Anion channel SLAH3 functions in nitrate-dependent alleviation of ammonium toxicity in Arabidopsis

Plant Cell and Environment

Volumn 38, Issue 3, 2015, Pages 474-486

  Zheng, Xiaojiang ^a,b,c   He, Kai ^b,d   Kleist, Thomas ^b   Chen, Fang ^a   Luan, Sheng ^b,c  

^a SICHUAN UNIVERSITY   (China)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NANJING UNIVERSITY   (China)

^d LANZHOU UNIVERSITY   (China)

Author keywords

Growth; Nitrogen; Nutrients

Indexed keywords

ARABIDOPSIS;

AMMONIUM DERIVATIVE; ANION; ARABIDOPSIS PROTEIN; ION CHANNEL; NITRIC ACID DERIVATIVE; SLAH3 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; DRUG EFFECTS; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY; PLANT ROOT; REPORTER GENE;

AMMONIUM COMPOUNDS; ANIONS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENES, REPORTER; ION CHANNELS; MUTATION; NITRATES; PLANT ROOTS;

EID: 84922742338     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12389     Document Type: Article

References (51)

1. - fluxes in roots of barley seedlings. Plant Physiology 108, 727-734.
2. + toxicity in higher plants: a critical review. Journal of Plant Physiology 159, 567-584.
3. Britto D.T. & Kronzucker H.J. (2005) Nitrogen acquisition, PEP carboxylase, and cellular pH homeostasis: new views on old paradigms. Plant, Cell and Environment 28, 1396-1409.
4. + cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proceedings of the National Academy of Sciences of the United States of America 98, 4255-4258.
5. Chen Y., Hu L., Punta M., Bruni R., Hillerich B., Kloss B. Hendrickson W.A. (2010) Homologue structure of the SLAC1 anion channel for closing stomata in leaves. Nature 467, 1074-1080.
6. Chiu C.C., Lin C.S., Hsia A.P., Su R.C., Lin H.L. & Tsay Y.F. (2004) Mutation of a nitrate transporter, AtNRT1:4, results in a reduced petiole nitrate content and altered leaf development. Plant & Cell Physiology 45, 1139-1148.
7. Clough S.J. & Bent A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735-743.
8. Davies D.D. (1986) The fine control of cytosolic pH. Physiologia Plantarum 67, 702-706.
9. Demir F., Horntrich C., Blachutzik J.O., Scherzer S., Reinders Y., Kierszniowska S. Kreuzer I. (2013) Arabidopsis nanodomain-delimited ABA signaling pathway regulates the anion channel SLAH3. Proceedings of the National Academy of Sciences of the United States of America 110, 8296-8301.
10. Domene L. & Ayres R.U. (2001) Nitrogen's role in industrial systems. Journal of Industrial Ecology 5, 77-103.
11. Escobar M.A., Geisler D.A. & Rasmusson A.G. (2006) Reorganization of the alternative pathways of the Arabidopsis respiratory chain by nitrogen supply: opposing effects of ammonium and nitrate. The Plant Journal 45, 775-788.
12. Garnica M., Houdusse F., Zamarreño A.M. & Garcia-Mina J.M. (2009) Nitrate modifies urea root uptake and assimilation in wheat seedlings. Journal of the Science of Food and Agriculture 89, 55-62.
13. Geiger D., Scherzer S., Mumm P., Stange A., Marten I., Bauer H. Hedrich R. (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proceedings of the National Academy of Sciences of the United States of America 106, 21425-21430.
14. Geiger D., Maierhofer T., Al-Rasheid K.A., Scherzer S., Mumm P., Liese A. Hedrich R. (2011) Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Science Signaling 4, ra32.
15. Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W. & Gascuel O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of phyml 3.0. Systematic Biology 59, 307-321.
16. Guo J.H., Liu X.J., Zhang Y., Shen J.L., Han W.X., Zhang W.F. Zhang F.S. (2010) Significant acidification in major Chinese croplands. Science 327, 1008-1010.
17. Gutermuth T., Lassig R., Portes M.T., Maierhofer T., Romeis T., Borst J.W. Konrad K.R. (2013) Pollen tube growth regulation by free anions depends on the interaction between the anion channel SLAH3 and calcium-dependent protein kinases CPK2 and CPK20. The Plant Cell 25, 4525-4543.
18. Hachiya T., Watanabe C.K., Fujimoto M., Ishikawa T., Takahara K., Kawai-Yamada M. 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 Physiology 53, 577-591.
19. Ho C.H., Lin S.H., Hu H.C. & Tsay Y.F. (2009) CHL1 functions as a nitrate sensor in plants. Cell 138, 1184-1194.
20. Hrabak E.M., Chan C.W., Gribskov M., Harper J.F., Choi J.H., Halford N. Harmon A.C. (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiology 132, 666-680.
21. Hu H.C., Wang Y.Y. & Tsay Y.F. (2009) AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. The Plant Journal 57, 264-278.
22. Huang N.C., Liu K.H., Lo H.J. & Tsay Y.F. (1999) Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake. The Plant Cell 11, 1381-1392.
23. Jefferson R.A., Kavanagh T.A. & Bevan M.W. (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. The EMBO Journal 6, 3901-3907.
