Reactive oxygen species (ROS): Beneficial companions of plants’ developmental processes

Frontiers in Plant Science

Volumn 7, Issue September2016, 2016, Pages

  Singh, Rachana ^a   Singh, Samiksha ^a   Parihar, Parul ^a   Mishra, Rohit K ^a   Tripathi, Durgesh K ^a   Singh, Vijay P ^b   Chauhan, Devendra K ^a   Prasad, Sheo M ^a  

^a UNIVERSITY OF ALLAHABAD   (India)

^b Govt Ramanuj Pratap Singhdev Post Graduate College   (India)

Author keywords

NADPH oxidases; Plant growth and development; Programmed cell death; Reactive oxygen species signaling; Seed germination

Indexed keywords

EID: 84989962815     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.01299     Document Type: Review

References (223)

1. Adachi, H., Nakano, T., Miyagawa, N., Ishihama, N., Yoshioka, M., Katou, Y., et al. (2015). WRKY transcription factors phosphorylated by MAPK regulate a plant immune NADPH oxidase in Nicotiana benthamiana. Plant Cell 27, 2645–2663. doi: 10.1105/tpc.15.00213
2. Aguirre, J., Rios-Momberg, M., Hewitt, D., and Hansberg, W. (2005). Reactive oxygen species and development in microbial eukaryotes.Trends Microbiol. 13, 111–118. doi: 10.1016/j.tim.2005.01.007
3. Aken, V., and Van Breusegem, F. (2015). Licensed to kill: mitochondria, chloroplasts, and cell death Olivier. Trends Plant Sci. 20, 754–766. doi: 10.1016/j.tplants.2015.08.002
4. Altartouri, B., and Geitmann, A. (2015). Understanding plant cell morphogenesis requires real-time monitoring of cell wall polymers.Curr. Opin. Plant Biol. 23, 76–82. doi: 10.1016/j.pbi.2014.11.007
5. Ambastha, A. K., Gong, T., Bolan, S., Dinh, T. A., and Lim, T. C. (2015). “Automated prognosis analysis for traumatic brain injury CT images,” in Proceeding of the 3rd Asian Conference on Pattern Recognition (ACPR), Beijing.
6. Amien, S., Kliwer, I., Márton, M. L., Debener, T., Geiger, D., Becker, D., et al. (2010). Defensin-like ZmES4 mediates pollen tube burst in maize via opening of the potassium channel KZM1. PLOS Biol. 8:e1000388. doi: 10.1371/journal.pbio.1000388
7. Apel, K., and Hirt, H. (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373–399. doi: 10.1146/annurev.arplant.55.031903.141701
8. 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
9. 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
10. Ashtamker, C., Kiss, V., Sagi, M., Davydov, O., and Fluhr, R. (2007). Diverse subcellular locations of cryptogein-induced reactive oxygen species production in tobacco bright yellow-2 cells. Plant Physiol. 143, 1817–1826. doi: 10.1104/pp.106.090902
11. Bahin, E., Bailly, C., Sotta, B., Kranner, I., Corbineau, F., and Leymarie, J. (2011). Crosstalk between reactive oxygen species and hormonal signaling pathways regulates grain dormancy in barley. Plant Cell Environ. 34, 980–993. doi: 10.1111/j.1365-3040.2011.02298.x
12. Bailly, C. (2004). Active oxygen species and antioxidants in seed biology. Seed Sci. Res. 14, 93–107. doi: 10.1079/SSR2004159
13. Bailly, C., El-Maarouf-Bouteau, H., and Corbineau, F. (2008). From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. C. R. Biol. 331, 806–814. doi: 10.1016/j.crvi.2008.07.022
14. 2+ activation of the NADPH oxidase 5 (NOX5). J. Biol. Chem. 279, 18583–18591. doi: 10.1074/jbc.M310268200
15. 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
16. Baxter, A., Mittler, R., and Suzuki, N. (2014). ROS as key players in plant stress signalling. J. Exp. Bot. 65, 1229–1240. doi: 10.1093/jxb/ert375
17. Bazin, J., Langlade, N., Vincourt, P., Arribat, S., Balzergue, S., El-Maarouf-Bouteau, H., et al. (2011). Targeted mRNA oxidation regulates sunflower seed dormancy alleviation during dry after-ripening. Plant Cell 23, 2196–2208. doi: 10.1105/tpc.111.086694
18. Bedard, K., and Krause, K. H. (2007). The Nox family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87, 245–313. doi: 10.1152/physrev.00044.2005
19. Beemster, G. T. S., Veylder, L. D., Vercruysse, S., West, S., Rombaut, D., Hummelen, P. V., et al. (2005). Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis. Plant Physiol. 138, 734–743. doi: 10.1104/pp.104.053884
20. Bewley, J. D., Bradford, K. J., Hilhorst, H. W. M., and Nonogaki, H. (2013). Seeds: Physiology of Development, Germination and Dormancy. Berlin: Springer.
21. Bhattacharjee, S. (2012). The language of reactive oxygen species signaling in plants. J. Bot. 2012, 985298. doi: 10.1155/2012/985298
22. Bhattacharjee, S. (2014). Membrane lipid peroxidation and its conflict of interest: the two faces of oxidative stress. Curr. Sci. 107, 1811–1823.
