Elevated CO2-induced production of nitric oxide (NO) by NO synthase differentially affects nitrate reductase activity in Arabidopsis plants under different nitrate supplies

Journal of Experimental Botany

Volumn 67, Issue 3, 2016, Pages 893-904

  Du, Shaoting ^a   Zhang, Ranran ^a   Zhang, Peng ^a   Liu, Huijun ^a   Yan, Minggang ^a   Chen, Ni ^a   Xie, Huaqiang ^a   Ke, Shouwei ^a  

^a ZHEJIANG GONGSHANG UNIVERSITY   (China)

Author keywords

CO2; elevated CO2; nitrate; nitrate reductase; nitric oxide; NO synthase; S nitrosylation

Indexed keywords

1,3-DIHYDROXY-4,4,5,5-TETRAMETHYL-2-(4-CARBOXYPHENYL)TETRAHYDROIMIDAZOLE; BENZOIC ACID DERIVATIVE; CARBON DIOXIDE; IMIDAZOLE DERIVATIVE; N(G) NITROARGININE METHYL ESTER; NITRATE REDUCTASE; NITRIC ACID DERIVATIVE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ARABIDOPSIS; BIOLOGICAL MODEL; BIOSYNTHESIS; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PLANT LEAF; PLANT ROOT; TIME FACTOR;

ARABIDOPSIS; BENZOATES; CARBON DIOXIDE; GENE EXPRESSION REGULATION, PLANT; IMIDAZOLES; MODELS, BIOLOGICAL; NG-NITROARGININE METHYL ESTER; NITRATE REDUCTASE; NITRATES; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PLANT LEAVES; PLANT ROOTS; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 84961749952     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv506     Document Type: Article

References (67)

