. Proc. Natl. Acad. Sci. U.S.A. 104: 9900-9905.
Jian, S., Liao, Q., Song, H., Liu, Q., Lepo, J.E., Guan, C., Zhang, J., Ismail, A.M., and Zhang, Z. (2018). NRT1.1-related NH4+ toxicity is associated with a disturbed balance between NH4+ uptake and assimilation. Plant Physiol. 178: 1473-1488.
Kanwar, P., Sanyal, S.K., Mahiwal, S., Ravi, B., Kaur, K., Fernandes, J.L., Yadav, A.K., Tokas, I., Srivastava, A.K., Suprasanna, P., and Pandey, G.K. (2022). CIPK9 targets VDAC3 and modulates oxidative stress responses in Arabidopsis. Plant J. 109: 241-260.
Kobayashi, Y., Ohyama, Y., Kobayashi, Y., Ito, H., Iuchi, S., Fujita, M., Zhao, C.R., Tanveer, T., Ganesan, M., Kobayashi, M., and Koyama, H. (2014). STOP2 activates transcription of several genes for Al- and low pH-tolerance that are regulated by STOP1 in Arabidopsis. Mol. Plant 7: 311-322.
Kronzucker, H.J., Britto, D.T., Davenport, R.J., and Tester, M. (2001). Ammonium toxicity and the real cost of transport. Trends Plant Sci. 6: 335-337.
Lager, I., Andréasson, O., Dunbar, T.L., Andreasson, E., Escobar, M.A., and Rasmusson, A.G. (2010). Changes in external pH rapidly alter plant gene expression and modulate auxin and elicitor responses. Plant Cell Environ. 33: 1513-1528.
Lehmann, J., Jorgensen, M.E., Fratz, S., Muller, H.M., Kusch, J., Scherzer, S., Navarro-Retamal, C., Mayer, D., Bohm, J., Konrad, K.R., Terpitz, U., Dreyer, I., Mueller, T.D., Sauer, M., Hedrich, R., Geiger, D., and Maierhofer, T. (2021). Acidosis-induced activation of anion channel SLAH3 in the flooding-related stress response of Arabidopsis. Curr. Biol. 31: 3575-3585.
Li, B., Li, G., Kronzucker, H.J., Baluska, F., and Shi, W. (2014). Ammonium stress in Arabidopsis: Signaling, genetic loci, and physiological targets. Trends Plant Sci. 19: 107-114.
Liu, K., and Tsay, Y. (2003). Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J. 22: 1005-1013.
Liu, Y., and von Wiren, N. (2017). Ammonium as a signal for physiological and morphological responses in plants. J. Exp. Bot. 68: 2581-2592.
Nacry, P., Bouguyon, E., and Gojon, A. (2013). Nitrogen acquisition by roots: Physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil 370: 1-29.
Oldroyd, G.E., and Dixon, R. (2014). Biotechnological solutions to the nitrogen problem. Curr. Opin. Biotechnol. 26: 19-24.
Palmer, S.M., and Driscoll, C.T. (2002). Acidic deposition: Decline in mobilization of toxic aluminium. Nature 417: 242-243.
Parker, J.L., and Newstead, S. (2014). Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature 507: 68-72.
Patterson, K., Cakmak, T., Cooper, A., Lager, I., Rasmusson, A.G., and Escobar, M.A. (2010). Distinct signalling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. Plant Cell Environ. 33: 1486-1501.
Peccia, J., Haznedaroglu, B., Gutierrez, J., and Zimmerman, J.B. (2013). Nitrogen supply is an important driver of sustainable microalgae biofuel production. Trends Biotechnol. 31: 134-138.
Robertson, G.P., and Vitousek, P.M. (2009). Nitrogen in agriculture: Balancing the cost of an essential resource. Annu. Rev. Environ. Resour. 34: 97-125.
Roosta, H.R., and Schjoerring, J.K. (2007). Effects of ammonium toxicity on nitrogen metabolism and elemental profile of cucumber plants. J. Plant Nutr. 30: 1933-1951.
Sawaki, Y., Iuchi, S., Kobayashi, Y., Kobayashi, Y., Ikka, T., Sakurai, N., Fujita, M., Shinozaki, K., Shibata, D., Kobayashi, M., and Koyama, H. (2009). STOP1 regulates multiple genes that protect arabidopsis from proton and aluminum toxicities. Plant Physiol. 150: 281-294.
Stoddard, J.L., Jeffries, D.S., Lükewille, A., Clair, T.A., and Wilander, A. (1999). Regional trends in aquatic recovery from acidification in North America and Europe. Nature 401: 575-578.