23. Bindschedler, L. V., Dewdney, J., Blee, K. A., Stone, J. M., Asai, T., Plotnikov, J., et al. (2006). Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J. 47, 851–863. doi: 10.1111/j.1365-313X.2006.02837.x
24. Boisson-Dernier, A., Lituiev, D. S., Nestorova, A., Franck, C. M., Thirugnanarajah, S., and Grossniklaus, U. (2013). ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases. PLOS Biol. 11:e1001719. doi: 10.1371/journal.pbio.1001719
25. Bollhöner, B., Prestele, J., and Tuominen, H. (2012). Xylem cell death: emerging understanding of regulation and function. J. Exp. Bot.63, 1081–1094. doi: 10.1093/jxb/err438
26. Bosch, M., and Franklin-Tong, N. (2007). Temporal and spatial activation of caspase-like enzymes induced by self-incompatibility in papaver pollen. Proc. Natl. Acad. Sci. U.S.A. 104, 18327–18332. doi: 10.1073/pnas.0705826104
27. Bosch, M., Poulter, N. S., Perry, R. M., Wilkins, K. A., and Franklin-Tong, V. E. (2010). Characterization of a legumain/vacuolar processing enzyme and YVADase activity in Papaver pollen. Plant Mol. Biol. 74, 381–393. doi: 10.1007/s11103-010-9681-9
28. Bouche, N., Fait, A., Bouchez, D., Moller, S. G., and Fromm, H. (2003). Mitochondrial succinic-semialdehyde dehydrogenase of the gamma-aminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants. Proc. Natl. Acad. Sci. U.S.A. 100, 6843–6848. doi: 10.1073/pnas.1037532100
29. Braidwood, L., Breuer, C., and Sugimoto, K. (2014). My body is a cage: mechanisms and modulation of plant cell growth. New Phytol.201, 388–402. doi: 10.1111/nph.12473
30. 2/cellulose synthase interacting 1 is essential for the functional association of cellulose synthase and microtubules in Arabidopsis. Plant Cell 24, 163–177. doi: 10.1105/tpc.111.093575
31. Cai, S., and Lashbrook, C. C. (2008). Stamen abscission zone transcriptome profiling reveals new candidates for abscission control: enhanced retention of floral organs in transgenic plants overexpressing Arabidopsis ZINC FINGER PROTEIN2. Plant Physiol. 146, 1305–1321. doi: 10.1104/pp.107.110908
32. 2-generating oxalate oxidase gene expression during wheat embryo germination. Plant J. 15, 165–171. doi: 10.1046/j.1365-313X.1998.00191.x
33. Cárdenas, L., McKenna, S. T., Kunkel, J. G., and Hepler, P. K. (2006). NAD(P)H oscillates in pollen tubes and is correlated with tip growth. Plant Physiol. 142, 1460–1468. doi: 10.1104/pp.106.087882
34. Carmody, M., Crisp, P. A., d’Alessandro, S., Ganguly, D., Gordon, M., Havaux, M., et al. (2016). Uncoupling high light responses from singlet oxygen retrograde signaling and spatial-temporal systemic acquired acclimation in Arabidopsis. Plant Physiol. 171, 1734–1749. doi: 10.1104/pp.16.00404
35. Cervantes, E. (2001). ROS in root gravitropism: the auxin messengers? Trends Plant Sci. 6, 556. doi: 10.1016/S1360-1385(01)02197-5
36. 2 elevation. J. Plant Pysiol. 169, 86–97. doi: 10.1016/j.jplph.2011.08.002
37. Chen, S. P., Lin, I. W., Chen, X., Huang, Y. H., Chang, H. C., Lo, H. S., et al. (2016). Sweet potato NAC transcription factor, IbNAC1, upregulates sporamin gene expression by binding the SWRE motif against mechanical wounding and herbivore attack. Plant J. 86, 234–248. doi: 10.1111/tpj.13171
38. 2 activates local and systemic cell death and defense response to bacterial pathogens. Plant Physiol. 145, 890–904. doi: 10.1104/pp.107.103325
39. Choi, W. G., Hilleary, R., Swanson, S. J., Kim, S. H., and Gilroy, S. (2016). Rapid, long distance electrical and calcium signaling in plants.Annu. Rev. Plant Biol. 67, 287–307. doi: 10.1146/annurev-arplant-043015-112130
40. Chopra, K. R. (2012). Leaf senescence and abiotic stresses share reactive oxygen species-mediated chloroplast degradation. Protoplasma 249, 469–481. doi: 10.1007/s00709-011-0308-z
41. Corbineau, F., Xia, Q., Bailly, C., and El-Maarouf-Bouteau, H. (2014). Ethylene, a key factor in the regulation of seed dormancy. Front. Plant Sci. 5:539. doi: 10.3389/fpls.2014.00539
42. Cosio, C., Vuillemin, L., De Meyer, M., Kevers, C., Penel, C., and Dunand, C. (2008). An anionic class III peroxidase from zucchini may regulate hypocotyl elongation thanks to its auxin oxidase activity. Planta 229, 823–836. doi: 10.1007/s00425-008-0876-0
43. Crescenzi, V., Belardinelli, M., and Rinaldi, C. (1997). Polysaccharides depolymerization via hydroxyl radicals attack in dilute aqueous solution. J. Carbo. Chem. 16, 561–572. doi: 10.1080/07328309708007335
44. de Pinto, M. C., Locato, V., and De Gara, L. (2012). Redox regulation in plant programmed cell death. Plant Cell Environ. 35, 234–244. doi: 10.1111/j.1365-3040.2011.02387.x
45. De Rybel, B., Vassileva, V., Parizot, B., Demeulenaere, M., Grunewald, W., Audenaert, D., et al. (2010). A novel aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr. Biol. 20, 1697–1706. doi: 10.1016/j.cub.2010.09.007
46. del Rio, L. A., Sandalio, L. M., Corpas, F. J., and Barroso, J. B. (2006). Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol. 141, 330–335.
