Hydrogen peroxide signaling in plant development and abiotic responses: Crosstalk with nitric oxide and calcium

Frontiers in Plant Science

Volumn 7, Issue MAR2016, 2016, Pages

  Niu, Lijuan ^a   Liao, Weibiao ^a  

^a GANSU AGRICULTURAL UNIVERSITY   (China)

Author keywords

Calcium (Ca2+); Crosstalk; Hydrogen peroxide (H2O2); Nitric oxide (NO); Signal molecule

Indexed keywords

EID: 84960126790     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.00230     Document Type: Review

References (127)

1. Alberto, G., Cabrera, M. D., Josefa, H., Contreras, R. A., Bernardo, M., and Alejandra, M. (2012). Cross talk among calcium, hydrogen peroxide, and nitric oxide and activation of gene expression involving calmodulins and calcium-dependent protein kinases inulva compressa exposed to copper excess. Plant Physiol. 158, 1451-1462. doi: 10.1104/pp.111.191759
2. Alemayehu, A., Zelinová, V., Boèová, B., Huttová, J., Mistrík, I., and Tamás, L. (2015). Enhanced nitric oxide generation in root transition zone during the early stage of cadmium stress is required for maintaining root growth in barley. Plant Soil 390, 213-222. doi: 10.1007/s11104-015-2397-5
3. Asada, K. (2006). Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 141, 391-396. doi: 10.1104/pp.106.082040
4. Ashraf, M. A., Rasheed, R., Hussain, I., Iqbal, M., Haider, M. Z., Parveen, S., et al. (2015). Hydrogen peroxide modulates antioxidant system and nutrient relation in maize (Zea mays L.) under water-deficit conditions. Arch. Agron. Soil Sci. 61, 507-523. doi: 10.1080/03650340.2014.938644
5. 2 during pea seed germination: a combined proteomic and hormone profiling approach. Plant Cell Environ. 34, 1907-1919. doi: 10.1111/j.1365-3040.2011.02386.x
6. Begara-Morales, J. C., Sánchez-Calvo, B., Chaki, M., Valderrama, R., Mata-Pérez, C., López-Jaramillo, J., et al. (2013). Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J. Exp. Bot. 65, 527-538. doi: 10.1093/jxb/ert396
7. Ben Rejeb, K., Vos, L. D., Le Disquet, I., Leprince, A. S., Bordenave, M., Maldiney, R., et al. (2015). Hydrogen peroxide produced by NADPH oxidases increases proline accumulation during salt or mannitol stress in Arabidopsis thaliana. New Phytol. 208, 1138-1148. doi: 10.1111/nph.13550
8. Brewer, T. F., Garcia, F. J., Onak, C. S., Carroll, K. S., and Chang, C. J. (2015). Chemical approaches to discovery and study of sources and targets of hydrogen peroxide redox signaling through NAPDH oxidase proteins. Annu. Rev. Biochem. 84, 765-790. doi: 10.1146/annurev-biochem-060614-034018
9. Brychkova, G., Yarmolinsky, D., Fluhr, R., and Sagi, M. (2012). The determination of sulfite levels and its oxidation in plant leaves. Plant Sci. 190, 123-130. doi: 10.1016/j.plantsci.2012.04.004
10. Chang, Q., and Tang, H. (2014). Optical determination of glucose and hydrogen peroxide using a nanocomposite prepared from glucose oxidase and magnetite nanoparticles immobilized on graphene oxide. Microchim. Acta 181, 527-534. doi: 10.1007/s00604-013-1145-x
11. Chen, J., Xiang, L., Chao, W., Yin, S. S., Li, X. L., Hu, W. J., et al. (2015). Nitric oxide ameliorates zinc oxide nanoparticles-induced phytotoxicity in rice seedlings. J. Hazard. Mater. 297, 173-182. doi: 10.1016/j.jhazmat.2015.04.077
12. Chen, Z. H., Wang, Y. Z., Wang, J. W., Babla, M., Zhao, C., García-Mata, C., et al. (2016). Nitrate reductase mutation alters potassium nutrition as well as nitric oxide-mediated control of guard cell ion channels in Arabidopsis. New Phytol. 209, 1456-1469. doi: 10.1111/nph.13714
13. Cheng, X. X., Yu, M., Zhang, N., Zhou, Z. Q., Xu, Q. T., Mei, F. Z., et al. (2015). Reactive oxygen species regulate programmed cell death progress of endosperm in winter wheat (Triticum aestivum L.) under waterlogging. Protoplasma. doi: 10.1007/s00709-015-0811-8. [Epub ahead of print].
