Plant survival in a changing environment: The role of nitric oxide in plant responses to abiotic stress

Frontiers in Plant Science

Volumn 6, Issue NOVEMBER, 2015, Pages

  Simontacchi, Marcela ^a   Galatro, Andrea ^b   Ramos Artuso, Facundo ^a   Santa María, Guillermo E ^c  

^a Universidad Nacional de La Plata   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c UNIVERSIDAD NACIONAL DE SAN MARTÍN   (Argentina)

Author keywords

Drought; Mineral nutrition; Nitric oxide; Salinity; Ultraviolet radiation; UV B

Indexed keywords

EID: 84947577851     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00977     Document Type: Review

References (223)

1. Abat, J. K., and Deswal, R. (2009). Differential modulation of S-nitrosoproteome ofBrassica juncea by low temperature: change in S-nitrosylation of Rubisco is responsible for the inactivation of its carboxylase activity. Proteomics 9, 4368-4380. doi: 10.1002/pmic.200800985
2. Amtmann, A. (1999). K+-Selective inward-rectifying channels and apoplastic pH in barley roots. Plant Physiol. 120, 331-338. doi: 10.1104/pp.120.1.331
3. Andrews, M., and Lea, P. J. (2013). Our nitrogen "footprint": the need for increased crop nitrogen use efficiency. Ann. Appl. Biol. 163, 165-169. doi: 10.1111/aab.12052
4. Arasimowicz-Jelonek, M., Floryszak-Wieczorek, J., and Kubiś, J. (2009). Involvement of nitric oxide in water stress-induced responses of cucumber roots. Plant Sci. 177, 682-690. doi: 10.1016/j.plantsci.2009.09.007
5. Arc, E., Sechet, J., Corbineau, F., Rajjou, L., and Marion-Poll, A. (2013). ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Front. Plant Sci. 4:63. doi: 10.3389/fpls.2013.00063
6. Arnaud, N., Murgia, I., Boucherez, J., Briat, J.-F., Cellier, F., and Gaymard, F. (2006). An iron-induced nitric oxide burst precedes ubiquitin-dependent protein degradation for Arabidopsis AtFer1 ferritin gene expression. J. Biol. Chem. 281, 23579-23588. doi: 10.1074/jbc.M602135200
7. Aro, E., Virgin, I., and Andersson, B. (1993). Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta 1143, 113-134. doi: 10.1016/0005-2728(93)90134-2
8. Asai, S., Ohta, K., and Yoshioka, H. (2008). MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. Plant Cell 20, 1390-1406. doi: 10.1105/tpc.107.055855
9. Beligni, M. V., and Lamattina, L. (2001). Nitric oxide: a non-traditional regulator of plant growth. Trends Plant Sci. 6, 508-509. doi: 10.1016/S1360-1385(01)02156-2
10. Bethke, P. C., Badger, M. R., and Jones, R. L. (2004). Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 16, 332-341. doi: 10.1105/tpc.017822
11. Borisjuk, L., Macherel, D., Benamar, A., Wobus, U., and Rolletschek, H. (2007). Low oxygen sensing and balancing in plant seeds: a role for nitric oxide. New Phytol. 176, 813-823. doi: 10.1111/j.1469-8137.2007.02226.x
12. 2 synthesis.Plant J. 45, 113-122. doi: 10.1111/j.1365-313X.2005.02615.x
13. Britto, D. T., Siddiqi, M. Y., Glass, A. D., 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. doi: 10.1073/pnas.061034698
14. Brown, B. A., Cloix, C., Jiang, G. H., Kaiserli, E., Herzyk, P., Kliebenstein, D. J., et al. (2005). A UV-B-specific signaling component orchestrates plant UV protection. Proc. Natl. Acad. Sci. U.S.A. 102, 18225-18230. doi: 10.1073/pnas.0507187102
15. Buet, A., Moriconi, J. I., Santa-María, G. E., and Simontacchi, M. (2014). An exogenous source of nitric oxide modulates zinc nutritional status in wheat plants.Plant Physiol. Biochem. 83, 337-345. doi: 10.1016/j.plaphy.2014.08.020
16. Buet, A., and Simontacchi, M. (2015). Nitric oxide and plant iron homeostasis. Ann. N. Y. Acad. Sci. 1340, 39-46. doi: 10.1111/nyas.12644
17. Cakmak, I. (2005). The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J. Plant Nutr. Soil Sci. 168, 521-530. doi: 10.1002/jpln.200420485
18. Calcagno, C., Novero, M., Genre, A., Bonfante, P., and Lanfranco, L. (2012). The exudate from an arbuscular mycorrhizal fungus induces nitric oxide accumulation inMedicago truncatula roots. Mycorrhiza 22, 259-269. doi: 10.1007/s00572-011-0400-4
19. Camejo, D., Romero-Puertas, M. D. C., Rodríguez-Serrano, M., Sandalio, L. M., Lázaro, J. J., Jiménez, A., et al. (2013). Salinity-induced changes in S-nitrosylation of pea mitochondrial proteins. J. Proteom. 79, 87-99. doi: 10.1016/j.jprot.2012.12.003
20. Cecconi, D., Orzetti, S., Vandelle, E., Rinalducci, S., Zolla, L., and Delledonne, M. (2009). Protein nitration during defense response in Arabidopsis thaliana.Electrophoresis 30, 2460-2468. doi: 10.1002/elps.200800826
21. Chaki, M., Valderrama, R., Fernández-Ocaña, A. M., Carreras, A., López-Jaramillo, J., Luque, F., et al. (2009). Protein targets of tyrosine nitration in sunflower (Helianthus annuus L.) hypocotyls. J. Exp. Bot. 60, 4221-4234. doi: 10.1093/jxb/erp263
22. Chen, J., Xiao, Q., Wang, C., Wang, W.-H., Wu, F.-H., Chen, J., et al. (2014). Nitric oxide alleviates oxidative stress caused by salt in leaves of a mangrove species,Aegiceras corniculatum. Aquat. Bot. 117, 41-47. doi: 10.1016/j.aquabot.2014.04.004
23. Chen, J., Xiao, Q., Wu, F., Dong, X., He, J., Pei, Z., et al. (2010). Nitric oxide enhances salt secretion and Na+ sequestration in a mangrove plant, Avicennia marina, through increasing the expression of H(+)-ATPase and Na(+)/H(+) antiporter under high salinity. Tree Physiol. 30, 1570-1585. doi: 10.1093/treephys/tpq086
24. Chen, J., Xiong, D.-Y., Wang, W.-H., Hu, W.-J., Simon, M., Xiao, Q., et al. (2013a). Nitric oxide mediates root K+/Na+ balance in a mangrove plant, Kandelia obovata, by enhancing the expression of AKT1-type K+ channel and Na+/H+ antiporter under high salinity. PLoS ONE 8:e71543. doi: 10.1371/journal.pone.0071543
25. Chen, K., Chen, L., Fan, J., and Fu, J. (2013b). Alleviation of heat damage to photosystem II by nitric oxide in tall fescue. Photosynth. Res. 116, 21-31. doi: 10.1007/s11120-013-9883-5
26. Chun, H. J., Park, H. C., Koo, S. C., Lee, J. H., Park, C. Y., Choi, M. S., et al. (2012). Constitutive expression of mammalian nitric oxide synthase in tobacco plants triggers disease resistance to pathogens. Mol. Cells 34, 463-471. doi: 10.1007/s10059-012-0213-0