24. Katoh K., Misawa K., Kuma K.I. & Miyata T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059-3066.
25. Kiba T., Feria-Bourrellier A.B., Lafouge F., Lezhneva L., Boutet-Mercey S., Orsel M. Krapp A. (2012) The Arabidopsis nitrate transporter NRT2.4 plays a double role in roots and shoots of nitrogen-starved plants. The Plant Cell 24, 245-258.
26. Koyama H., Toda T. & Hara T. (2001) Brief exposure to low-pH stress causes irreversible damage to the growing root in Arabidopsis thaliana: pectin-Ca interaction may play an important role in proton rhizotoxicity. Journal of Experimental Botany 52, 361-368.
27. Kronzucker H.J., Siddiqi M.Y., Glass A.D. & Kirk G.J. (1999) Nitrate-ammonium synergism in rice: a subcellular flux analysis. Plant Physiology 119, 1041-1045.
28. Lager I., Andréasson O., Dunbar T.L., Andreasson E., Escobar M.A. & Rasmusson A.G. (2010) Changes in external pH rapidly alter plant gene expression and modulate auxin and elicitor responses. Plant, Cell & Environment 33, 1513-1528.
29. Lambers H., Neetseson J.J. & Stulen I. (1986) Fundamental, Ecological and Agricultural Aspects of Nitrogen Metabolism in Higher Plants: Proceedings of a Symposium. Martinus Nijhoff, Dordrecht, South Holland, Netherlands.
30. Lee S.C., Lan W., Buchanan B.B. & Luan S. (2009) A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proceedings of the National Academy of Sciences of the United States of America 106, 21419-21424.
31. Li B., Li G., Kronzucker H.J., Baluška F. & Shi W. (2014) Ammonium stress in Arabidopsis: signaling, genetic loci, and physiological targets. Trends in Plant Science 19, 107-114.
32. Li W., Wang Y., Okamoto M., Crawford N.M., Siddiqi M.Y. & Glass A.D. (2007) Dissection of the AtNRT2.1:AtNRT2.2 inducible high-affinity nitrate transporter gene cluster. Plant Physiology 143, 425-433.
33. Liu K.H., Huang C.Y. & Tsay Y.F. (1999) CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. The Plant Cell 11, 865-874.
34. Ludewig U., Neuhäuser B. & Dynowski M. (2007) Molecular mechanisms of ammonium transport and accumulation in plants. FEBS Letters 581, 2301-2308.
35. 2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452, 483-486.
36. Orsel M., Eulenburg K., Krapp A. & Daniel-Vedele F. (2004) Disruption of the nitrate transporter genes AtNRT2.1 and AtNRT2.2 restricts growth at low external nitrate concentration. Planta 219, 714-721.
37. Orsel M., Chopin F., Leleu O., Smith S.J., Krapp A., Daniel-Vedele F. & Miller A.J. (2006) Characterization of a two-component high-affinity nitrate uptake system in Arabidopsis. Physiology and protein-protein interaction. Plant Physiology 142, 1304-1317.
38. Pasqualini S., Ederli L., Piccioni C., Batini P., Bellucci M., Arcioni S. & Antonielli M. (2001) Metabolic regulation and gene expression of root phosphoenolpyruvate carboxylase by different nitrogen sources. Plant, Cell & Environment 24, 439-447.
39. Patterson K., Cakmak T., Cooper A., Lager I., Rasmusson A.G. & Escobar M.A. (2010) Distinct signaling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. Plant, Cell & Environment 33, 1486-1501.
40. Sagi M., Dovrat A., Kipnis T. & Lips H. (1998) Nitrate reductase, phosphoenolpyruvate carboxylase, and glutamine synthetase in annual ryegrass as affected by salinity and nitrogen. Journal of Plant Nutrition 21, 707-723.
41. Salsac L., Chaillou S., Morot-Gaudry J.F., Lesaint C. & Jolivoe E. (1987) Nitrate and ammonium nutrition in plants. Plant Physiology and Biochemistry 25, 805-812.
42. Segonzac C., Boyer J.C., Ipotesi E., Szponarski W., Tillard P., Touraine B. Gibrat R. (2007) Nitrate efflux at the root plasma membrane: identification of an Arabidopsis excretion transporter. The Plant Cell 19, 3760-3777.
43. Tsay Y.F., Schroeder J.I., Feldmann K.A. & Crawford N.M. (1993) The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72, 705-713.
44. Vahisalu T., Kollist H., Wang Y.F., Nishimura N., Chan W.Y., Valerio G. Kangasjärvi J. (2008) SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452, 487-491.
45. Van Der Heijden M.G.A., Bardgett R.D. & Van Straalen N.M. (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters 11, 296-310.
46. Wang Y.Y., Hsu P.K. & Tsay Y.F. (2012) Uptake, allocation and signaling of nitrate. Trends in Plant Science 17, 458-467.
47. Wood C.C., Porée F., Dreyer I., Koehler G.J. & Udvardi M.K. (2006) Mechanisms of ammonium transport, accumulation, and retention in ooyctes and yeast cells expressing Arabidopsis AtAMT1;1. FEBS Letters 580, 3931-3936.
48. Xu G., Fan X. & Miller A.J. (2012) Plant nitrogen assimilation and use efficiency. Annual Review of Plant Biology 63, 153-182.
49. + transporter AKT1 in Arabidopsis. Cell 125, 1347-1360.
50. Zhu J.K. (2002) Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53, 247-273.
51. +-ATPase of rice roots to low pH as related to ammonium nutrition. Plant, Cell & Environment 32, 1428-1440.