14. Cona, A., Rea, G., Botta, M., Corelli, F., Federico, R., and Angelini, R. (2006). Flavin-containing polyamine oxidase is a hydrogen peroxide source in the oxidative response to the protein phosphatase inhibitor cantharidin in Zea mays L. J. Exp. Bot. 57, 2277-2289. doi: 10.1093/jxb/erj195
15. Corpas, F. J., Barroso, J. B., and Del Río, L. A. (2004). Enzymatic sources of nitric oxide in plant cells-beyond one protein-one function. New Phytol. 162, 246-248. doi: 10.1111/j.1469-8137.2004.01058.x
16. Dat, J., Vandenabeele, S., Vranová, E., Van Montagu, M., Inzé, D., and Van Breusegem, F. (2000). Dual action of the active oxygen species during plant stress responses. Cell Mol. Life Sci. 57, 779-795. doi: 10.1007/s000180050041
17. 2+channels. Plant J. 49, 377-386. doi: 10.1111/j.1365-313X.2006.02971.x
18. Dickinson, B. C., and Chang, C. J. (2011). Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat. Chem. Biol. 7, 504-511. doi: 10.1038/nchembio.607
19. Duan, X., Li, X., Ding, F., Zhao, J., Guo, A., Zhang, L., et al. (2015). Interaction of nitric oxide and reactive oxygen species and associated regulation of root growth in wheat seedlings under zinc stress. Ecotox. Environ. Safe 113, 95-102. doi: 10.1016/j.ecoenv.2014.11.030
20. Esringu, A., Aksakal, O., Tabay, D., and Kara, A. A. (2015). Effects of sodium nitroprusside (SNP) pretreatment on UV-B stress tolerance in lettuce (Lactuca sativaL.) seedlings. Environ. Sci. Pollut. Res. 23, 589-597. doi: 10.1007/s11356-015-5301-1
21. Fan, H. F., Du, C. X., Ding, L., and Xu, Y. L. (2013). Effects of nitric oxide on the germination of cucumber seeds and antioxidant enzymes under salinity stress. Acta Physiol. Plant 35, 2707-2719. doi: 10.1007/s11738-013-1303-0
22. Fan, J., Chen, K., Amombo, E., Hu, Z., Chen, L., and Fu, J. (2015). Physiological and molecular mechanism of nitric oxide (NO) involved in bermudagrass response to cold stress. PLoS ONE 10:e0132991. doi: 10.1371/journal.pone.0132991
23. 4 nanoparticles for chemiluminescence sensing of hydrogen peroxide and glucose. Analyst 137, 1225-1231. doi: 10.1039/c2an16105b
24. Förstermann, U., Closs, E. I., Pollock, J. S., Nakane, M., Schwarz, P., Gath, I., et al. (1994). Nitric oxide synthase isozymes. Characterization, purification, molecular cloning, and functions. Hypertension 23, 1121-1131. doi: 10.1161/01.HYP.23.6.1121
25. Foyer, C. H., and Noctor, G. (2003). Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol. Plant 119, 355-364. doi: 10.1034/j.1399-3054.2003.00223.x
26. Francoz, E., Ranocha, P., Nguyen-Kim, H., Jamet, E., Burlat, V., and Dunand, C. (2015). Roles of cell wall peroxidases in plant development. Phytochemistry 112, 15-21. doi: 10.1016/j.phytochem.2014.07.020
27. García-Mata, C., and Lamattina, L. (2013). Gasotransmitters are emerging as new guard cell signaling molecules and regulators of leaf gas exchange. Plant Sci. 201, 66-73. doi: 10.1016/j.plantsci.2012.11.007
28. Ge, X. M., Cai, H. L., Lei, X., Zou, X., Yue, M., and He, J. M. (2015). Heterotrimeric G protein mediates ethylene-induced stomatal closure via hydrogen peroxide synthesis in Arabidopsis. Plant J. 82, 138-150. doi: 10.1111/tpj.12799
29. 2+ release. Cell Calcium 58, 237-245. doi: 10.1016/j.ceca.2015.05.005
30. González, A., de los Ángeles Cabrera, M., Henríquez, M. J., Contreras, R. A., Morales, B., and Moenne, A. (2012). Cross talk among calcium, hydrogen peroxide, and nitric oxide and activation of gene expression involving calmodulins and calcium-dependent protein kinases in Ulva compressa exposed to copper excess. Plant Physiol. 158, 1451-1462. doi: 10.1104/pp.111.191759