27. Cogliatti, D. H., and Santa-Maria, G. E. (1990). Influx and efflux of phosphorus in roots of wheat plants in non-growth-limiting concentrations of phosphorus. J. Exp. Bot. 41, 601-607. doi: 10.1093/jxb/41.5.601
28. Contestabile, A. (2008). Regulation of transcription factors by nitric oxide in neurons and in neural-derived tumor cells. Prog. Neurobiol. 84, 317-328. doi: 10.1016/j.pneurobio.2008.01.002
29. Cooney, R. V., Harwood, P. J., Custer, L. J., and Franke, A. A. (1994). Light-mediated conversion of nitrogen dioxide to nitric oxide by carotenoids. Environ. Health Perspect. 102, 460-462. doi: 10.1289/ehp.94102460
30. Corpas, F. J., de la Colina, C., Sánchez-Rasero, F., and del Rio, L. A. (1997). A role for leaf peroxisomes in the catabolism of purines. J. Plant Physiol. 151, 246-250. doi: 10.1016/S0176-1617(97)80161-7
31. Corpas, F. J., Hayashi, M., Mano, S., Nishimura, M., and Barroso, J. B. (2009). Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of Arabidopsis plants. Plant Physiol. 151, 2083-2094. doi: 10.1104/pp.109.146100
32. Correa-Aragunde, N., Foresi, N., and Lamattina, L. (2013). Structure diversity of nitric oxide synthases (NOS): the emergence of new forms in photosynthetic organisms.Front. Plant Sci. 4:232. doi: 10.3389/fpls.2013.00232
33. Correa-Aragunde, N., Lombardo, C., and Lamattina, L. (2008). Nitric oxide: an active nitrogen molecule that modulates cellulose synthesis in tomato roots. New Phytol.179, 386-396. doi: 10.1111/j.1469-8137.2008.02466.x
34. Corti Monzón, G., Pinedo, M., Di Rienzo, J., Novo-Uzal, E., Pomar, F., Lamattina, L., et al. (2014). Nitric oxide is required for determining root architecture and lignin composition in sunflower. Supporting evidence from microarray analyses. Nitric Oxide 39, 20-28. doi: 10.1016/j.niox.2014.04.004
35. Crawford, N. M. (1995). Nitrate: nutrient and signal for plant growth. Plant Cell 7, 859-868. doi: 10.1105/tpc.7.7.859
36. Cushman, J. C. (2001). Crassulacean acid metabolism. A plastic photosynthetic adaptation to arid environments. Plant Physiol. 127, 1439-1448. doi: 10.1104/pp.010818
37. D'Autréaux, B., Tucker, N. P., Dixon, R., and Spiro, S. (2005). A non-haem iron centre in the transcription factor NorR senses nitric oxide. Nature 437, 769-772. doi: 10.1038/nature03953
38. David, A., Yadav, S., and Bhatla, S. C. (2010). Sodium chloride stress induces nitric oxide accumulation in root tips and oil body surface accompanying slower oleosin degradation in sunflower seedlings. Physiol. Plant. 140, 342-354. doi: 10.1111/j.1399-3054.2010.01408.x
39. Demidchik, V., Cuin, T. A., Svistunenko, D., Smith, S. J., Miller, A. J., Shabala, S., et al. (2010). Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death.J. Cell Sci. 123, 1468-1479. doi: 10.1242/jcs.064352
40. De Montaigu, A., Sanz-Luque, E., Galván, A., and Fernández, E. (2010). A soluble guanylate cyclase mediates negative signaling by ammonium on expression of nitrate reductase in Chlamydomonas. Plant Cell 22, 1532-1548. doi: 10.1105/tpc.108.062380
41. Desikan, R., Griffiths, R., Hancock, J., and Neill, S. (2002). A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A.99, 16314-16318. doi: 10.1073/pnas.252461999
42. di Palma, A. A., Lamattina, L., and Creus, C. M. (2011). "Nitric oxide as a signal molecule in intracellular and extracellular bacteria-plant interactions," in Ecological Aspects of Nitrogen Metabolism in Plants, eds J. C. Polacco and C. D. Todd (New York City, NY: John Wiley & Sons, Inc.), 397-420.
43. Dordas, C., Hasinoff, B. B., Igamberdiev, A. U., Manac'h, N., Rivoal, J., and Hill, R. D. (2003). Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. Plant J. 35, 763-770. doi: 10.1046/j.1365-313X.2003.01846.x
44. Duan, Y. H., Zhang, Y. L., Ye, L. T., Fan, X. R., Xu, G. H., and Shen, Q. R. (2007). Responses of rice cultivars with different nitrogen use efficiency to partial nitrate nutrition. Ann. Bot. 99, 1153-1160. doi: 10.1093/aob/mcm051
45. Durner, J., Wendehenne, D., and Klessig, D. F. (1998). Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc. Natl. Acad. Sci. U.S.A. 95, 10328-10333. doi: 10.1073/pnas.95.17.10328
46. Epstein, E., Rains, D. W., and Elzam, O. E. (1963). Resolution of dual mechanisms of potassium absorption by barley roots. Proc. Natl. Acad. Sci. U.S.A. 49, 684-692. doi: 10.1073/pnas.49.5.684
47. Fares, A., Rossignol, M., and Peltier, J.-B. (2011). Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochem. Biophys. Res. Commun. 416, 331-336. doi: 10.1016/j.bbrc.2011.11.036
48. Fazzari, M., Trostchansky, A., Schopfer, F. J., Salvatore, S. R., Sánchez-Calvo, B., Vitturi, D., et al. (2014). Olives and olive oil are sources of electrophilic fatty acid nitroalkenes. PLoS ONE 9:e84884. doi: 10.1371/journal.pone.0084884
49. Feechan, A., Kwon, E., Yun, B.-W., Wang, Y., Pallas, J. A., and Loake, G. J. (2005). A central role for S-nitrosothiols in plant disease resistance. Proc. Natl. Acad. Sci. U.S.A.102, 8054-8059. doi: 10.1073/pnas.0501456102
50. Fernández-Marcos, M., Sanz, L., Lewis, D. R., Muday, G. K., and Lorenzo, O. (2011). Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport. Proc. Natl. Acad. Sci. U.S.A. 108, 18506-18511. doi: 10.1073/pnas.1108644108
51. Fernández-Marcos, M., Sanz, L., and Lorenzo, O. (2012). Nitric oxide: an emerging regulator of cell elongation during primary root growth. Plant Signal. Behav. 7, 196-200. doi: 10.4161/psb.18895
52. Flores, T., Todd, C. D., Tovar-Mendez, A., Dhanoa, P. K., Correa-Aragunde, N., Hoyos, M. E., et al. (2008). Arginase-negative mutants of Arabidopsis exhibit increased nitric oxide signaling in root development. Plant Physiol. 147, 1936-1946. doi: 10.1104/pp.108.121459
53. Floss, D. S., Levy, J. G., Lévesque-Tremblay, V., Pumplin, N., and Harrison, M. J. (2013). DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. U.S.A. 110, E5025-E5034. doi: 10.1073/pnas.1308973110
54. Foissner, I., Wendehenne, D., Langebartels, C., and Durner, J. (2000). In vivo imaging of an elicitor-induced nitric oxide burst in tobacco. Plant J. 23, 817-824. doi: 10.1046/j.1365-313X.2000.00835.x
55. Foresi, N., Correa-Aragunde, N., Parisi, G., Caló, G., Salerno, G., and Lamattina, L. (2010). Characterization of a nitric oxide synthase from the plant kingdom: NO generation from the green alga Ostreococcus tauri is light irradiance and growth phase dependent. Plant Cell 22, 3816-3830. doi: 10.1105/tpc.109.073510