1. Agüera E, Ruano D, Cabello P, de la Haba P.2006.Impact of atmospheric CO2 on growth, photosynthesis and nitrogen metabolism in cucumber (Cucumis sativus L.) plants.Journal of Plant Physiology 163, 809-817.
2. Beevers L, Hageman RH.1969.Nitrate reduction in higher plants. Annual Review of Plant Physiology 20, 495-522.
3. Bloom AJ, Asensio JSR, Randall L, Rachmilevitch S, Cousins AB, Carlisle EA.2012.CO2 enrichment inhibits shoot nitrate assimilation in C3 but not C4 plants and slows growth under nitrate in C3 plants.Ecology 93, 355-367.
4. Bolin B, Kheshgi HS.2001.On strategies for reducing greenhouse gas emissions.Proceedings of the National Academy of Sciences, USA 98, 4850-4854.
5. Bradford MM.1976.A rapid and sensitive method for the quantities of protein utilizing the principle of protein-dye binding.Analytical Biochemistry 72, 248-254.
6. Buchanan BB, Gruissem W, Jones RL.2000.Biochemistry and molecular biology of plants .Rockville, MD: american Society of Plant Physiologists.
7. Courtois C, Besson A, Dahan J, Bourque S, Dobrowolska G, Pugin A, Wendehenne D.2008.Nitric oxide signalling in plants: interplays with Ca2+ and protein kinases.Journal of Experimental Botany 59, 155-163.
8. Chen TL, Chen JH, Abd-Allah EF, Wang PK, Wang GP, Hu XY, Shi JS.2015.Quantitative proteomics analysis reveals that S-nitrosoglutathione reductase (GSNOR) and nitric oxide signaling enhance poplar defense against chilling stress.Planta 242, 1361-1390.
9. Chen WW, Yang JL, Qin C, Jin CW, Mo JH, Ye T, Zheng SJ.2010.Nitric oxide acts downstream of auxin to trigger root ferric chelate reductase activity in response to iron deficiency in Arabidopsis.Plant Physiology 154, 810-819.
10. Clarkson DT, Hanson JB.1980.The mineral nutrition of higher plants. Annual Review of Plant Physiology 31, 239-298.
11. Constable JVH, BassiriRad H, Lussenhop J, Zerihun A.2001.Influence of elevated CO2 and mycorrhizae on nitrogen acquisition: contrasting responses in Pinus taeda and Liquidambar styraciflua.Tree Physiology 21, 83-91.
12. Correa-Aragunde N, Lombardo C, Lamattina L.2008.Nitric oxide: an active nitrogen molecule that modulates cellulose synthesis in tomato roots.New Phytologist 179, 386-396.
13. Crawford NM.1995.Nitrate: nutrient and signal for plant growth.The Plant Cell 7, 859-868.
14. Dechorgnat J, Nguyen CT, Armengaud P, Jossier M, Diatloff E, Filleur S, Daniel-Vedele F.2011.From the soil to the seeds: the long journey of nitrate in plants.Journal of Experimental Botany 62, 1349-1359.
15. del Río LA, Corpas FJ, Barroso JB.2004.Nitric oxide and nitric oxide synthase activity in plants.Phytochemistry 65, 783-792.
16. Du ST, Zhang YS, Lin XY, Wang Y, Tang CX.2008.Regulation of nitrate reductase by nitric oxide in Chinese cabbage pakchoi (Brassica chinensis L.).Plant, Cell and Environment 31, 195-204.
17. Duval BD, Blankinship JC, Dijkstra P, Hungate BA.2012.CO2 effects on plant nutrient concentration depend on plant functional group and available nitrogen: a meta-analysis.Plant Ecology 213, 505-521.
18. Frungillo L, Skelly MJ, Loake GJ, Spoel SH, Salgado I.2014.S-Nitrosothiols regulate nitric oxide production and storage in plants through the nitrogen assimilation pathway.Nature Communications 5, 5401.
19. Geiger M, Liu PW, Engels C, Harnecker J.Schulze ED, Ludewig F, Sonnewald U, Scheible WR, Stitt M.1998.Enhanced carbon dioxide leads to a modified diurnal rhythm of nitrate reductase activity in older plants, and a large stimulation of nitrate reductase activity and higher levels of amino acids in young tobacco plants.Plant, Cell and Environment 21, 253-268.
20. Gojon A, Dapoigny L, Lejay L, Tillard P, Rufty TW.1998.Effects of genetic modification of nitrate reductase expression on 15NO3-uptake and reduction in Nicotiana plants.Plant, Cell and Environment 21, 43-53.
21. Guo FQ.2006.Response to Zemojtel et al.: plant nitric oxide synthase: AtNOS1 is just the beginning.Trends in Plant Science 11, 527-528.
22. Guo FQ, Crawford NM.2005.Arabidopsis nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and darkinduced senescence.The Plant Cell 17, 3436-3450.