47. Desikan, R., Reynolds, A., Hancock, J. T., and Neill, S. J. (1998). Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on defence gene expression in Arabidopsis suspension cultures. Biochem. J. 330, 115–120. doi: 10.1042/bj3300115
48. Diaz-Vivancos, P., Barba-Espin, G., and Hernandez, J. A. (2013). Elucidating hormonal/ROS networks during seed germination: insights and perspectives. Plant Cell Rep. 32, 1491–1502. doi: 10.1007/s00299-013-1473-7
49. Dietz, K. J. (2016). Thiol-based peroxidases and ascorbate peroxidases: why plants rely on multiple peroxidase systems in the photosynthesizing chloroplast? Mol. Cells 39, 20–25. doi: 10.14348/molcells.2016.2324
50. Drose, S., and Brandt, U. (2012). Molecular mechanisms of superoxide production by the mitochondrial respiratory chain. Adv. Exp. Med. Biol. 748, 145–169. doi: 10.1007/978-1-4614-3573-0_6
51. Duan, Q., Kita, D., Johnson, E. A., Aggarwal, M., Gates, L., Wu, H. M., et al. (2014). Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat. Commun. 5, 3129. doi: 10.1038/ncomms4129
52. Duan, Q., Kita, D., Li, C., Cheung, A. Y., and Wu, H. M. (2010). FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc. Natl. Acad. Sci. U.S.A. 107, 17821–17826. doi: 10.1073/pnas.1005366107
53. Dubrovsky, J. G., Sauer, M., Napsucialy-Mendivil, S., Ivanchenko, M. G., Friml, J., Shishkova, S., et al. (2008). Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc. Natl. Acad. Sci. U.S.A. 105, 8790–8794. doi: 10.1073/pnas.0712307105
54. Dunand, C., Crevecoeur, M., and Penel, C. (2007). Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. New Phytol. 174, 332–341. doi: 10.1111/j.1469-8137.2007.01995.x
55. Durme, M. V., and Nowack, M. K. (2016). Mechanisms of developmentally controlled cell death in plants. Curr. Opin. Plant Biol. 29, 29–37. doi: 10.1016/j.pbi.2015.10.013
56. El-Maarouf-Bouteau, H., and Bailly, C. (2008). Oxidative signaling in seed germination and dormancy. Plant Signal. Behav. 3, 175–182. doi: 10.4161/psb.3.3.5539
57. El-Maarouf-Bouteau, H., Meimoun, P., Job, C., Job, D., and Bailly, C. (2013). Role of protein and mRNA oxidation in seed dormancy and germination. Front. Plant Sci. 4:77. doi: 10.3389/fpls.2013.00077
58. Evans, M. J., Choi, W. G., Gilroy, S., and Morris, R. (2016). A ROS-assisted calcium wave dependent on AtRBOHD and TPC1 propagates the systemic response to salt stress in Arabidopsis roots. Plant Physiol. 171, 1771–1784. doi: 10.1104/pp.16.00215
59. Falhof, J., Pedersen, J. T., Fuglsang, A. T., and Palmgren, M. (2016). Plasma membrane H+-ATPase regulation in the center of plant physiology. Mol. Plant 9, 323–337. doi: 10.1016/j.molp.2015.11.002
60. Fang, Y., Liao, K., Du, H., Xu, Y., Song, H., Li, X., et al. (2015). A stress responsive NAC transcription factor SNAC3 confers heat and drought tolerance through modulation of reactive oxygen species in rice. J. Exp. Bot. 66, 6803–6817. doi: 10.1093/jxb/erv386
61. Fendrych, M., Van Hautegem, T., Van Durme, M., Olvera-Carrillo, Y., Huysmans, M., Karimi, M., et al. (2014). Programmed cell death controlled by ANAC033/SOMBRERO determines root cap organ size in Arabidopsis. Curr. Biol. 24, 931–940. doi: 10.1016/j.cub.2014.03.025
62. Finkelstein, R., Reeves, W., Ariizumi, T., and Steber, C. (2008). Molecular aspects of seed dormancy. Annu. Rev. Plant Biol. 59, 387–415. doi: 10.1146/annurev.arplant.59.032607.092740
63. Foreman, J., Demidchik, V., Bothwell, J. H., Mylona, P., Miedema, H., Torres, M. A., et al. (2003). Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422, 442–446. doi: 10.1038/nature01485
64. Foyer, C. H., and Noctor, G. (2005). Redox homeostasis and antioxidant signalling: a metabolic interface between stress perception and physiological responses. Plant Cell 17, 1866–1875. doi: 10.1105/tpc.105.033589
65. Foyer, C. H., and Noctor, G. (2013). Redox signaling in plants. Antioxid. Redox Signal. 18, 2087–2090. doi: 10.1089/ars.2013.5278
66. Foyer, C. H., and Noctor, G. (2016). Stress-triggered redox signalling: what’s in pROSpect? Plant Cell Environ. 39, 951–964. doi: 10.1111/pce.12621
67. Fukuda, H. (1996). Xylogenesis: initiation, progression and cell death. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 299–325. doi: 10.1146/annurev.arplant.47.1.299
68. Gadjev, I., Stone, J. M., and Gechev, T. S. (2008). Programmed cell death in plants: new insights into redox regulation and the role of hydrogen peroxide. Int. Rev. Cell Mol. Biol. 270, 87–144. doi: 10.1016/S1937-6448(08)01403-2
69. Gapper, C., and Dolan, L. (2006). Control of plant development by reactive oxygen species. Plant Physiol. 141, 341–345. doi: 10.1104/pp.106.079079
70. Gechev, T. S., Van Breusegem, F., Stone, J. M., Denev, I., and Laloi, C. (2006). Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays 28, 1091–1101. doi: 10.1002/bies.20493
71. Gessler, N. N., Aver’yanov, A. A., and Belozerskaya, T. A. (2007). Reactive oxygen species in regulation of fungal development.Biochemistry 72, 1091–1109.
72. Gill, S. S., and Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909–930. doi: 10.1016/j.plaphy.2010.08.016
73. Gilroy, S., Bialasek, M., Suzuki, N., Górecka, M., Devireddy, A. R., Karpinski, S., et al. (2016). ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol. 171, 1606–1615.
74. Halliwell, B., and Gutteridge, J. M. C. (1989). Free Radicals in Biology and Medicine. Oxford: Clarendon Press, 450–499.
75. Hautegem, T. V., Waters, A. J., Goodrich, J., and Nowack, M. K. (2015). Only in dying, life: programmed cell death during plant development. Trends Plant Sci. 20, 102–113. doi: 10.1016/j.tplants.2014.10.003
76. Hayashi, Y., Yamada, K., Shimada, T., Matsushima, R., Nishizawa, N. K., and Nishimura, M. A. (2001). proteinase-storing body that prepares for cell death or stresses in the epidermal cells of Arabidopsis. Plant Cell Physiol. 42, 894–899. doi: 10.1093/pcp/pce144
77. He, L., Ma, X., Li, Z., Jiao, Z., Li, Y., and Ow, D. W. (2016). Maize OXIDATIVE STRESS2 homologs enhance cadmium tolerance inArabidopsis through activation of a putative SAM-dependent methyltransferase gene. Plant Physiol. 171, 1675–1685. doi: 10.1104/pp.16.00220
78. Hepler, P. K., Kunkel, J. G., Rounds, C. M., and Winship, L. J. (2012). Calcium entry into pollen tubes. Trends Plant Sci. 17, 32–38. doi: 10.1016/j.tplants.2011.10.007
79. Hite, D. R., Auh, C., and Scandalios, J. G. (1999). Catalase activity and hydrogen peroxide levels are inversely correlated in maize scutella during seed germination. Redox Rep. 4, 29–34. doi: 10.1179/135100099101534710
80. Hohl, M., Greiner, H., and Schopfer, P. (1995). The cryptic growth response of maize coleoptiles and its relationship to H2O2 dependent cell wall stiffening. Physiol. Plant 94, 491–498. doi: 10.1034/j.1399-3054.1995.940318.x
81. Holdsworth, M. J., Bentsink, L., and Soppe, W. J. (2008). Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol. 179, 33–54. doi: 10.1111/j.1469-8137.2008.02437.x