56. Foresi, N., Mayta, M. L., Lodeyro, A. F., Scuffi, D., Correa-Aragunde, N., García-Mata, C., et al. (2015). Expression of the tetrahydrofolate-dependent nitric oxide synthase from the green alga Ostreococcus tauri increases tolerance to abiotic stresses and influences stomatal development in Arabidopsis. Plant J. 82, 806-821. doi: 10.1111/tpj.12852
57. Freschi, L., Rodrigues, M. A., Domingues, D. S., Purgatto, E., Van Sluys, M.-A., Magalhaes, J. R., et al. (2010). Nitric oxide mediates the hormonal control of Crassulacean acid metabolism expression in young pineapple plants. Plant Physiol.152, 1971-1985. doi: 10.1104/pp.109.151613
58. Frohnmeyer, H., and Staiger, D. (2003). Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection. Plant Physiol. 133, 1420-1428. doi: 10.1104/pp.103.030049
59. Frungillo, L., Skelly, M. J., Loake, G. J., Spoel, S. H., and Salgado, I. (2014). S-nitrosothiols regulate nitric oxide production and storage in plants through the nitrogen assimilation pathway. Nat. Commun. 5, 5401. doi: 10.1038/ncomms6401
60. Furchgott, R. F., and Zawadzki, J. V. (1980). The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288, 373-376. doi: 10.1038/288373a0
61. Galatro, A., Puntarulo, S., Guiamet, J. J., and Simontacchi, M. (2013). Chloroplast functionality has a positive effect on nitric oxide level in soybean cotyledons. Plant Physiol. Biochem. 66, 26-33. doi: 10.1016/j.plaphy.2013.01.019
62. Galatro, A., Simontacchi, M., and Puntarulo, S. (2001). Free radical generation and antioxidant content in chloroplasts from soybean leaves exposed to ultraviolet-B.Physiol. Plant. 113, 564-570. doi: 10.1034/j.1399-3054.2001.1130416.x
63. Galetskiy, D., Lohscheider, J. N., Kononikhin, A. S., Popov, I. A., Nikolaev, E. N., and Adamska, I. (2011). Phosphorylation and nitration levels of photosynthetic proteins are conversely regulated by light stress. Plant Mol. Biol. 77, 461-473. doi: 10.1007/s11103-011-9824-7
64. García, M. J., Lucena, C., Romera, F. J., Alcántara, E., and Pérez-Vicente, R. (2010). Ethylene and nitric oxide involvement in the up-regulation of key genes related to iron acquisition and homeostasis in Arabidopsis. J. Exp. Bot. 61, 3885-3899. doi: 10.1093/jxb/erq203
65. García-Mata, C., Gay, R., Sokolovski, S., Hills, A., Lamattina, L., and Blatt, M. R. (2003). Nitric oxide regulates K+ and Cl- channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc. Natl. Acad. Sci. U.S.A. 100, 11116-11121. doi: 10.1073/pnas.1434381100
66. García-Mata, C., and Lamattina, L. (2001). Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol. 126, 1196-1204. doi: 10.1104/pp.126.3.1196
67. García-Mata, C., and Lamattina, L. (2002) Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol. 128, 790-792. doi: 10.1104/pp.011020
68. Gas, E., Flores-Pérez, U., Sauret-Güeto, S., and Rodríguez-Concepción, M. (2009). Hunting for plant nitric oxide synthase provides new evidence of a central role for plastids in nitric oxide metabolism. Plant Cell 21, 18-23. doi: 10.1105/tpc.108.065243
69. Gaston, B. (1999). Nitric oxide and thiol groups. Biochim. Biophys. Acta 1411, 323-333. doi: 10.1016/S0005-2728(99)00023-7
70. Gibbs, D. J., Md Isa, N., Movahedi, M., Lozano-Juste, J., Mendiondo, G. M., Berckhan, S., et al. (2014). Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors. Mol. Cell 53, 369-379. doi: 10.1016/j.molcel.2013.12.020
71. Gould, K. S., Lamotte, O., Klinguer, A., Pugin, A., and Wendehenne, D. (2003). Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ. 26, 1851-1862. doi: 10.1046/j.1365-3040.2003.01101.x
72. Graziano, M., Beligni, M. V., and Lamattina, L. (2002). Nitric oxide improves internal iron availability in plants. Plant Physiol. 130, 1852-1859. doi: 10.1104/pp.009076
73. Graziano, M., and Lamattina, L. (2007). Nitric oxide accumulation is required for molecular and physiological responses to iron deficiency in tomato roots. Plant J. 52, 949-960. doi: 10.1111/j.1365-313X.2007.03283.x
74. Gupta, K. J., Stoimenova, M., and Kaiser, W. M. (2005). In higher plants, only root mitochondria, but not leaf mitochondria reduce nitrite to NO, in vitro and in situ. J. Exp. Bot. 56, 2601-2609. doi: 10.1093/jxb/eri252
75. Hao, G., Du, X., Zhao, F., Shi, R., and Wang, J. (2009). Role of nitric oxide in UV-B-induced activation of PAL and stimulation of flavonoid biosynthesis in Ginkgo bilobacallus. Plant Cell Tissue Organ Cult. 97, 175-185. doi: 10.1007/s11240-009-9513-2
76. Harberd, N. P., Belfield, E., and Yasumura, Y. (2009). The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: how an "inhibitor of an inhibitor" enables flexible response to fluctuating environments. Plant Cell 21, 1328-1339. doi: 10.1105/tpc.109.066969
77. Hasanuzzaman, M., Hossain, M. A., and Fujita, M. (2011). Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. Plant Biotechnol. Rep. 5, 353-365. doi: 10.1007/s11816-011-0189-9
78. Hayes, S., Velanis, C. N., Jenkins, G. I., and Franklin, K. A. (2014). UV-B detected by the UVR8 photoreceptor antagonizes auxin signaling and plant shade avoidance. Proc. Natl. Acad. Sci. U.S.A. 111, 11894-11899. doi: 10.1073/pnas.1403052111
79. He, J.-M., Xu, H., She, X.-P., Song, X.-G., and Zhao, W.-M. (2005). The role and the interrelationship of hydrogen peroxide and nitric oxide in the UV-B-induced stomatal closure in broad bean. Funct. Plant Biol. 32, 237-247. doi: 10.1071/FP04185
80. He, Y., Tang, R.-H., Hao, Y., Stevens, R. D., Cook, C. W., Ahn, S. M., et al. (2004). Nitric oxide represses the Arabidopsis floral transition. Science 305, 1968-1971. doi: 10.1126/science.1098837
81. Hebelstrup, K. H., Shah, J. K., and Igamberdiev, A. U. (2013). The role of nitric oxide and hemoglobin in plant development and morphogenesis. Physiol. Plant. 148, 457-469. doi: 10.1111/ppl.12062
82. Henry, Y., and Guissani, A. (1999). Interactions of nitric oxide with hemoproteins: roles of nitric oxide in mitochondria. Cell. Mol. Life Sci. 55, 1003-1014. doi: 10.1007/s000180050351