23. Guo FQ, Okamoto M, Crawford NM.2003.Identification of a plant nitric oxide synthase gene involved in hormonal signaling.Science 302, 100-103.
24. Gow AJ, Stamler JS.1998.Reactions between nitric oxide and haemoglobin under physiological conditions.Nature 391, 169-173.
25. Hofmann LC, Straub S, Bischof K.2013.Elevated CO2 levels affect the activity of nitrate reductase and carbonic anhydrase in the calcifying rhodophyte Corallina officinalis.Journal of Experimental Botany 64, 899-908.
26. IPCC.2001.Climate change 2001: the scientific basis .Cambridge: Cambridge University Press.
27. IPCC.2007.Climate change 2007: the physical science basis. Cambridge: Cambridge University Press.
28. IPCC.2013.Climate change 2013: the physical science basis. Cambridge: Cambridge University Press.
29. Jeandroz S, Lamotte O, Astier J, et al.2013.There's more to the picture than meets the eye: nitric oxide cross talk with Ca2+ signaling.Plant Physiology 163, 459-470.
30. Jin CW, Du ST, Chen WW, Li GX, Zhang YS, Zheng SJ.2009a. Elevated carbon dioxide improves plants iron nutrition through enhancing the iron-deficiency-induced responses under iron-limited conditions in tomato.Plant Physiology 150, 272-280.
31. Jin CW, Du ST, Zhang YS, Lin XY, Tang CX.2009b.Differential regulatory role of nitric oxide in mediating nitrate reductase activity in roots of tomato (Solanum lycocarpum).Annals of Botany 104, 9-17.
32. Jin CW, Du ST, Zhang YS, Tang C, Lin XY.2009c.Atmospheric nitric oxide stimulates plant growth and improves the quality of spinach (Spinacia oleracea).Annals of Applied Biology 155, 113-120.
33. Jin CW, Du ST, Shamsi IH, Luo BF, Lin XY.2011.NO synthasegenerated NO acts downstream of auxin in regulating Fe-deficiencyinduced root branching that enhances Fe-deficiency tolerance in tomato plants.Journal of Experimental Botany 62, 3875-3884.
34. Kim HY, Lieffering M, Miura S, Kobayashi K, Okada M.2001.Growth and nitrogen uptake of CO2-enriched rice under field conditions.New Phytologist 150, 223-239.
35. Lamattina L, García-Mata C, Graziano M, Pagnussat G.2003.Nitric oxide: the versatility of an extensive signal molecule.Annual Review of Plant Biology 54, 109-136.
36. Larios B, Agüera E, de la Haba P, Pérez-Vicente Maldonado JM. 2001.A short-term exposure of cucumber plants to rising atmospheric CO2 increases leaf carbohydrate content and enhances nitrate reductase expression and activity.Planta 212, 305-312.
37. Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR. 2009a.Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE.Journal of Experimental Botany 60, 2859-2876.
38. Leakey ADB, Xu FX, Gillespie KM, McGrath JM, Ainsworth EA, Ort DR.2009b.Genomic basis for stimulated respiration by plants growing under elevated carbon dioxide.Proceedings of the National Academy of Sciences, USA 106, 3597-3602.
39. Lekshmy S, Jain V, Khetarpal S, Pandey R.2013.Inhibition of nitrate uptake and assimilation in wheat seedlings grown under elevated CO2. Indian Journal of Plant Physiology 18, 23-29.
40. Leleu O, Vuylsteker C.2004.Unusual regulatory nitrate reductase activity in cotyledons of Brassica napus seedlings: enhancement of nitrate reductase activity by ammonium supply.Journal of Experimental Botany 55, 815-823.
41. Lindermayr C, Saalbach G, Durner J.2005.Proteomic identification of S-nitrosylated proteins in Arabidopsis.Plant Physiology 137, 921-930.
42. Lin SH, Kuo HF, Canivenc G, et al.2008.Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport. The Plant Cell 20, 2514-2528.
43. Matt P, Geiger M, Liu PW, Engels C, Krapp A, Stitt M.2001.Elevated carbon dioxide increases nitrate uptake and nitrate reductase activity when tobacco is growing on nitrate, but increases ammonium uptake and inhibits nitrate reductase activity when tobacco is growing on ammonium nitrate.Plant, Cell and Environment 24, 1119-1137.
44. Melzer JM, Kleinhofs A, Warner RL.1989.Nitrate reductase regulation: effects of nitrate and light on nitrate reductase mRNA accumulation. Molecular and General Genetics 217, 341-346.