31. Grivennikova, V. G., and Vinogradov, A. D. (2013). Partitioning of superoxide and hydrogen peroxide production by mitochondrial respiratory complex I. BBA-MOL. Cell. Res. 1827, 446-454. doi: 10.1016/j.bbabio.2013.01.002
32. Guo, F., Okamoto, M., and Crawford, N. M. (2003). Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302, 100-103. doi: 10.1126/science.1086770
33. 2and nitric oxide interactions mediated cold-induced S-adenosylmethionine synthetase in Medicago sativa subsp. falcata that confers cold tolerance through up-regulating polyamine oxidation. Plant Biotechnol. J. 12, 601-612. doi: 10.1111/pbi.12166
34. 2mitigate drought stress in wheat. Cereal Res. Commun. 42, 450-462. doi: 10.1556/CRC.2013.0066
35. 2+ influx across the plasma membrane of root cells inArabidopsis seedlings. New Phytol. 205, 695-706. doi: 10.1111/nph.12990
36. He, J. M., Ma, X. G., Zhang, Y., Sun, T. F., Xu, F. F., Chen, Y. P., et al. (2013). Role and interrelationship of Gα protein, hydrogen peroxide, and nitric oxide in ultraviolet B-induced stomatal closure in Arabidopsis leaves. Plant Physiol. 161, 1570-1583. doi: 10.1104/pp.112.211623
37. 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
38. Hernández-Barrera, A., Velarde-Buendía, A., Zepeda, I., Sanchez, F., Quinto, C., Sánchez-Lopez, R., et al. (2015). Hyper, a hydrogen peroxide sensor, indicates the sensitivity of the Arabidopsis root elongation zone to aluminum treatment. Sensors 15, 855-867. doi: 10.3390/s150100855
39. Himschoot, E., Beeckman, T., Friml, J., and Vanneste, S. (2015). Calcium is an organizer of cell polarity in plants. Biochim. Biophys. Acta 1853, 2168-2172. doi: 10.1016/j.bbamcr.2015.02.017
40. Hu, X., Bidney, D. L., Yalpani, N., Duvick, J. P., Crasta, O., Folkerts, O., et al. (2003). Overexpression of a gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower. Plant Physiol. 133, 170-181. doi: 10.1104/pp.103.024026
41. 2 production in leaves of maize (Zea mays) plants. New Phytol.173, 27-38. doi: 10.1111/j.1469-8137.2006.01888.x
42. 2+ signal contributing to the synthesis and emission of monoterpenes regulated by light intensity in Lilium 'siberia'. Plant Physiol. Biochem. 91, 1-9. doi: 10.1016/j.plaphy.2015.03.005
43. Huang, A. X., Wang, Y. S., She, X. P., Mu, J., and Zhao, J. L. (2015). Copper amine oxidase-catalysed hydrogen peroxide involves production of nitric oxide in darkness-induced stomatal closure in broad bean. Funct. Plant Biol. 42, 1057-1067. doi: 10.1071/FP15172
44. Huang, S. S., Chen, J., Dong, X. J., Patton, J., Pei, Z. M., and Zheng, H. L. (2012). Calcium and calcium receptor CAS promote Arabidopsis thaliana de-etiolation. Physiol. Plant.144, 73-82. doi: 10.1111/j.1399-3054.2011.01523.x
45. Iakimova, E. T., and Woltering, E. J. (2015). Nitric oxide prevents wound-induced browning and delays senescence through inhibition of hydrogen peroxide accumulation in fresh-cut lettuce. Innov. Food Sci. Emerg. Technol. 30, 157-169. doi: 10.1016/j.ifset.2015.06.001
46. Jahan, A. A., and Anis, M. (2014). Changes in antioxidative enzymatic responses during acclimatization of in vitro raised plantlets of Cardiospermum halicacabum L. against oxidative stress. J. Plant Physiol. Pathol. 4, 2. doi: 10.4172/2329-955x.1000137
47. Jansen, M. A. K., and Bornman, J. F. (2012). UV-B radiation: from generic stressor to specific regulator. Physiol. Plant. 145, 501-504. doi: 10.1111/j.1399-3054.2012.01656.x
48. Kapoor, D., Sharma, R., Handa, N., Kaur, H., Rattan, A., Yadav, P., et al. (2015). Redox Homeostasis in Plants under Abiotic Stress: role of electron carriers, energy metabolism mediators and proteinaceous thiols. Front. Environ. Sci. 3:13. doi: 10.3389/fenvs.2015.00013