83. Hichri, I., Boscari, A., Castella, C., Rovere, M., Puppo, A., and Brouquisse, R. (2015). Nitric oxide: a multifaceted regulator of the nitrogen-fixing symbiosis. J. Exp. Bot. 66, 2877-2887. doi: 10.1093/jxb/erv051
84. Hogg, N., and Kalyanaraman, B. (1999). Nitric oxide and lipid peroxidation. Biochim. Biophys. Acta 1411, 378-384. doi: 10.1016/S0005-2728(99)00027-4
85. Hughes, M. N. (1999). Relationships between nitric oxide, nitroxyl ion, nitrosonium cation and peroxynitrite. Biochim. Biophys. Acta 1411, 263-272. doi: 10.1016/S0005-2728(99)00019-5
86. Jasid, S., Simontacchi, M., Bartoli, C. G., and Puntarulo, S. (2006). Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. Plant Physiol. 142, 1246-1255. doi: 10.1104/pp.106.086918
87. Jasid, S., Simontacchi, M., and Puntarulo, S. (2008). Exposure to nitric oxide protects against oxidative damage but increases the labile iron pool in sorghum embryonic axes. J. Exp. Bot. 59, 3953-3962. doi: 10.1093/jxb/ern235
88. Jiang, C., Gao, X., Liao, L., Harberd, N. P., and Fu, X. (2007). Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiol. 145, 1460-1470. doi: 10.1104/pp.107.103788
89. Jin, C. W., Du, S. T., Zhang, Y. S., Lin, X. Y., and Tang, C. X. (2009). Differential regulatory role of nitric oxide in mediating nitrate reductase activity in roots of tomato (Solanum lycocarpum). Ann. Bot. 104, 9-17. doi: 10.1093/aob/mcp087
90. Joshi, M. S., Ponthier, J. L., and Lancaster, J. R. (1999). Cellular antioxidant and pro-oxidant actions of nitric oxide. Free Radic. Biol. Med. 27, 1357-1366. doi: 10.1016/S0891-5849(99)00179-3
91. Kanner, J., Harel, S., and Rina, G. (1991). Nitric oxide as an antioxidant. Arch. Biochem. Biophys. 289, 130-136. doi: 10.1016/0003-9861(91)90452-O
92. Kataria, S., Jajoo, A., and Guruprasad, K. N. (2014). Impact of increasing Ultraviolet-B (UV-B) radiation on photosynthetic processes. J. Photochem. Photobiol. B Biol. 137, 55-66. doi: 10.1016/j.jphotobiol.2014.02.004
93. Khurana, A., Khurana, J. P., and Babbar, S. B. (2011). Nitric oxide induces flowering in the duckweed Lemna aequinoctialis Welw. (Syn. L. paucicostata Hegelm.) under noninductive conditions. J. Plant Growth Regul. 30, 378-385. doi: 10.1007/s00344-011-9199-7
94. Klepper, L. (1979). Nitric oxide (NO) and nitrogen dioxide (NO2) emissions from herbicide-treated soybean plants. Atmos. Environ. 13, 537-542. doi: 10.1016/0004-6981(79)90148-3
95. Kneeshaw, S., Gelineau, S., Tada, Y., Loake, G. J., and Spoel, S. H. (2014). Selective protein denitrosylase activity of Thioredoxin-h5 modulates plant immunity. Mol. Cell56, 153-162. doi: 10.1016/j.molcel.2014.08.003
96. Kolbert, S., Petô, A., Szôllôsi, R., Erdei, L., and Tari, I. (2011). Nitric oxide (NO) generation during vegetative/generative transition of the apical meristem in wheat.Acta Biol. Szeged. 55, 95-97.
97. Kopyra, M., and Gwóźdź, E. A. (2003). Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth ofLupinus luteus. Plant Physiol. Biochem. 41, 1011-1017. doi: 10.1016/j.plaphy.2003.09.003
98. Kovácik, J., Klejdus, B., and Backor, M. (2009). Nitric oxide signals ROS scavenger-mediated enhancement of PAL activity in nitrogen-deficient Matricaria chamomillaroots: side effects of scavengers. Free Radic. Biol. Med. 46, 1686-1693. doi: 10.1016/j.freeradbiomed.2009.03.020
99. Krasuska, U., Ciacka, K., Andryka-Dudek, P., and Bogatek, R. (2015). "Signaling and communication in plants," in Reactive Oxygen and Nitrogen Species Signaling and Communication in Plants, eds K. J. Gupta and A. U. Igamberdiev (New York City, NY: Springer International Publishing), 316.
100. Kronzucker, H. J., Szczerba, M. W., Moazami-Goudarzi, M., and Britto, D. T. (2006). The cytosolic Na+: K+ ratio does not explain salinity-induced growth impairment in barley: a dual-tracer study using 42K+ and 24Na+. Plant Cell Environ. 29, 2228-2237. doi: 10.1111/j.1365-3040.2006.01597.x
101. Lambers, H., Finnegan, P. M., Laliberté, E., Pearse, S. J., Ryan, M. H., Shane, M. W., et al. (2011). Update on phosphorus nutrition in Proteaceae. Phosphorus nutrition of proteaceae in severely phosphorus-impoverished soils: are there lessons to be learned for future crops? Plant Physiol. 156, 1058-1066. doi: 10.1104/pp.111.174318
102. Lamotte, O., Bertoldo, J. B., Besson-Bard, A., Rosnoblet, C., Aimé, S., Hichami, S., et al. (2014). Protein S-nitrosylation: specificity and identification strategies in plants.Front. Chem. 2:114. doi: 10.3389/fchem.2014.00114
103. Lauff, D. B., and Santa-María, G. E. (2010). Potassium deprivation is sufficient to induce a cell death program in Saccharomyces cerevisiae. FEMS Yeast Res. 10, 497-507. doi: 10.1111/j.1567-1364.2010.00628.x
104. Laxalt, A. M., Raho, N., Have, A. T., and Lamattina, L. (2007). Nitric oxide is critical for inducing phosphatidic acid accumulation in xylanase-elicited tomato cells. J. Biol. Chem. 282, 21160-21168. doi: 10.1074/jbc.M701212200
105. Leshem, Y. Y., and Haramaty, E. (1996). The characterization and contrasting effects of the nitric oxide free radical in vegetative stress and senescence of Pisum sativumLinn. foliage. J. Plant Physiol. 148, 258-263. doi: 10.1016/S0176-1617(96)80251-3
106. Liu, F., and Guo, F.-Q. (2013). Nitric oxide deficiency accelerates chlorophyll breakdown and stability loss of thylakoid membranes during dark-induced leaf senescence in Arabidopsis. PLoS ONE 8:e56345. doi: 10.1371/journal.pone.0056345
107. Lombardo, M. C., Graziano, M., Polacco, J. C., and Lamattina, L. (2006). Nitric oxide functions as a positive regulator of root hair development. Plant Signal. Behav. 1, 28-33. doi: 10.4161/psb.1.1.2398
108. López-Bucio, J., Hernández-Abreu, E., Sánchez-Calderón, L., Nieto-Jacobo, M. F., Simpson, J., and Herrera-Estrella, L. (2002). Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol. 129, 244-256. doi: 10.1104/pp.010934
109. Lozano-Juste, J., Colom-Moreno, R., and León, J. (2011). In vivo protein tyrosine nitration in Arabidopsis thaliana. J. Exp. Bot. 62, 3501-3517. doi: 10.1093/jxb/err042
110. Lozano-Juste, J., and León, J. (2010). Enhanced abscisic acid-mediated responses in nia1nia2noa1-2 triple mutant impaired in NIA/NR- and AtNOA1-dependent nitric oxide biosynthesis in Arabidopsis. Plant Physiol. 152, 891-903. doi: 10.1104/pp.109.148023