82. Huang, A. H. C., Trelease, R. N., and Moore, T. S. (1983). Plant Peroxisomes. London: Academic Press.
83. Huang, S., Van Aken, O., Schwarzländer, M., Belt, K., and Millar, A. H. (2016). The roles of mitochondrial reactive oxygen species in cellular signaling and stress responses in plants. Plant Physiol. 171, 1551–1559. doi: 10.1104/pp.16.00166
84. Hulskamp, M. (2004). Plant trichomes: a model for cell differentiation. Nat. Rev. Mol. Cell Biol. 5, 471–480. doi: 10.1038/nrm1404
85. Ishibashi, Y., Koda, Y., Zheng, S. H., Yuasa, T., and Iwaya-Inoue, M. (2013). Regulation of soybean seed germination through ethylene production in response to reactive oxygen species. Ann. Bot. 111, 95–102. doi: 10.1093/aob/mcs240
86. Ishibashi, Y., Tawaratsumida, T., Kondo, K., Kasa, S., Sakamoto, M., Aoki, N., et al. (2012). Reactive oxygen species are involved in gibberellin/abscisic acid signaling in barley aleurone cells. Plant Physiol. 158, 1705–1714. doi: 10.1104/pp.111.192740
87. Ishibashi, Y., Tawaratsumida, T., Zheng, S. H., Yuasa, T., and Iwaya-Inoue, M. (2010). NADPH oxidases act as key enzyme on germination and seedling growth in barley (Hordeum vulgare L.). Plant Prod. Sci. 13, 45–52. doi: 10.1626/pps.13.45
88. Ishibashi, Y., Yamamoto, K., Tawaratsumida, T., Yuasa, T., and Iwaya-Inoue, M. (2008). Hydrogen peroxide scavenging regulates germination ability during wheat (Triticum aestivum L.) seed maturation. Plant Signal. Behav. 3, 183–188. doi: 10.4161/psb.3.3.5540
89. Jajic, I., Sarna, T., and Strzalka, K. (2015). Senescence, stress, and reactive oxygen species. Plants 4, 393–411.
90. Jiang, X., Gao, Y., Zhou, H., Chen, J., Wu, J., and Zhang, S. (2014). Apoplastic calmodulin promotes self-incompatibility pollen tube growth by enhancing calcium influx and reactive oxygen species concentration in Pyrus pyrifolia. Plant Cell Rep. 33, 255–263. doi: 10.1007/s00299-013-1526-y
91. Jomova, K., Vondrakova, D., Lawson, M., and Valko, M. (2010). Metals, oxidative stress and neurodegenerative disorders. Mol. Cell Biochem. 345, 91–104. doi: 10.1007/s11010-010-0563-x
92. Joo, J. H., Bae, Y. S., and Lee, J. S. (2001). Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol. 126, 1055–1060. doi: 10.1104/pp.126.3.1055
93. Joo, J. H., Yoo, H. J., Hwang, I., Lee, J. S., Nam, K. H., and Bae, Y. S. (2005). Auxin-induced reactive oxygen species production requires the activation of phosphatydil linositol 3-kinase. FEBS Lett. 579, 1243–1248. doi: 10.1016/j.febslet.2005.01.018
94. Kalogeris, T., Bao, Y., and Korthuis, R. J. (2014). Mitochondrial reactive oxygen species: a double edged sword in ischemia/reperfusion vs preconditioning. Redox Biol. 2, 702–714. doi: 10.1016/j.redox.2014.05.006
95. 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. Plant Sci. 3:13. doi: 10.3389/fenvs.2015.00013
96. Karuppanapandian, T., Moon, J. C., Kim, C., Manoharan, K., and Kim, W. (2011). Reactive oxygen species in plants: their generation, signal transduction, and scavenging mechanisms. Aust J. Crop Sci. 5, 709–725.
97. 2+-activated reactive oxygen species production by Arabidopsis RbohH and RbohJ is essential for proper pollen tube tip growth. Plant Cell 26, 1069–1080. doi: 10.1105/tpc.113.120642
98. Kerchev, P., Waszczak, C., Lewandowska, A., Willems, P., Shapiguzov, A., Li, Z., et al. (2016). Lack of GLYCOLATE OXIDASE1, but not GLYCOLATE OXIDASE2, attenuates the photorespiratory phenotype of CATALASE2-deficient Arabidopsis. Plant Physiol. 171, 1704–1719. doi: 10.1104/pp.16.00359
99. Khanna-Chopra, R. (2012). Leaf senescence and abiotic stresses share reactive oxygen species-mediated chloroplast degradation.Protoplasma 249, 469–481. doi: 10.1007/s00709-011-0308-z
100. Kleine, T., and Leister, D. (2016). Retrograde signaling: organelles go networking. Biochim. Biophys. Acta 1857, 1313–1325. doi: 10.1016/j.bbabio.2016.03.017
101. Konrad, K. R., Wudick, M. M., and Feijó, J. A. (2011). Calcium regulation of tip growth: new genes for old mechanisms. Curr. Opin. Plant Biol. 14, 721–730. doi: 10.1016/j.pbi.2011.09.005
102. Laloi, C., Apel, K., and Danon, A. (2004). Reactive oxygen signalling: the latest news. Curr. Opin. Plant Biol. 7, 323–328. doi: 10.1016/j.pbi.2004.03.005
103. Lam, E. (2004). Controlled cell death, plant survival and development. Nat. Rev. Mol. Cell Biol. 5, 305–315. doi: 10.1038/nrm1358
104. Lassig, R., Gutermuth, T., Bey, T. D., Konrad, K. R., and Romeis, T. (2014). Pollen tube NAD(P)H oxidases act as a speed control to dampen growth rate oscillations during polarized cell growth. Plant J. 78, 94–106. doi: 10.1111/tpj.12452
105. Lavenus, J., Goh, T., Roberts, I., Guyomarch, S., Lucas, M., De Smet, I., et al. (2013). Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci. 18, 450–458. doi: 10.1016/j.tplants.2013.04.006