49. Karpets, Y. V., Kolupaev, Y. E., and Vayner, A. A. (2015). Functional interaction between nitric oxide and hydrogen peroxide during formation of wheat seedling induced heat resistance. Russ. J. Plant Physiol. 62, 65-70. doi: 10.1134/S1021443714060090
50. Kaur, G., Singh, H. P., Batish, D. R., Mahajan, P., Kohli, R. K., and Rishi, V. (2015). Exogenous nitric oxide (NO) interferes with lead (Pb)-induced toxicity by detoxifying reactive oxygen species in hydroponically grown wheat (triticum aestivum) roots.PLoS ONE 10:e0138713. doi: 10.1371/journal.pone.0138713
51. 2 production and gene expression of antioxidant enzymes in kimchi cabbage (Brassica rapa var. glabraRegel) seedlings regulated by plant development and nitrosative stress-triggered cell death. Plant Biotechnol. Rep. 9, 67-78. doi: 10.1007/s11816-015-0343-x
52. 2+ level to counteract effect of abscisic acid in seed germination. Plant Physiol. 167, 1630-1642. doi: 10.1104/pp.114.251298
53. Kovacs, I., Durner, J., and Lindermayr, C. (2015). Crosstalk between nitric oxide and glutathione is required for NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1)-dependent defense signaling in Arabidopsis thaliana. New Phytol. 208, 860-872. doi: 10.1111/nph.13502
54. Krifka, S., Hiller, K. A., Spagnuolo, G., Jewett, A., Schmalz, G., and Schweikl, H. (2012). The influence of glutathione on redox regulation by antioxidant proteins and apoptosis in macrophages exposed to 2-hydroxyethyl methacrylate (HEMA). Biomaterials 33, 5177-5186. doi: 10.1016/j.biomaterials.2012.04.013
55. Lang, T., Sun, H. M., Li, N. Y., Lu, Y. J., Shen, Z. D., Jing, X. S., et al. (2014). Multiple signaling networks of extracellular ATP, hydrogen peroxide, calcium, and nitric oxide in the mediation of root ion fluxes in secretor and non-secretor mangroves under salt stress. Aquat. Bot. 119, 33-43. doi: 10.1016/j.aquabot.2014.06.009
56. Li, J., Wang, X., Zhang, Y., Jia, H., and Bi, Y. (2011). cGMP regulates hydrogen peroxide accumulation in calcium-dependent salt resistance pathway in Arabidopsis thalianaroots. Planta 234, 709-722. doi: 10.1007/s00425-011-1439-3
57. Li, J. H., Liu, Y. Q., Lü, P., Lin, H. F., Bai, Y., Wang, X. C., et al. (2009). A signaling pathway linking nitric oxide production to heterotrimeric G protein and hydrogen peroxide regulates extracellular calmodulin induction of stomatal closure inArabidopsis. Plant Physiol. 150, 114-124. doi: 10.1104/pp.109.137067
58. Li, P., Zhao, C., Zhang, Y., Wang, X., Wang, X., Wang, J., et al. (2016). Calcium alleviates cadmium-induced inhibition on root growth by maintaining auxin homeostasis inArabidopsis seedlings. Protoplasma 253, 185-200. doi: 10.1007/s00709-015-0810-9
59. 2+, cGMP, and MAPKs during adventitious rooting in mung bean seedlings. In Vitro Cell Dev. Biol. 46, 142-148. doi: 10.1007/s11627-009-9275-x
60. Li, Z. G., Luo, L. J., and Sun, Y. F. (2015). Signal crosstalk between nitric oxide and hydrogen sulfide may be involved in hydrogen peroxide -induced thermotolerance in maize seedlings. Russ. J. Plant Physiol. 62, 507-514. doi: 10.1134/S1021443715030127
61. Liao, W. B., Huang, G. B., Yu, J. H., Zhang, M. L., and Shi, X. L. (2011). Nitric oxide and hydrogen peroxide are involved in indole-3-butyric acid-induced adventitious root development in marigold. J. Hortic. Sci. Biotech. 86, 159-165. doi: 10.1080/14620316.2011.11512742