111. Lozano-Juste, J., and León, J. (2011). Nitric oxide regulates DELLA content and PIF expression to promote photomorphogenesis in Arabidopsis. Plant Physiol. 156, 1410-1423. doi: 10.1104/pp.111.177741
112. Lu, C., and Koppenol, W. H. (2005). Inhibition of the Fenton reaction by nitrogen monoxide. J. Biol. Inorg. Chem. 10, 732-738. doi: 10.1007/s00775-005-0019-z
113. Mackerness, S., John, C. F., Jordan, B., and Thomas, B. (2001). Early signaling components in ultraviolet-B responses: distinct roles for different reactive oxygen species and nitric oxide. FEBS Lett. 489, 237-242. doi: 10.1016/S0014-5793(01)02103-2
114. Manai, J., Gouia, H., and Corpas, F. J. (2014). Redox and nitric oxide homeostasis are affected in tomato (Solanum lycopersicum) roots under salinity-induced oxidative stress. J. Plant Physiol. 171, 1028-1035. doi: 10.1016/j.jplph.2014.03.012
115. Mangano, S., Silberstein, S., and Santa-María, G. E. (2008). Point mutations in the barley HvHAK1 potassium transporter lead to improved K+-nutrition and enhanced resistance to salt stress. FEBS Lett. 582, 3922-3928. doi: 10.1016/j.febslet.2008.10.036
116. Manjunatha, G., Lokesh, V., and Neelwarne, B. (2010). Nitric oxide in fruit ripening: trends and opportunities. Biotechnol. Adv. 28, 489-499. doi: 10.1016/j.biotechadv.2010.03.001
117. Mannick, J. B. (2001). S-Nitrosylation of mitochondrial caspases. J. Cell Biol. 154, 1111-1116. doi: 10.1083/jcb.200104008
118. Manoli, A., Begheldo, M., Genre, A., Lanfranco, L., Trevisan, S., and Quaggiotti, S. (2014). NO homeostasis is a key regulator of early nitrate perception and root elongation in maize. J. Exp. Bot. 65, 185-200. doi: 10.1093/jxb/ert358
119. Melo, P. M., Silva, L. S., Ribeiro, I., Seabra, A. R., and Carvalho, H. G. (2011). Glutamine synthetase is a molecular target of nitric oxide in root nodules of Medicago truncatula and is regulated by tyrosine nitration. Plant Physiol. 157, 1505-1517. doi: 10.1104/pp.111.186056
120. Meng, Z. B., Chen, L. Q., Suo, D., Li, G. X., Tang, C. X., and Zheng, S. J. (2012). Nitric oxide is the shared signalling molecule in phosphorus- and iron-deficiency-induced formation of cluster roots in white lupin (Lupinus albus). Ann. Bot. 109, 1055-1064. doi: 10.1093/aob/mcs024
121. Miller, G., Suzuki, N., Ciftci-Yilmaz, S., and Mittler, R. (2010). Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ. 33, 453-467. doi: 10.1111/j.1365-3040.2009.02041.x
122. Młodzińska, E., Kłobus, G., Christensen, M. D., and Fuglsang, A. T. (2015). The plasma membrane H(+) -ATPase AHA2 contributes to the root architecture in response to different nitrogen supply. Physiol. Plant. 154, 270-282. doi: 10.1111/ppl.12305
123. Moncada, S., and Erusalimsky, J. D. (2002). Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat. Rev. Mol. Cell Biol. 3, 214-220. doi: 10.1038/nrm762
124. Monreal, J. A., Arias-Baldrich, C., Tossi, V., Feria, A. B., Rubio-Casal, A., García-Mata, C., et al. (2013). Nitric oxide regulation of leaf phosphoenolpyruvate carboxylase-kinase activity: implication in sorghum responses to salinity. Planta 238, 859-869. doi: 10.1007/s00425-013-1933-x
125. Moriconi, J. I., Buet, A., Simontacchi, M., and Santa-María, G. E. (2012). Near-isogenic wheat lines carrying altered function alleles of the Rht-1 genes exhibit differential responses to potassium deprivation. Plant Sci. 18, 199-207. doi: 10.1016/j.plantsci.2011.10.011
126. Munns, R. (1993). Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses. Plant Cell Environ. 16, 15-24. doi: 10.1111/j.1365-3040.1993.tb00840.x
127. Mur, L. A. J., Mandon, J., Persijn, S., Cristescu, S. M., Moshkov, I. E., Novikova, G. V., et al. (2013). Nitric oxide in plants: an assessment of the current state of knowledge.AoB Plants 5, ls052. doi: 10.1093/aobpla/pls052
128. Neill, S., Barros, R., Bright, J., Desikan, R., Hancock, J., Harrison, J., et al. (2008). Nitric oxide, stomatal closure, and abiotic stress. J. Exp. Bot. 59, 165-176. doi: 10.1093/jxb/erm293
129. Neill, S. J., Desikan, R., Clarke, A., and Hancock, J. T. (2002) Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol. 128, 13-16. doi: 10.1104/pp.010707
130. Neill, S. J., Desikan, R., and Hancock, J. T. (2003). Nitric oxide signalling in plants.New Phytol. 159, 11-35. doi: 10.1046/j.1469-8137.2003.00804.x
131. Niu, Y. F., Chai, R. S., Jin, G. L., Wang, H., Tang, C. X., and Zhang, Y. S. (2013). Responses of root architecture development to low phosphorus availability: a review.Ann. Bot. 112, 391-408. doi: 10.1093/aob/mcs285
132. Noritake, T., Kawakita, K., and Doke, N. (1996). Nitric oxide induces phytoalexin accumulation in potato tuber tissues. Plant Cell Physiol. 37, 113-116. doi: 10.1093/oxfordjournals.pcp.a028908
133. Pagnussat, G. C., Lanteri, M. L., Lombardo, M. C., and Lamattina, L. (2004). Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol. 135, 279-286. doi: 10.1104/pp.103.038554
134. Pagnussat, G. C., Simontacchi, M., Puntarulo, S., and Lamattina, L. (2002). Nitric oxide is required for root organogenesis. Plant Physiol. 129, 954-956. doi: 10.1104/pp.004036
135. Palmieri, M. C., Lindermayr, C., Bauwe, H., Steinhauser, C., and Durner, J. (2010). Regulation of plant glycine decarboxylase by s-nitrosylation and glutathionylation.Plant Physiol. 152, 1514-1528. doi: 10.1104/pp.109.152579
136. Patel, R. P., McAndrew, J., Sellak, H., White, C. R., Jo, H., Freeman, B. A., et al. (1999). Biological aspects of reactive nitrogen species. Biochim. Biophys. Acta 1411, 385-400. doi: 10.1016/S0005-2728(99)00028-6
137. Perazzolli, M., Dominici, P., Romero-Puertas, M. C., Zago, E., Zeier, J., Sonoda, M., et al. (2004). Arabidopsis nonsymbiotic hemoglobin AHb1 modulates nitric oxide bioactivity. Plant Cell 16, 2785-2794. doi: 10.1105/tpc.104.025379
138. Planchet, E., Jagadis Gupta, K., Sonoda, M., and Kaiser, W. M. (2005). Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J. 41, 732-743. doi: 10.1111/j.1365-313X.2005.02335.x
139. Procházková, D., and Wilhelmová, N. (2011). Nitric oxide, reactive nitrogen species and associated enzymes during plant senescence. Nitric Oxide 24, 61-65. doi: 10.1016/j.niox.2011.01.005