106. Le, C. T., Brumbarova, T., Ivanov, R., Stoof, C., Weber, E., Mohrbacher, J., et al. (2016). ZINC FINGER OF ARABIDOPSIS THALIANA12 (ZAT12) interacts with FER-LIKE IRON DEFICIENCYINDUCED TRANSCRIPTION FACTOR (FIT) linking iron deficiency and oxidative stress responses. Plant Physiol. 170, 540–557. doi: 10.1104/pp.15.01589
107. Lee, S., Seo, P. J., Lee, H. J., and Park, C. M. (2012). A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. Plant J. 70, 831–844. doi: 10.1111/j.1365-313X.2012.04932.x
108. Lee, Y., Rubio, M. C., Alassimone, J., and Geldner, N. (2013). A mechanism for localized lignin deposition in the endodermis. Cell 153, 402–412. doi: 10.1016/j.cell.2013.02.045
109. Leymarie, J., Vitkauskaite, G., Hoang, H. H., Gendreau, E., Chazoule, V., Meimoun, P., et al. (2012). Role of reactive oxygen species in the regulation of Arabidopsis seed dormancy. Plant Cell Physiol. 53, 96–106. doi: 10.1093/pcp/pcr129
110. Li, N., Zhang, D. S., Liu, H. S., Yin, C. S., Li, X. X., Liang, W. Q., et al. (2006). The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18, 2999–3014. doi: 10.1105/tpc.106.044107
111. Libik-Konieczny, M., Kozieradzka-Kiszkurno, M., Desel, C., Michalec-Warzecha, Z., Miszalski, Z., and Konieczny, R. (2015). The localization of NADPH oxidase and reactive oxygen species in in vitro-cultured Mesembryanthemum crystallinum L. hypocotyls discloses their differing roles in rhizogenesis. Protoplasma 252, 477–487. doi: 10.1007/s00709-014-0692-2
112. Liszkay, A., Kenk, B., and Schopfer, P. (2003). Evidence for the involvement of cell wall peroxidase in the generation of hydroxyl radicals mediating extension growth. Planta 217, 658–667. doi: 10.1007/s00425-003-1028-1
113. Liu, Y., Ye, N., Liu, R., Chen, M., and Zhang, J. (2010). H2O2 mediates the regulation of ABA catabolism and GA biosynthesis inArabidopsis seed dormancy and germination. J. Exp. Bot. 61, 2979–2990. doi: 10.1093/jxb/erq125
114. Lovy-Wheeler, A., Kunkel, J. G., Allwood, E. G., Hussey, P. J., and Hepler, P. K. (2006). Oscillatory increases in alkalinity anticipate growth and may regulate actin dynamics in pollen tubes of lily. Plant Cell 18, 2182–2193. doi: 10.1105/tpc.106.044867
115. Lu, D., Wang, T., Persson, S., Mueller-Roeber, B., and Schippers, J. H. M. (2014). Transcriptional control of ROS homeostasis by KUODA1 regulates cell expansion during leaf development. Nat. commun. 5:3767. doi: 10.1038/ncomms4767
116. Lupini, A., Aranitia, F., Sunseri, F., and Abenavoli, M. R. (2013). Gravitropic response induced by coumarin: evidences of ROS distribution involvement. Plant Signal. Behav. 8: e23156. doi: 10.4161/psb.23156
117. Ma, F., Wang, L., Li, J., Samma, M. K., Xie, Y., Wang, R., et al. (2014). Interaction between HY1 and HO in auxin-induced lateral root formation in Arabidopsis. Plant Mol. Biol. 85, 49–61. doi: 10.1007/s11103-013-0168-3
118. Macpherson, N., Takeda, S., Shang, Z., Dark, A., Mortimer, J. C., Brownlee, C., et al. (2008). NADPH oxidase involvement in cellular integrity. Planta 227, 1415–1418. doi: 10.1007/s00425-008-0716-2
119. Mangano, S., Denita Juárez, S., and Estevez, J. M. (2016). ROS regulation of polar growth in plant cells. Plant Physiol. 171, 1593–1605. doi: 10.1104/pp.16.00191
120. Manzano, C., Pallero-Baena, M., Casimiro, I., De Rybel, B., Orman-Ligeza, B., Van Isterdael, G., et al. (2014). The emerging role of reactive oxygen species signaling during lateral root development. Plant Physiol. 165, 1105–1119. doi: 10.1104/pp.114.238873
121. Marchi, S., Giorgi, C., Suski, J. M., Agnoletto, C., Bononi, A., Bonora, M., et al. (2012). Mitochondria-ros crosstalk in the control of cell death and aging. J. Signal Transduct. 2012:329635. doi: 10.1155/2012/329635
122. Marino, D., Dunand, C., Puppo, A., and Pauly, N. (2012). A burst of plant NADPH oxidases. Trends Plant Sci. 17, 9–15. doi: 10.1016/j.tplants.2011.10.001
123. Marjamaa, K., Kukkola, E. M., and Fagerstedt, K. V. (2009). The role of xylem class III peroxidases in lignifications. J. Exp. Bot. 60, 367–376. doi: 10.1093/jxb/ern278
124. Matsuo, M., Johnson, J. M., Hieno, A., Tokizawa, M., Nomoto, M., Tada, Y., et al. (2015). High REDOX RESPONSIVE TRANSCRIPTION FACTOR1 levels result in accumulation of reactive oxygen species in Arabidopsis thaliana shoots and roots. Mol. Plant 8, 1253–1273. doi: 10.1016/j.molp.2015.03.011
125. Mattila, H., Khorobrykh, S., Havurinne, V., and Tyystjärvi, E. (2015). Reactive oxygen species: reactions and detection from photosynthetic tissues. J. Photochem. Photobiol. B 152 (Pt. B), 176–214. doi: 10.1016/j.jphotobiol.2015.10.001