62. Liao, W. B., Xiao, H. L., and Zhang, M. L. (2009). Role and relationship of nitric oxide and hydrogen peroxide in adventitious root development of marigold. Acta Physiol. Plant. 31, 1279-1289. doi: 10.1007/s11738-009-0367-3
63. Liao, W. B., Xiao, H. L., and Zhang, M. L. (2010). Effect of nitric oxide and hydrogen peroxide on adventitious root development from cuttings of ground-cover chrysanthemum and associated biochemical changes. J. Plant Growth Regul. 29, 338-348. doi: 10.1007/s00344-010-9140-5
64. Liao, W. B., Zhang, M. L., and Yu, J. H. (2013). Role of nitric oxide in delaying senescence of cut rose flowers and its interaction with ethylene. Sci. Horticult. 155, 30-38. doi: 10.1016/j.scienta.2013.03.005
65. 2-induced adventitious root development in marigold. J. Plant Growth Regul. 31, 253-264. doi: 10.1007/s00344-011-9235-7
66. Liao, W. B., Zhang, M. L., Huang, G. B., and Yu, J. H. (2012b). Hydrogen peroxide in the vase solution increases vase life and keeping quality of cut Oriental × Trumpet hybrid lily 'Manissa'. Sci. Horticult. 139, 32-38. doi: 10.1016/j.scienta.2012.02.040
67. Lin, A. H., Wang, Y. Q., Tang, J. Y., Xue, P., Li, C. L., Liu, L. C., et al. (2012). Nitric oxide and protein S-Nitrosylation are integral to hydrogen peroxide-induced leaf cell death in Rice. Plant Physiol. 158, 451-464. doi: 10.1104/pp.111.184531
68. Liu, J., Macarisin, D., Wisniewski, M., Sui, Y., By, S., Norelli, J., et al. (2013). Production of hydrogen peroxide and expression of ros-generating genes in peach flower petals in response to host and non-host fungal pathogens. Plant Pathol. 62, 820-828. doi: 10.1111/j.1365-3059.2012.02683.x
69. Liu, W., Li, R. J., Han, T. T., Cai, W., Fu, Z. W., and Lu, Y. T. (2015). Salt stress reduces root meristem size by nitric oxide-mediated modulation of auxin accumulation and signaling in Arabidopsis. Plant Physiol. 168, 343-356. doi: 10.1104/pp.15.00030
70. Liu, W. W., Chen, H. B., Lu, X. Y., Rahman, M. J., Zhong, S., and Zhou, B. Y. (2015). Identification of nitric oxide responsive genes in the floral buds of Litchi chinensis. Biol. Plant. 59, 115-122. doi: 10.1007/s10535-014-0466-x
71. 2-and NO-induced antioxidant enzyme activities. Plant Physiol. Biochem. 47, 132-138. doi: 10.1016/j.plaphy.2008.10.006
72. Lu, Y., Li, N., Sun, J., Hou, P., Jing, X., Zhu, H., et al. (2013). Exogenous hydrogen peroxide, nitric oxide and calcium mediate root ion fluxes in two non-secretor mangrove species subjected to NaCl stress. Tree Physiol. 33, 81-95. doi: 10.1093/treephys/tps119
73. 2 in auxin-induced lateral root formation in Arabidopsis. Plant Mol. Biol. 85, 49-61. doi: 10.1007/s11103-013-0168-3
74. Ma, F. F., Lu, R., Liu, H. Y., Shi, B., Zhang, J. H., Tan, M. P., et al. (2012). Nitric oxide-activated calcium/calmodulin-dependent protein kinase regulates the abscisic acid-induced antioxidant defence in maize. J. Exp. Bot. 63, 4835-4847. doi: 10.1093/jxb/ers161
75. Mayer, B., and Hemmens, B. (1998). Biosynthesis and action of nitric oxide in mammalian cells. Trends Biochem. Sci. 22, 477-481. doi: 10.1016/S0968-0004(97)01147-X
76. Mehler, A. H. (1951). Studies on reactions of illuminated chloroplasts. II. Stimulation and inhibition of the reaction with molecular oxygen. Arch. Biochem. Biophys.33, 339-351. doi: 10.1016/0003-9861(51)90082-3
77. Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 7, 405-410. doi: 10.1016/S1360-1385(02)02312-9
78. Mohamed, H. E., Hemeida, A. E., and Mohamed, A. G. (2015). Role of hydrogen peroxide pretreatment on developing antioxidant capacity in the leaves of tomato plant (Lycopersicon esculentum) grown under saline stress. Int. J. Adv. Res. 3, 878-879.