140. Pyo, Y. J., Gierth, M., Schroeder, J. I., and Cho, M. H. (2010). High-affinity K+ transport in Arabidopsis: AtHAK5 and AKT1 are vital for seedling establishment and postgermination growth under low-potassium conditions. Plant Physiol. 153, 863-875. doi: 10.1104/pp.110.154369
141. Radi, R. (1998). Peroxynitrite reactions and diffusion in biology. Chem. Res. Toxicol.11, 720-721. doi: 10.1021/tx980096z
142. Ribeiro, D. A., Desikan, R., Bright, J., Confraria, A., Harrison, J., Hancock, J. T., et al. (2009). Differential requirement for NO during ABA-induced stomatal closure in turgid and wilted leaves. Plant Cell Environ. 32, 46-57. doi: 10.1111/j.1365-3040.2008.01906.x
143. Rizzini, L., Favory, J.-J., Cloix, C., Faggionato, D., O'Hara, A., Kaiserli, E., et al. (2011). Perception of UV-B by the Arabidopsis UVR8 protein. Science 332, 103-106. doi: 10.1126/science.1200660
144. Rockel, P. (2002). Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J. Exp. Bot. 53, 103-110. doi: 10.1093/jexbot/53.366.103
145. Rosales, E. P., Iannone, M. F., Groppa, M. D., and Benavides, M. P. (2011). Nitric oxide inhibits nitrate reductase activity in wheat leaves. Plant Physiol. Biochem. 49, 124-130. doi: 10.1016/j.plaphy.2010.10.009
146. Rose, T., and Wissuwa, M. (2012). Rethinking internal phosphorus utilization efficiency: a new approach is needed to improve PUE in grain crops. Adv. Agron. 116, 185-217. doi: 10.1016/B978-0-12-394277-7.00005-1
147. Royo, B., Moran, J. F., Ratcliffe, G. R., and Gupta, K. J. (2015). Nitric oxide induces the alternative oxidase pathway in Arabidopsis seedlings deprived of inorganic phosphate. J. Exp. Bot. 66, 6273-6280. doi: 10.1093/jxb/erv338
148. Rubbo, H. (2000). Nitric oxide reaction with lipid peroxyl radicals spares alpha -tocopherol during lipid peroxidation. Greater oxidant protection from the pair nitric oxide/alpha -tocopherol than alpha -tocopherol/ascorbate. J. Biol. Chem. 275, 10812-10818. doi: 10.1074/jbc.275.15.10812
149. Rubbo, H., and Radi, R. (2008). Protein and lipid nitration: role in redox signaling and injury. Biochim. Biophys. Acta 1780, 1318-1324. doi: 10.1016/j.bbagen.2008.03.007
150. Rubio, F., Alemán, F., Nieves-Cordones, M., and Martínez, V. (2010). Studies onArabidopsis athak5, atakt1 double mutants disclose the range of concentrations at which AtHAK5, AtAKT1 and unknown systems mediate K+ uptake. Physiol. Plant.139, 220-228. doi: 10.1111/j.1399-3054.2010.01354.x
151. Sainz, M., Calvo-Begueria, L., Pérez-Rontomé, C., Wienkoop, S., Abián, J., Staudinger, C., et al. (2015). Leghemoglobin is nitrated in functional legume nodules in a tyrosine residue within the heme cavity by a nitrite/peroxide-dependent mechanism. Plant J.81, 723-735. doi: 10.1111/tpj.12762
152. Santa-Cruz, D. M., Pacienza, N. A., Polizio, A. H., Balestrasse, K. B., Tomaro, M. L., and Yannarelli, G. G. (2010). Nitric oxide synthase-like dependent NO production enhances heme oxygenase up-regulation in ultraviolet-B-irradiated soybean plants.Phytochemistry 71, 1700-1707. doi: 10.1016/j.phytochem.2010.07.009
153. Santa-Cruz, D. M., Pacienza, N. A., Zilli, C. G., Tomaro, M. L., Balestrasse, K. B., and Yannarelli, G. G. (2014). Nitric oxide induces specific isoforms of antioxidant enzymes in soybean leaves subjected to enhanced ultraviolet-B radiation. J. Photochem. Photobiol. 141, 202-209. doi: 10.1016/j.jphotobiol.2014.09.019
154. Santa-Maria, G. E., Danna, C. H., and Czibener, C. (2000). High-affinity potassium transport in barley roots. Ammonium-sensitive and -insensitive pathways. Plant Physiol. 123, 297-306. doi: 10.1104/pp.123.1.297
155. Santa-María, G. E., Moriconi, J. I., and Oliferuk, S. (2015). Internal efficiency of nutrient utilization: what is it and how to measure it during vegetative plant growth? J. Exp. Bot. 66, 3011-3018. doi: 10.1093/jxb/erv162
156. Santos, C. X., Bonini, M. G., and Augusto, O. (2000). Role of the carbonate radical anion in tyrosine nitration and hydroxylation by peroxynitrite. Arch. Biochem. Biophys. 377, 146-152. doi: 10.1006/abbi.2000.1751
157. Sanz, L., Albertos, P., Mateos, I., Sanchez-Vicente, I., Lechon, T., Fernandez-Marcos, M., et al. (2015). Nitric oxide (NO) and phytohormones crosstalk during early plant development. J. Exp. Bot. 66, 2857-2868. doi: 10.1093/jxb/erv213
158. Sanz-Luque, E., Ocaña-Calahorro, F., Llamas, A., Galvan, A., and Fernandez, E. (2013). Nitric oxide controls nitrate and ammonium assimilation in Chlamydomonas reinhardtii. J. Exp. Bot. 64, 3373-3383. doi: 10.1093/jxb/ert175
159. Schäfer, U., Schneider, A., and Neugebauer, E. (2000). Identification of a nitric oxide-regulated zinc finger containing transcription factor using motif-directed differential display. Biochim. Biophys. Acta 1494, 269-276. doi: 10.1016/S0167-4781(00)00249-9
160. Scuffi, D., Álvarez, C., Laspina, N., Gotor, C., Lamattina, L., and García-Mata, C. (2014). Hydrogen sulfide generated by L-cysteine desulfhydrase acts upstream of nitric oxide to modulate abscisic acid-dependent stomatal closure. Plant Physiol. 166, 2065-2076. doi: 10.1104/pp.114.245373
161. Shabala, S., and Pottosin, I. (2014). Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance. Physiol. Plant.151, 257-279. doi: 10.1111/ppl.12165
162. Shao, R., Wang, K., and Shangguan, Z. (2010). Cytokinin-induced photosynthetic adaptability of Zea mays L. to drought stress associated with nitric oxide signal: probed by ESR spectroscopy and fast OJIP fluorescence rise. J. Plant Physiol. 167, 472-479. doi: 10.1016/j.jplph.2009.10.020
163. Shen, H., Chen, J., Wang, Z., Yang, C., Sasaki, T., Yamamoto, Y., et al. (2006). Root plasma membrane H+-ATPase is involved in the adaptation of soybean to phosphorus starvation. J. Exp. Bot. 57, 1353-1362. doi: 10.1093/jxb/erj111
164. Shen, J., Yuan, L., Zhang, J., Li, H., Bai, Z., Chen, X., et al. (2011). Phosphorus dynamics: from soil to plant. Plant Physiol. 156, 997-1005. doi: 10.1104/pp.111.175232
165. Shi, H.-T., Li, R.-J., Cai, W., Liu, W., Wang, C.-L., and Lu, Y.-T. (2012). Increasing nitric oxide content in Arabidopsis thaliana by expressing rat neuronal nitric oxide synthase resulted in enhanced stress tolerance. Plant Cell Physiol. 53, 344-357. doi: 10.1093/pcp/pcr181