126. McDonald, M. B. (1999). Seed deterioration: physiology, repair and assessment. Seed Sci. Tech. 27, 177–237.
127. Meir, S., Hunter, D. A., Chen, J. C., Halaly, V., and Reid, M. S. (2006). Molecular changes occurring during acquisition of abscission competence following auxin depletion in Mirabilis jalapa. Plant Physiol. 141, 1604–1616. doi: 10.1104/pp.106.079277
128. Messerli, M. A., and Robinson, K. R. (2007). MS channels in tip-growing systems: mechanosensitive ion channels, part A. Curr. Topic Membr. 58, 393–412. doi: 10.1016/S1063-5823(06)58015-9
129. Miransari, M., and Smith, D. L. (2014). Plant hormones and seed germination. Environ. Exp. Bot. 99, 110–121. doi: 10.1016/j.envexpbot.2013.11.005
130. Mittler, R., and Blumwald, E. (2010). Genetic engineering for modern agriculture: challenges and perspectives. Annu. Rev. Plant Biol. 61, 443–462. doi: 10.1146/annurev-arplant-042809-112116
131. Mittler, R., Vanderauwera, S., Suzuki, N., Miller, G., Tognetti, V. B., Vandepoele, K., et al. (2011). ROS signaling: the new wave? Trends Plant Sci. 16, 300–309. doi: 10.1016/j.tplants.2011.03.007
132. Moller, I. M. (2001). Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 561–591. doi: 10.1146/annurev.arplant.52.1.561
133. Moller, I. M., and Sweetlove, L. J. (2010). ROS signalling –specificity is required. Trends Plant Sci. 15, 370–374. doi: 10.1016/j.tplants.2010.04.008
134. Monshausen, G. B., Bibikova, T. N., Messerli, M. A., Shi, C., and Gilroy, S. (2007). Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc. Natl. Acad. Sci. U.S.A. 104, 20996–21001. doi: 10.1073/pnas.0708586104
135. 2+ regulates reactive oxygen species production and pH during mechanosensing in Arabidopsis roots. Plant Cell 21, 2341–2356. doi: 10.1105/tpc.109.068395
136. Monshausen, G. B., and Gilroy, S. (2009). Feeling green: mechanosensing in plants. Trends Cell Biol. 19, 228–235. doi: 10.1016/j.tcb.2009.02.005
137. 2+ follow oscillating increases in growth in root hairs of Arabidopsis. Plant Physiol. 147, 1690–1698. doi: 10.1104/pp.108.123638
138. Moriwaki, T., Miyazawa, Y., Kobayashi, A., Uchida, M., Watanabe, C., Fujii, N., et al. (2011). Hormonal regulation of lateral root development in Arabidopsis modulated by MIZ1 and requirement of GNOM activity for MIZ1 function. Plant physiol. 157, 1209–1220. doi: 10.1104/pp.111.186270
139. Müller, K., Linkies, A., Vreeburg, R. A. M., Fry, S. C., Krieger-Liszkay, A., and Luebner- Metzger, G. (2009). In vivo cell wall loosening by hydroxyl radicals during cress seed germination and elongation growth. Plant Physiol. 150, 1855–1865. doi: 10.1104/pp.109.139204
140. 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
141. Neill, S., Desikan, R., and Hancock, J. (2002). Hydrogen peroxide signalling. Curr. Opin. Plant Biol. 5, 388–395. doi: 10.1016/S1369-5266(02)00282-0
142. Noctor, G., De Paepe, R., and Foyer, C. H. (2007). Mitochondrial redox biology and homeostasis in plants. Trends Plant Sci. 12, 125–134. doi: 10.1016/j.tplants.2007.01.005
143. Nonogaki, H. (2014). Seed dormancy and germination-emerging mechanisms and new hypotheses. Front. Plant Sci. 5:233. doi: 10.3389/fpls.2014.00233
144. Ogawa, K., and Iwabuchi, M. (2001). A mechanism for promoting the germination of Zinnia elegans seeds by hydrogen peroxide. Plant Cell Physiol. 42, 286–291. doi: 10.1093/pcp/pce032
145. Oracz, K., El-Maarouf-Bouteau, H., Farrant, J. M., Copper, K., Belghazi, M., Job, C., et al. (2007). ROS production and protein oxidation as novel mechanism of seed dormancy alleviation. Plant J. 50, 452–465. doi: 10.1111/j.1365-313X.2007.03063.x
146. Palma, J. M., Corpas, F. J., and del Rio, L. A. (2009). Proteome of plant peroxisomes: new perspectives on the role of these organelles in cell biology. Proteomics 9, 2301–2312. doi: 10.1002/pmic.200700732
147. Panavas, T., and Rubinstein, B. (1998). Oxidative events during programmed cell death of daylily (Hemerocallis hybrid) petals. Plant Sci.133, 125–138. doi: 10.1016/S0168-9452(98)00034-X
148. Passaia, G., Queval, G., Bai, J., Margis-Pinheiro, M., and Foyer, C. H. (2014). The effects of redox controls mediated by glutathione peroxidases on root architecture in Arabidopsis thaliana. J. Exp. Bot. 65, 1403–1413. doi: 10.1093/jxb/ert486
149. Passardi, F., Penel, C., and Dunand, C. (2004). Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci.9, 534–540. doi: 10.1016/j.tplants.2004.09.002
150. Petrasek, J., and Friml, J. (2009). Auxin transport routes in plant development. Development 136, 2675–2688. doi: 10.1242/dev.030353
151. Petrov, V., Hille, J., Mueller-Roeber, B., and Gechev, T. S. (2015). ROS-mediated abiotic stress-induced programmed cell death in plants.Front. Plant Sci. 6:69. doi: 10.3389/fpls.2015.00069
152. Petrov, V. D., and Van Breusegem, F. (2012). Hydrogen peroxide –a central hub for information flow in plant cells. AoB Plants 2012, ls014. doi: 10.1093/aobpla/pls014
153. Pierson, E. S., Miller, D. D., Callaham, D. A., Shipley, A. M., Rivers, B. A., Cresti, M., et al. (1994). Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: effect of BAPTAtype buffers and hypertonic media. Plant Cell 6, 1815–1828. doi: 10.2307/3869910
154. Plackett, A. R. G., Thomas, S. G., Wilson, Z. A., and Hedden, P. (2011). Gibberellin control of stamen development: a fertile field. Trends Plant Sci. 16, 568–578. doi: 10.1016/j.tplants.2011.06.007
155. Pospisil, P. (2012). Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II. Biochimi Biophys. Acta 1817, 218–231. doi: 10.1016/j.bbabio.2011.05.017
156. Potikha, T. S., Collins, C. C., Johnson, D. I., Delmer, D. P., and Levine, A. (1999). The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers. Plant Physiol. 119, 849–858. doi: 10.1104/pp.119.3.849
157. Prasad, S. M., Kumar, S., Parihar, P., Singh, A., and Singh, R. (2015). Evaluating the combined effects of pretilachlor and UV-B on twoAzolla species. Pesti. Biochem. Physiol. 128, 45–56. doi: 10.1016/j.pestbp.2015.10.006
158. Puntarulo, S., Sanchez, R. A., and Boveris, A. (1988). Hydrogen peroxide metabolism in soybean embryonic axes at the onset of germination. Plant Physiol. 86, 626–630. doi: 10.1104/pp.86.2.626
159. Punwani, J. A., Rabiger, D. S., and Drews, G. N. (2007). MYB98 positively regulates a battery of synergid-expressed genes encoding filiform apparatus localized proteins. Plant Cell 19, 2557–2568. doi: 10.1105/tpc.107.052076
160. Qin, Y., and Yang, Z. (2011). Rapid tip growth: insights from pollen tubes. Semin. Cell Dev. Biol. 22, 816–824. doi: 10.1016/j.semcdb.2011.06.004
161. Rajhi, I., Yamauchi, T., Takahashi, H., Nishiuchi, S., Shiono, K., Watanabe, R., et al. (2011). Identification of genes expressed in maize root cortical cells during lysigenous aerenchyma formation using laser microdissection and microarray analyses. New Phytol. 190, 351–368. doi: 10.1111/j.1469-8137.2010.03535.x
162. Rentel, M. C., and Knight, M. R. (2004). Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol. 135, 1471–1479. doi: 10.1104/pp.104.042663
163. Rhoads, D. M., Umbach, A. L., Subbaiah, C. C., and Siedow, J. N. (2006). Mitochondrial reactive oxygen species. Contribution to oxidative stress and interorganellar signaling. Plant Physiol. 141, 357–366.