79. Nathan, C. F., and Hibbs, J. B. (1991). Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol. 3, 65-70. doi: 10.1016/0952-7915(91)90079-G
80. Navrot, N., Rouhier, N., Gelhaye, E., and Jacquot, J. P. (2007). Reactive oxygen species generation and antioxidant systems in plant mitochondria. Physiol. Plant. 129, 185-195. doi: 10.1111/j.1399-3054.2006.00777.x
81. Noelia, F., Mayta, M. L., Lodeyro, A. F., Denise, S., Natalia, C., Carlos, G., 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
82. Nyathi, Y., and Baker, A. (2006). Plant peroxisomes as a source of signaling molecules.Biochim. Biophys. Acta 1763, 1478-1495. doi: 10.1016/j.bbamcr.2006.08.031
83. 2accumulation in field-grown aspen and birch is linked to foliar ultrastructure and peroxisomal activity. New Phytol. 161, 791-799. doi: 10.1111/j.1469-8137.2003.00981.x
84. Orabi, S. A., Dawood, M. G., and Salman, S. R. (2015). Comparative study between the physiological role of hydrogen peroxide and salicylic acid in alleviating the harmful effect of low temperature on tomato plants grown under sand-ponic culture. Sci. Agric. 9, 49-59. doi: 10.15192/PSCP.SA.2015.1.9.4959
85. 2+ entry. Sci. Signal. 8, 1-32. doi: 10.1126/scisignal.2005672
86. 2. J. Exp. Bot. 66, 5853-5866. doi: 10.1093/jxb/erv294
87. Rasul, S., Dubreuil-Maurizi, C., Lamotte, O., Koen, E., Poinssot, B., Alcaraz, G., et al. (2012). Nitric oxide production mediates oligogalacturonide-triggered immunity and resistance to botrytis cinerea in Arabidopsis thaliana. Plant Cell Environ. 35, 1483-1499. doi: 10.1111/j.1365-3040.2012.02505.x
88. Remans, T., Opdenakker, K., Smeets, K., Mathijsen, D., Vangronsveld, J., and Cuypers, A. (2010). Metal-specific and NADPH oxidase dependent changes in lipoxygenase and NADPH oxidase gene expression in Arabidopsis thaliana exposed to cadmium or excess copper. Funct. Plant Biol. 37, 532-544. doi: 10.1071/FP09194
89. 2-induced calcium signature in Arabidopsis thaliana roots. Plant J. 77, 136-145. doi: 10.1111/tpj.12372
90. Rockel, P., Strube, F., Rockel, A., Wildt, J., and Kaiser, W. M. (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
91. Sathiyaraj, G., Srinivasan, S., Kim, Y. J., Lee, O. R., Parvin, S., Balusamy, S. R. D., et al. (2014). Acclimation of hydrogen peroxide enhances salt tolerance by activating defense-related proteins in Panax ginseng C.A. Meyer. Mol. Biol. Rep. 41, 3761-3771. doi: 10.1007/s11033-014-3241-3
92. Serrano, I., Romero-Puertas, M. C., Rodríguez-Serrano, M., Sandalio, L. M., and Olmedilla, A. (2012). Peroxynitrite mediates programmed cell death both in papillar cells and in self-incompatible pollen in the olive (Olea europaea L.). J. Exp. Bot. 63, 1479-1493. doi: 10.1093/jxb/err392
93. 2+pathway implication during Xenopus laevis vitellogenesis. Zygote 23, 99-110. doi: 10.1017/S0967199413000324
94. 2+decoding mechanisms. New Phytol. 204, 782-790. doi: 10.1111/nph.13031
95. Shan, C., Yan, Z., and Liu, M. (2015). Nitric oxide participates in the regulation of the ascorbate-glutathione cycle by exogenous jasmonic acid in the leaves of wheat seedlings under drought stress. Protoplasma 252, 1397-1405. doi: 10.1007/s00709-015-0756-y
96. Shi, C., Qi, C., Ren, H. Y., Huang, A. X., Hei, S. M., and She, X. P. (2015). Ethylene mediates brassinosteroid-induced stomatal closure via Gα protein-activated hydrogen peroxide and nitric oxide production in Arabidopsis. Plant J. 82, 280-301. doi: 10.1111/tpj.12815