166. Shi, H., Ye, T., Zhu, J.-K., and Chan, Z. (2014). Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis. J. Exp. Bot. 65, 4119-4131. doi: 10.1093/jxb/eru184
167. Shi, S., Wang, G., Wang, Y., Zhang, L., and Zhang, L. (2005). Protective effect of nitric oxide against oxidative stress under ultraviolet-B radiation. Nitric Oxide 13, 1-9. doi: 10.1016/j.niox.2005.04.006
168. Simontacchi, M., Buet, A., Lamattina, L., and Puntarulo, S. (2012). Exposure to nitric oxide increases the nitrosyl-iron complexes content in sorghum embryonic axes.Plant Sci. 183, 159-166. doi: 10.1016/j.plantsci.2011.08.006
169. Singh, S., Agrawal, S. B., and Agrawal, M. (2014). UVR8 mediated plant protective responses under low UV-B radiation leading to photosynthetic acclimation. J. Photochem. Photobiol. 137, 67-76. doi: 10.1016/j.jphotobiol.2014.03.026
170. Singh, S. P., Singh, Z., and Swinny, E. E. (2009). Postharvest nitric oxide fumigation delays fruit ripening and alleviates chilling injury during cold storage of Japanese plums (Prunus salicina Lindell). Postharvest Biol. Technol. 53, 101-108. doi: 10.1016/j.postharvbio.2009.04.007
171. Sokolovski, S., and Blatt, M. R. (2004). Nitric oxide block of outward-rectifying K+ channels indicates direct control by protein nitrosylation in guard cells. Plant Physiol.136, 4275-4284. doi: 10.1104/pp.104.050344
172. Spalding, E. P. (1999). Potassium uptake supporting plant growth in the absence of AKT1 channel activity. Inhibition by ammonium and stimulation by sodium. J. Gen. Physiol. 113, 909-918. doi: 10.1085/jgp.113.6.909
173. Stöhr, C., Strube, F., Marx, G., Ullrich, W. R., and Rockel, P. (2001). A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite. Planta 212, 835-841. doi: 10.1007/s004250000447
174. Stoimenova, M., Igamberdiev, A. U., Gupta, K. J., and Hill, R. D. (2007). Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria. Planta 226, 465-474. doi: 10.1007/s00425-007-0496-0
175. Stuehr, D. J. (1999). Mammalian nitric oxide synthases. Biochim. Biophys. Acta 1411, 217-230. doi: 10.1016/S0005-2728(99)00016-X
176. Sun, H., Li, J., Song, W., Tao, J., Huang, S., Chen, S., et al. (2015). Nitric oxide generated by nitrate reductase increases nitrogen uptake capacity by inducing lateral root formation and inorganic nitrogen uptake under partial nitrate nutrition in rice. J. Exp. Bot. 66, 2449-2459. doi: 10.1093/jxb/erv030
177. Tanou, G., Filippou, P., Belghazi, M., Job, D., Diamantidis, G., Fotopoulos, V., et al. (2012). Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J. 72, 585-599. doi: 10.1111/j.1365-313X.2012.05100.x
178. Tattini, M., Loreto, F., Fini, A., Guidi, L., Brunetti, C., Velikova, V., et al. (2015). Isoprenoids and phenylpropanoids are part of the antioxidant defense orchestrated daily by drought-stressed Platanus × acerifolia plants during Mediterranean summers. New Phytol. 207, 613-626. doi: 10.1111/nph.13380
179. Terrile, M. C., París, R., Calderón-Villalobos, L. I. A., Iglesias, M. J., Lamattina, L., Estelle, M., et al. (2012). Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis transport inhibitor response 1 auxin receptor. Plant J.70, 492-500. doi: 10.1111/j.1365-313X.2011.04885.x
180. Tewari, R. K., Prommer, J., and Watanabe, M. (2013). Endogenous nitric oxide generation in protoplast chloroplasts. Plant Cell Rep. 32, 31-44. doi: 10.1007/s00299-012-1338-5
181. Tian, X., and Lei, Y. (2006). Nitric oxide treatment alleviates drought stress in wheat seedlings. Biol. Plant. 50, 775-778. doi: 10.1007/s10535-006-0129-7
182. Tossi, V., Amenta, M., Lamattina, L., and Cassia, R. (2011). Nitric oxide enhances plant ultraviolet-B protection up-regulating gene expression of the phenylpropanoid biosynthetic pathway. Plant Cell Environ. 34, 909-921. doi: 10.1111/j.1365-3040.2011.02289.x
183. Tossi, V., Lamattina, L., and Cassia, R. (2009). An increase in the concentration of abscisic acid is critical for nitric oxide-mediated plant adaptive responses to UV-B irradiation. New Phytol. 181, 871-879. doi: 10.1111/j.1469-8137.2008.02722.x
184. Tossi, V., Lamattina, L., Jenkins, G. I., and Cassia, R. (2014). Ultraviolet-B-induced stomatal closure in Arabidopsis is regulated by the UV resistance locus 8 photoreceptor in a nitric oxide-dependent mechanism. Plant Physiol. 164, 2220-2230. doi: 10.1104/pp.113.231753
185. Tossi, V., Lombardo, C., Cassia, R., and Lamattina, L. (2012). Nitric oxide and flavonoids are systemically induced by UV-B in maize leaves. Plant Sci. 19, 103-109. doi: 10.1016/j.plantsci.2012.05.012
186. Trapet, P., Kulik, A., Lamotte, O., Jeandroz, S., Bourque, S., Nicolas-Francès, V., et al. (2015). NO signaling in plant immunity: a tale of messengers. Phytochemistry 112, 72-79. doi: 10.1016/j.phytochem.2014.03.015
187. Trevisan, S., Manoli, A., and Quaggiotti, S. (2014). NO signaling is a key component of the root growth response to nitrate in Zea mays L. Plant Signal. Behav. 9, e28290. doi: 10.4161/psb.28290
188. Trevisan, S., Manoli, A., Ravazzolo, L., Botton, A., Pivato, M., Masi, A., et al. (2015). Nitrate sensing by the maize root apex transition zone: a merged transcriptomic and proteomic survey. J. Exp. Bot. 66, 3699-3715. doi: 10.1093/jxb/erv165
189. Tuteja, N. (2007). Abscisic acid and abiotic stress signaling. Plant Signal. Behav. 2, 135-138. doi: 10.4161/psb.2.3.4156
190. Uchida, A., Jagendorf, A. T., Hibino, T., Takabe, T., and Takabe, T. (2002). Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci. 163, 515-523. doi: 10.1016/S0168-9452(02)00159-0
191. Urzica, E. I., Casero, D., Yamasaki, H., Hsieh, S. I., Adler, L. N., Karpowicz, S. J., et al. (2012). Systems and trans-system level analysis identifies conserved iron deficiency responses in the plant lineage. Plant Cell 24, 3921-3948. doi: 10.1105/tpc.112.102491
192. Valderrama, R., Corpas, F. J., Carreras, A., Fernández-Ocaña, A., Chaki, M., Luque, F., et al. (2007). Nitrosative stress in plants. FEBS Lett. 581, 453-461. doi: 10.1016/j.febslet.2007.01.006
193. Vanin, A. F., Svistunenko, D. A., Mikoyan, V. D., Serezhenkov, V. A., Fryer, M. J., Baker, N. R., et al. (2004). Endogenous superoxide production and the nitrite/nitrate ratio control the concentration of bioavailable free nitric oxide in leaves. J. Biol. Chem. 279, 24100-24107. doi: 10.1074/jbc.M312601200