164. Roberts, K., and McCann, M. C. (2000). Xylogenesis: the birth of a corpse. Curr. Opin. Plant Biol. 3, 517–522. doi: 10.1016/S1369-5266(00)00122-9
165. Rodríguez-Serrano, M., Romero-Puertas, M. C., Sanz-Fernández, M., Hu, J., and Sandalio, L. M. (2016). Peroxisomes extend peroxules in a fast response to stress via a reactive oxygen species-mediated induction of the peroxin PEX11a. Plant Physiol. 171, 1665–1674. doi: 10.1104/pp.16.00648
166. Ros Barceló, A. (2005). Xylem parenchyma cells deliver the H2O2 necessary for lignification in differentiating xylem vessels. Planta 220, 747–756. doi: 10.1007/s00425-004-1394-3
167. Rubio-Diaz, S., Perez-Perez, J. M., Gonzalez-Bayon, R., Munoz-Viana, R., Borrega, N., Mouille, G., et al. (2012). Cell expansion-mediated organ growth is affected by mutations in three EXIGUA genes. PLoS ONE 7:e36500. doi: 10.1371/journal.pone.0036500
168. Sagi, M., and Fluhr, R. (2006). Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol. 141, 336–340. doi: 10.1104/pp.106.078089
169. Sakamoto, M., Munemura, I., Tomita, R., and Kobayashi, K. (2008). Reactive oxygen species in leaf abscission signaling. Plant Signal. Behav. 3, 1014–1015. doi: 10.4161/psb.6737
170. Sandalio, L. M., Rodríguez-Serrano, M., Romero-Puertas, M. C., and del Rio, L. A. (2013). Role of peroxisomes as a source of reactive oxygen species (ROS) signalling molecules. Subcell. Biochem. 69, 231–255. doi: 10.1007/978-94-007-6889-5_13
171. Schopfer, P. (1996). Hydrogen peroxide-mediated cell-wall stiffening in vitro in maize coleoptiles. Planta 199, 43–49. doi: 10.1007/BF00196879
172. Schopfer, P., Liszkay, A., Bechtold, M., Frahry, G., and Wagner, A. (2002). Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 214, 821–828. doi: 10.1007/s00425-001-0699-8
173. Schopfer, P., Plachy, C., and Frahry, G. (2001). Production of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin, and abscisic acid. Plant Physiol. 125, 1591–1602. doi: 10.1104/pp.125.4.1591
174. Schweikert, C., Liszkay, A., and Schopfer, P. (2000). Scission of polysaccharides by peroxidase-generated hydroxyl radicals.Phytochemistry 53, 562–570. doi: 10.1016/S0031-9422(99)00586-5
175. Serrano, I., María, C., Romero-Puertas, Sandalio, L. M., and Olmedilla, A. (2015). The role of reactive oxygen species and nitric oxide in programmed cell death associated with self-incompatibility. J. Exp. Bot. 66, 2869–2876. doi: 10.1093/jxb/erv083
176. Serrano, I., and Olmedilla, A. (2012). Histochemical location of key enzyme activities involved in receptivity and self-incompatibility in the olive tree (Olea europaea L.). Plant Sci. 197, 40–49. doi: 10.1016/j.plantsci.2012.07.007
177. 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
178. Sharma, P., Jha, A. B., Dubey, R. S., and Pessarakli, M. (2012). Reactive oxygen species, oxidative damage and anti-oxidative defense mechanism in plants under stressful conditions. J. Bot. 2012, 1–26. doi: 10.1155/2012/217037
179. Singh, S., Ambasth, V., Levine, A., Sopory, S. K., Yadava, P. K., Tripathy, B. C., et al. (2015). Anhydrobiosis and programmed cell death in plants: Commonalities and Differences. Curr. Plant Biol. 2, 12–20. doi: 10.1016/j.cpb.2014.12.001
180. Singh, V. P., Singh, S., Kumar, J., and Prasad, S. M. (2015a). Hydrogen sulfide alleviates toxic effects of arsenate in pea seedlings through up-regulation of the ascorbate-glutathione cycle: possible involvement of nitric oxide. J. Plant Physiol. 181, 20–29. doi: 10.1016/j.jplph.2015.03.015
181. Singh, V. P., Singh, S., Kumar, J., and Prasad, S. M. (2015b). Investigating the roles of ascorbate-glutathione cycle and thiol metabolism in arsenate tolerance in ridged Luffa seedlings. Protoplasma 252, 1217–1229. doi: 10.1007/s00709-014-0753-6
182. Singh, V. P., Srivastava, P. K., and Prasad, S. M. (2012a). Differential effect of UV-B radiation on growth, oxidative stress and ascorbate-glutathione cycle in two cyanobacteria under copper toxicity. Plant Physiol. Biochem. 61, 61–70. doi: 10.1016/j.plaphy.2012.09.005
183. Singh, V. P., Srivastava, P. K., and Prasad, S. M. (2012b). UV-B induced differential effect on growth and nitrogen metabolism in two cyanobacteria under copper toxicity. Cell Mol. Biol. 58, 81–91.