97. 2-induced stomatal movement in tomato.New Phytol. 208, 342-353. doi: 10.1111/nph.13621
98. Shi, Y., Liu, J., Xin, N., Gu, R., Qin Zhu, L., Zhang, C., et al. (2015). Signals induced by exogenous nitric oxide and their role in controlling brown rot disease caused by monilinia fructicola in postharvest peach fruit. J. Gen. Plant Pathol. 81, 68-76. doi: 10.1007/s10327-014-0562-y
99. Shoresh, M., Spivak, M., and Bernstein, N. (2011). Involvement of calcium-mediated effects on ROS metabolism in the regulation of growth improvement under salinity. Free Radic. Biol. Med. 51, 1221-1234. doi: 10.1016/j.freeradbiomed.2011.03.036
100. Skiba, U., Smith, K. A., and Fowler, D. (1993). Nitrification and denitrification as sources of nitric oxide and nitrous oxide in a sandy loam soil. Soil Biol. Biochem. 25, 1527-1536. doi: 10.1016/0038-0717(93)90007-X
101. 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
102. Tan, J., Wang, C., Xiang, B., Han, R., and Guo, Z. (2013). Hydrogen peroxide and nitric oxide mediated cold- and dehydration-induced myo-inositol phosphate synthase that confers multiple resistances to abiotic stresses. Plant Cell Environ. 36, 288-299. doi: 10.1111/j.1365-3040.2012.02573.x
103. Tang, R. J., Zhao, F. G., Garcia, V. J., Kleist, T. J., Yang, L., Zhang, H. X., et al. (2015). Tonoplast CBL-CIPK calcium signaling network regulates magnesium homeostasis inArabidopsis. Proc. Natl. Acad. Sci. U.S.A. 112, 3134-3139. doi: 10.1073/pnas.1420944112
104. Tanou, G., Job, C., Belghazi, M., Molassiotis, A., Diamantidis, G., and Job, D. (2010). Proteomic signatures uncover hydrogen peroxide and nitric oxide cross-talk signaling network in citrus plants. J. Proteome Res. 9, 5994-6006. doi: 10.1021/pr100782h
105. Tanou, G., Job, C., Rajjou, L., Arc, E., Belghazi, M., Diamantidis, G., et al. (2009). Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J. 60, 795-804. doi: 10.1111/j.1365-313X.2009.04000.x
106. 2+ against NaCl induced salt stress in two lentil (Lens culinaris) cultivars. Afr. J. Agr. Res. 10, 2389-2398. doi: 10.5897/AJAR2014.9479
107. Tossi, V., Lamattina, L., Jenkins, G. I., and Cassia, R. O. (2014). Ultraviolet-B-induced stomatal closure in Arabidopsis is regulated by the UV RESISTANCE LOCUS8 photoreceptor in a nitric oxide-dependent mechanism. Plant Physiol. 164, 2220-2230. doi: 10.1104/pp.113.231753
108. 2+-dependent protein kinases are induced by drought and high-salt stresses in Arabidopsis thaliana. Mol. Gen. Genet.244, 331-340. doi: 10.1007/BF00286684
109. Vandelle, E., Poinssot, B., Wendehenne, D., Bentejac, M., and Alain, P. (2006). Integrated signaling network involving calcium, nitric oxide, and active oxygen species but not mitogen-activated protein kinases in BcPG1-elicited grapevine defenses. Mol. Plant Microbe Interact. 19, 429-440. doi: 10.1094/MPMI-19-0429
110. Vavilala, S. L., Gawde, K. K., Sinha, M., and D'Souza, J. S. (2015). Programmed cell death is induced by hydrogen peroxide but not by excessive ionic stress of sodium chloride in the unicellular green alga Chlamydomonas reinhardtii. Eur. J. Phycol. 50, 422-438. doi: 10.1080/09670262.2015.1070437