45. Natali SM, Sañudo-Wilhelmy SA, Lerdau MT.2009.Effects of elevated carbon dioxide and nitrogen fertilization on nitrate reductase activity in sweetgum and loblolly pine trees in two temperate forests.Plant and Soil 314, 197-210.
46. Neill SJ, Desikan R, Hancock JT.2003.Nitric oxide signalling in plants. New Phytologist 159, 11-35.
47. Niu YF, Cai RS, Dong HF, Wang H, Tang CX, Zhang YS.2012.Effect of elevated CO2 on phosphorus nutrition of phosphate-deficient Arabidopsis thaliana (L.) Heynh under different nitrogen forms.Journal of Experimental Botany 64, 355-367.
48. Niu YF, Jin CW, Jin GL, Zhou QY, Lin XY, Tang CX, Zhang YS.2011.Auxin modulates the enhanced development of root hairs in Arabidopsis thaliana (L.) Heynh.under elevated CO2.Plant, Cell and Environment 34, 1304-1317.
49. Pérez-López U, Robredo A, Miranda-Apodaca J, Lacuesta M, Muñoz-Rueda A, Mena-Petite A.2013.Carbon dioxide enrichment moderates salinity-induced effects on nitrogen acquisition and assimilation and their impact on growth in barley plants.Environmental and Experimental Botany 87, 148-158.
50. Poonnachit U, Darnell R.2004.Effect of ammonium and nitrate on ferric chelate reductase and nitrate reductase in Vaccinium species.Annals of Botany 93, 399-405.
51. Robredo A, Pérez-López U, Miranda-Apodaca J, Lacuesta M. 2011.Elevated CO2 reduces the drought effect on nitrogen metabolism in barley plants during drought and subsequent recovery.Environmental and Experimental Botany 71, 399-408.
52. Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM.2002.Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. Journal of Experimental Botany 53, 103-110.
53. Sailo N, Verma R, Pandey R, Jain V.2013.Effect of elevated carbon dioxide on nitrogen assimilation and mobilization in wheat and rye genotypes of different ploidy levels.Indian Journal of Plant Physiology 18, 333-338.
54. Shapiro AD.2005.Nitric oxide signaling in plants.Vitamins and Hormones 72, 339-398.
55. Shi W, Norton JM.2000.Microbial control of nitrate concentrations in an agricultural soil treated with dairy waste compost or ammonium fertilizer. Soil Biology &Biochemistry 32, 1453-1457.
56. Sicher RC.2001.Responses of nitrogen metabolism in N-sufficient barley primary leaves to plant growth in elevated atmospheric carbon dioxide. Photosynthesis Research 68, 193-201.
57. Simontacchi M, García-Mata C, Bartoli CG, Santa-María GE, Lamattina L.2013.Nitric oxide as a key component in hormoneregulated processes.Plant Cell Reports 32, 853-866.
58. Singh RJ, Hogg N, Joseph J, Kalyanaraman B.1996.Mechanism of nitric oxide release from S-nitrosothiols.Journal of Biological Chemistry 271, 18596-18603.
59. Stitt M, Krapp A.1999.The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background.Plant, Cell and Environment 22, 583-621.
60. Vance CP.2001.Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources.Plant Physiology 127, 390-397.
61. Wang H, Xiao WD, Niu YF, Jin CW, Chai RS, Tang CX, Zhang YS. 2013.Nitric oxide enhances development of lateral roots in tomato (Solanum lycopersicum L.) under elevated carbon dioxide.Planta 237, 137-144.
62. Wang Y.2006.S-Nitrosylation: an emerging redox-based posttranslational modification in plants.Journal of Experimental Botany 57, 1777-1784.
63. Xiong J, Lu H, Lu KX, Duan YX, An LY, Zhu C.2009.Cadmium decreases crown root number by decreasing endogenous nitric oxide, which is indispensable for crown root primordial initiation in rice seedlings. Planta 230, 599-610.
64. Yamasaki H, Sakihama Y.2000.Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species.FEBS Letters 468, 89-92.
65. Yang HJ, Mu JY, Chen LC, Feng J, Hu JL, Li L, Zhou JM, Zuo JR.2015.S-Nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses.Plant Physiology 167, 1604-1615.
66. Zhao MG, Tian QY, Zhang WH.2007.Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiology 144, 206-217.
67. Zottini M, Costa A, De Michele R, Ruzzene M, Carimi F, Lo Schiavo F.2007.Salicylic acid activates nitric oxide synthesis in Arabidopsis. Journal of Experimental Botany 58, 1397-405.