Sun, D., Fang, X., Xiao, C., Ma, Z., Huang, X., Su, J., Li, J., Wang, J., Wang, S., Luan, S., and He, K. (2021). Kinase SnRK1.1 regulates nitrate channel SLAH3 engaged in nitrate-dependent alleviation of ammonium toxicity. Plant Physiol. 186: 731-749.
Sun, J., Bankston, J.R., Payandeh, J., Hinds, T.R., Zagotta, W.N., and Zheng, N. (2014). Crystal structure of the plant dual-affinity nitrate transporter NRT1.1. Nature 507: 73-77.
Sun, J., Chen, S., Dai, S., Wang, R., Li, N., Shen, X., Zhou, X., Lu, C., Zheng, X., Hu, Z., Zhang, Z., Song, J., and Xu, Y. (2009). NaCl-induced alternations of cellular and tissue ion fluxes in roots of salt-resistant and salt-sensitive poplar species. Plant Physiol. 149: 1141-1153.
Tegeder, M., and Masclaux-Daubresse, C. (2018). Source and sink mechanisms of nitrogen transport and use. New Phytol. 217: 35-53.
Tsay, Y.-F., Schroeder, J.I., Feldmann, K.A., and Crawford, N.M. (1993). The herbicide sensitivity gene CHL1 of arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72: 705-713.
Wang, F., Gao, J., Tian, Z., Liu, Y., Abid, M., Jiang, D., Cao, W., and Dai, T. (2016). Adaptation to rhizosphere acidification is a necessary prerequisite for wheat (Triticum aestivum L.) seedling resistance to ammonium stress. Plant Physiol. Biochem. 108: 447-455.
Wang, R., Tischner, R., Gutiérrez, R.A., Hoffman, M., Xing, X., Chen, M., Coruzzi, G., and Crawford, N.M. (2004). Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol. 136: 2512.
Wang, X., Feng, C., Tian, L., Hou, C., Tian, W., Hu, B., Zhang, Q., Ren, Z., Niu, Q., Song, J., Kong, D., Liu, L., He, Y., Ma, L., Chu, C., Luan, S., and Li, L. (2021). A transceptor-channel complex couples nitrate sensing to calcium signaling in Arabidopsis. Mol. Plant 14: 774-786.
Wang, Z.P., Xing, H.L., Dong, L., Zhang, H.Y., Han, C.Y., Wang, X.C., and Chen, Q.J. (2015). Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol. 16: 144.
Wu, W., Lin, Y., Chen, Q., Peng, W., Peng, J., Tian, J., Liang, C., and Liao, H. (2018). Functional conservation and divergence of soybean GmSTOP1 members in proton and aluminum tolerance. Front. Plant Sci. 9: 570.
Xie, Y., Mao, Y., Xu, S., Zhou, H., Duan, X., Cui, W., Zhang, J., and Xu, G. (2015). Heme-heme oxygenase 1 system is involved in ammonium tolerance by regulating antioxidant defence in Oryza sativa. Plant Cell Environ. 38: 129-143.
Xu, G., Fan, X., and Miller, A.J. (2012). Plant nitrogen assimilation and use efficiency. Annu. Rev. Plant Biol. 63: 153-182.
Xu, Q.F., Tsai, C.L., and Tsai, C.Y. (1992). Interaction of potassium with the form and amount of nitrogen nutrition on growth and nitrogen uptake of maize. J. Plant Nutr. 15: 23-33.
Ye, J.Y., Tian, W.H., Zhou, M., Zhu, Q.Y., Du, W.X., Zhu, Y.X., Liu, X.X., Lin, X.Y., Zheng, S.J., and Jin, C.W. (2021). STOP1 activates NRT1.1-mediated nitrate uptake to create a favorable rhizospheric pH for plant adaptation to acidity. Plant Cell 33: 3658-3674.
Yoo, S.D., Cho, Y.H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nat. Protoc. 2: 1565-1572.
Yuan, L., Loque, D., Kojima, S., Rauch, S., Ishiyama, K., Inoue, E., Takahashi, H., and Wiren, N. (2007). The organization of high-affinity ammonium uptake in Arabidopsis roots depends on the spatial arrangement and biochemical properties of AMT1-type transporters. Plant Cell 19: 2636-2652.
Zhao, L., and Wang, Y. (2017). Nitrate assay for plant tissues. Bio. Protoc. 7: e2029.
Zhao, X.Q., and Shen, R.F. (2018). Aluminum-nitrogen interactions in the soil-plant system. Front. Plant Sci. 9: 807.
Zheng, X., He, K., Kleist, T., Chen, F., and Luan, S. (2015). Anion channel SLAH3 functions in nitrate-dependent alleviation of ammonium toxicity in Arabidopsis. Plant Cell Environ. 38: 474-486.