194. Van Ree, K., Gehl, B., Chehab, E. W., Tsai, Y.-C., and Braam, J. (2011). Nitric oxide accumulation in Arabidopsis is independent of NOA1 in the presence of sucrose. Plant J. 68, 225-233. doi: 10.1111/j.1365-313X.2011.04680.x
195. Veneklaas, E. J., Lambers, H., Bragg, J., Finnegan, P. M., Lovelock, C. E., Plaxton, W. C., et al. (2012). Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol. 195, 306-320. doi: 10.1111/j.1469-8137.2012.04190.x
196. Vitart, V., Baxter, I., Doerner, P., and Harper, J. F. (2001). Evidence for a role in growth and salt resistance of a plasma membrane H+-ATPase in the root endodermis.Plant J. 27, 191-201. doi: 10.1046/j.1365-313x.2001.01081.x
197. Vivancos, P. D., Dong, Y., Ziegler, K., Markovic, J., Pallardó, F. V., Pellny, T. K., et al. (2010). Recruitment of glutathione into the nucleus during cell proliferation adjusts whole-cell redox homeostasis in Arabidopsis thaliana and lowers the oxidative defence shield. Plant J. 64, 825-838. doi: 10.1111/j.1365-313X.2010.04371.x
198. Wang, B. L., Tang, X. Y., Cheng, L. Y., Zhang, A. Z., Zhang, W. H., Zhang, F. S., et al. (2010). Nitric oxide is involved in phosphorus deficiency-induced cluster-root development and citrate exudation in white lupin. New Phytol. 187, 1112-1123. doi: 10.1111/j.1469-8137.2010.03323.x
199. Wang, Y., Feng, H., Qu, Y., Cheng, J., Zhao, Z., Zhang, M., et al. (2006). The relationship between reactive oxygen species and nitric oxide in ultraviolet-B-induced ethylene production in leaves of maize seedlings. Environ. Exp. Bot. 57, 51-61. doi: 10.1016/j.envexpbot.2005.04.009
200. Wang, Y., Li, L., Cui, W., Xu, S., Shen, W., and Wang, R. (2011). Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351, 107-119. doi: 10.1007/s11104-011-0936-2
201. Wang, Z., Straub, D., Yang, H., Kania, A., Shen, J., Ludewig, U., et al. (2014). The regulatory network of cluster-root function and development in phosphate-deficient white lupin (Lupinus albus) identified by transcriptome sequencing. Physiol. Plant.151, 323-338. doi: 10.1111/ppl.12187
202. Watt, M. (1999). Proteoid roots. Physiology and development. Plant Physiol. 121, 317-323. doi: 10.1104/pp.121.2.317
203. Werner, A. K., and Witte, C.-P. (2011). The biochemistry of nitrogen mobilization: purine ring catabolism. Trends Plant Sci. 16, 381-387. doi: 10.1016/j.tplants.2011.03.012
204. White, P. J., and Brown, P. H. (2010). Plant nutrition for sustainable development and global health. Ann. Bot. 105, 1073-1080. doi: 10.1093/aob/mcq085
205. Williamson, L. C. (2001). Phosphate availability regulates root system architecture inArabidopsis. Plant Physiol. 126, 875-882. doi: 10.1104/pp.126.2.875
206. Wink, D. A., and Mitchell, J. B. (1998). Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic. Biol. Med. 25, 434-456. doi: 10.1016/S0891-5849(98)00092-6
207. Wissuwa, M. (2003). How do plants achieve tolerance to phosphorus deficiency? Small causes with big effects. Plant Physiol. 133, 1947-1958. doi: 10.1104/pp.103.029306
208. Wu, A. P., Gong, L., Chen, X., and Wang, J. X. (2014). Interactions between nitric oxide, gibberellic acid, and phosphorus regulate primary root growth in Arabidopsis.Biol. Plant. 58, 335-340. doi: 10.1007/s10535-014-0408-7
209. Xia, J., Kong, D., Xue, S., Tian, W., Li, N., Bao, F., et al. (2014). Nitric oxide negatively regulates AKT1-mediated potassium uptake through modulating vitamin B6 homeostasis in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 111, 16196-16201. doi: 10.1073/pnas.1417473111
210. Xu, J., Yin, H., Li, Y., and Liu, X. (2010). Nitric oxide is associated with long-term zinc tolerance in Solanum nigrum. Plant Physiol. 154, 1319-1334. doi: 10.1104/pp.110.162982
211. Yamasaki, H., Sakihama, Y., and Takahashi, S. (1999). An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends Plant Sci. 4, 128-129. doi: 10.1016/S1360-1385(99)01393-X
212. Yanagisawa, S. (2014). Transcription factors involved in controlling the expression of nitrate reductase genes in higher plants. Plant Sci. 229, 167-171. doi: 10.1016/j.plantsci.2014.09.006
213. Yannarelli, G. G., Noriega, G. O., Batlle, A., and Tomaro, M. L. (2006). Heme oxygenase up-regulation in ultraviolet-B irradiated soybean plants involves reactive oxygen species. Planta 224, 1154-1162. doi: 10.1007/s00425-006-0297-x
214. Yu, M., Lamattina, L., Spoel, S. H., and Loake, G. J. (2014). Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytol. 202, 1142-1156. doi: 10.1111/nph.12739
215. Zaharieva, T. B., and Abadía, J. (2003). Iron deficiency enhances the levels of ascorbate, glutathione, and related enzymes in sugar beet roots. Protoplasma 221, 269-275. doi: 10.1007/s00709-002-0051-6
216. Zeng, C.-L., Liu, L., Wang, B.-R., Wu, X.-M., and Zhou, Y. (2011). Physiological effects of exogenous nitric oxide on Brassica juncea seedlings under NaCl stress. Biol. Plant.55, 345-348. doi: 10.1007/s10535-011-0051-5
217. Zeppel, M. J. B., Harrison, S. P., Adams, H. D., Kelley, D. I., Li, G., Tissue, D. T., et al. (2015). Drought and resprouting plants. New Phytol. 206, 583-589. doi: 10.1111/nph.13205
218. Zhang, H. (1998). An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407-409. doi: 10.1126/science.279.5349.407
219. Zhang, Y., Wang, L., Liu, Y., Zhang, Q., Wei, Q., and Zhang, W. (2006). Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta 224, 545-555. doi: 10.1007/s00425-006-0242-z
220. Zhao, D.-Y., Tian, Q.-Y., Li, L.-H., and Zhang, W.-H. (2007a). Nitric oxide is involved in nitrate-induced inhibition of root elongation in Zea mays. Ann. Bot. 100, 497-503. doi: 10.1093/aob/mcm142
221. Zhao, M.-G., Tian, Q.-Y., and Zhang, W.-H. (2007b). Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiol.144, 206-217. doi: 10.1104/pp.107.096842
222. Zhao, L., Zhang, F., Guo, J., Yang, Y., Li, B., and Zhang, L. (2004). Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol. 134, 849-857. doi: 10.1104/pp.103.030023
223. Zheng, C., Jiang, D., Liu, F., Dai, T., Liu, W., Jing, Q., et al. (2009). Exogenous nitric oxide improves seed germination in wheat against mitochondrial oxidative damage induced by high salinity. Environ. Exp. Bot. 67, 222-227. doi: 10.1016/j.envexpbot.2009.05.002