111. 2+ dynamics inArabidopsis. Plant Cell 27, 3190-3212. doi: 10.1105/tpc.15.00509
112. Wang, L., Guo, Y., Jia, L., Chu, H., Zhou, S., Chen, K., et al. (2014). Hydrogen peroxide acts upstream of nitric oxide in the heat shock pathway in Arabidopsis seedlings. Plant Physiol. 164, 2184-2196. doi: 10.1104/pp.113.229369
113. Wang, P., Zhu, J. K., and Lang, Z. (2015). Nitric oxide suppresses the inhibitory effect of abscisic acid on seed germination by s-nitrosylation of snrk2 proteins. Plant Signal. Behav. 10:e1031939. doi: 10.1080/15592324.2015.1031939
114. Wang, W. H., Yi, X. Q., Han, A. D., Liu, T. W., Chen, J., Wu, F. H., et al. (2011). Calcium-sensing receptor regulates stomatal closure through hydrogen peroxide and nitric oxide in response to extracellular calcium in Arabidopsis. J. Exp. Bot. 63, 177-190. doi: 10.1093/jxb/err259
115. 2+ and actin filament organization during cell wall construction in pinus bungeana pollen tubes. New Phytol. 182, 851-862. doi: 10.1111/j.1469-8137.2009.02820.x
116. Wang, Y., Zhang, J., Li, J. L., and Ma, X. R. (2014). Exogenous hydrogen peroxide enhanced the thermotolerance of Festuca arundinacea and Lolium perenne by increasing the antioxidative capacity. Acta Physiol. Plant 36, 2915-2924. doi: 10.1007/s11738-014-1661-2
117. Wen, J. F., Gong, M., Liu, Y., Hu, J. L., and Deng, M. H. (2013). Effect of hydrogen peroxide on growth and activity of some enzymes involved in proline metabolism of sweet corn seedlings under copper stress. Sci. Horticult. 164, 366-371. doi: 10.1016/j.scienta.2013.09.031
118. 3 plants. EMBO. J. 16, 4806-4816. doi: 10.1093/emboj/16.16.4806
119. 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
120. Wu, D., Chu, H. Y., Jia, L. X., Chen, K. M., and Zhao, L. Q. (2015). A feedback inhibition between nitric oxide and hydrogen peroxide in the heat shock pathway in arabidopsis seedlings. Plant Growth Regul. 75, 503-509. doi: 10.1007/s10725-014-0014-x
121. 2+-permeable channels and pollen tube growth. Plant J. 63, 1042-1053. doi: 10.1111/j.1365-313X.2010.04301.x
122. Xiang, Z., Jin, W., Jing, Y., Wang, X. L., Zhao, Q. P., Kong, P. T., et al. (2015). Nitric oxide-associated protein1 (atnoa1) is essential for salicylic acid-induced root waving inArabidopsis thaliana. New Phytol. 207, 211-224. doi: 10.1111/nph.13327
123. Yu, Y., Yang, Z., Guo, K., Li, Z., Zhou, H., Wei, Y., et al. (2015). Oxidative damage induced by heat stress could be relieved by nitric oxide in trichoderma harzianumLTR-2. Curr. Microbiol. 70, 618-622. doi: 10.1007/s00284-014-0764-8
124. Zhang, H., Wang, W., Yin, H., Zhao, X., and Du, Y. (2012). Oligochitosan induces programmed cell death in tobacco suspension cells. Carbohyd. Polym. 87, 2270-2278. doi: 10.1016/j.carbpol.2011.10.059
125. Zhang, F., Wang, Y., Yang, Y., Wu, H., Wang, D., and Liu, J. (2007). Involvement of hydrogen peroxide and nitric oxide in salt resistance in the calluses from Populus euphratica. Plant Cell Environ. 30, 775-785. doi: 10.1111/j.1365-3040.2007.01667.x
126. Zhou, L., Lan, W., Jiang, Y., Fang, W., and Luan, S. (2014). A calcium-dependent protein kinase interacts with and activates a calcium channel to regulate pollen tube growth.Mol. Plant 7, 369-376. doi: 10.1093/mp/sst125
127. 2 homeostasis in stomatal guard cells under drought stress. Plant Cell 27, 1445-1460. doi: 10.1105/tpc.15.00144