184. Spartz, A. K., Ren, H., Park, M. Y., Grandt, K. N., Lee, S. H., Murphy, A. S., et al. (2014). SAUR inhibition of PP2C-D phosphatases activates plasma membrane H+-ATPases to promote cell expansion in Arabidopsis. Plant Cell 26, 2129–2142. doi: 10.1105/tpc.114.126037
185. Springer, A., Acker, G., Bartsch, S., Bauerschmitt, H., Reinbothe, S., and Reinbothe, C. (2015). Differences in gene expression between natural and artificially induced leaf senescence in barley. J. Plant Pysiol. 176, 180–191. doi: 10.1016/j.jplph.2015.01.004
186. Steffens, B. (2014). The role of ethylene and ROS in salinity, heavy metal, and flooding responses in rice. Front. Plant Sci. 5:685. doi: 10.3389/fpls.2014.00685
187. 2. New Phytol. 190, 369–378. doi: 10.1111/j.1469-8137.2010.03496.x
188. 2 through an autoamplified signal pathway. Plant Cell 21, 184–196. doi: 10.1105/tpc.108.061887
189. Steinhorst, L., and Kudla, J. (2013). Calcium—A central regulator of pollen germination and tube growth. Biochim. Biophys. Acta 1833, 1573–1581. doi: 10.1016/j.bbamcr.2012.10.009
190. Stern, R., Kogan, G., Jedrzejas, M. J., and Soltés, L. (2007). The many ways to cleave hyaluronan. Biotechnol. Adv. 25, 537–557. doi: 10.1016/j.biotechadv.2007.07.001
191. Sundaravelpandian, K., Chandrika, N. N., and Schmidt, W. (2013). PFT1, a transcriptional Mediator complex subunit, controls root hair differentiation through reactive oxygen species (ROS) distribution in Arabidopsis. New Phytol. 197, 151–161. doi: 10.1111/nph.12000
192. Suzuki, N., Koussevitzky, S., Mittler, R., and Miller, G. (2012). ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ. 35, 259–270. doi: 10.1111/j.1365-3040.2011.02336.x
193. Suzuki, N., Miller, G., Salazar, C., Mondal, H. A., Shulaev, E., Cortes, D. F., et al. (2013). Temporal-spatial interaction between reactive oxygen species and abscisic acid regulates rapid systemic acclimation in plants. Plant Cell 25, 3553–3569. doi: 10.1105/tpc.113.114595
194. Swanson, S., and Gilroy, S. (2010). ROS in plant development. Physiol. Plant 138, 384–392. doi: 10.1111/j.1399-3054.2009.01313.x
195. Takagi, D., Takumi, S., Hashiguchi, M., Sejima, T., and Miyake, C. (2016). Superoxide and singlet oxygen produced within the thylakoid membranes both cause photosystem I photoinhibition. Plant Physiol. 171, 1626–1634. doi: 10.1104/pp.16.00246
196. Tanioka, S., Matsui, Y., Irie, T., Tanigawa, T., Tanaka, Y., Shibata, H., et al. (1996). Oxidative depolymerization of chitosan by hydroxyl radical. Biosci. Biotechnol. Biochem. 60, 2001–2004. doi: 10.1371/journal.pone.0100743
197. Thomas, H. (2013). Senescence, ageing and death of the whole plant. New Phytol. 197, 696–711. doi: 10.1111/nph.12047
198. Townsley, B. T., and Sinha, N. R. (2012). A new development: evolving concepts in leaf ontogeny. Annu. Rev. Plant Biol. 63, 535–562. doi: 10.1146/annurev-arplant-042811-105524
199. Tripathi, S. K., and Tuteja, N. (2007). Integrated signaling in flower senescence. Plant Signal. Behav. 2, 437–445. doi: 10.4161/psb.2.6.4991
200. Tsukagoshi, H., Busch, W., and Benfey, P. N. (2010). Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143, 606–616. doi: 10.1016/j.cell.2010.10.020
201. van Doorn, W. G., Beers, E. P., Dangl, J. L., Franklin-Tong, V. E., Gallois, P., Hara- Nishimura, I., et al. (2011). Morphological classification of plant cell deaths. Cell Death Differ. 18, 1241–1246. doi: 10.1038/cdd.2011.36
202. Vanacker, H., Sandalio, L. M., Jimenez, A., Palma, J. M., Corpas, F. J., Meseguer, V., et al. (2006). Role of redox regulation in leaf senescence of pea plants grown in different sources of nitrogen nutrition. J. Exp. Bot. 57, 1735–1745. doi: 10.1093/jxb/erl012
203. Vertucci, C. W., and Farrant, J. M. (1995). “Acquisition and loss of desiccation tolerance,” in Seed Development and Germination, eds J. Kigel and G. Galili (New York, NY: Marcel Dekker), 237–271.
204. Vogel, M. O., Moore, M., König, K., Pecher, P., Alsharafa, K., Lee, J., et al. (2014). Fast retrograde signaling in response to high light involves metabolite export, MITOGEN-ACTIVATED PROTEIN KINASE6, and AP2/ERF transcription factors in Arabidopsis. Plant Cell26, 1151–1165. doi: 10.1105/tpc.113.121061
205. Wang, C. L., and Zhang, S. L. (2011). A cascade signal pathway occurs in self-incompatibility of Pyrus pyrifolia. Plant Signal. Behav. 6, 420–421. doi: 10.4161/psb.6.3.14386
206. Wang, Y., Loake, G. J., and Chu, C. (2013). Cross talk of nitric oxide and reactive oxygen species in plant programmed cell death. Front. Plant Sci. 4:314. doi: 10.3389/fpls.2013.00314
207. Wells, D. M., Wilson, M. H., and Bennett, M. J. (2010). Feeling UPBEAT about growth: linking ROS gradients and cell proliferation. Dev. Cell 19, 644–646. doi: 10.1016/j.devcel.2010.10.017
208. Wilkins, K. A., Bancroft, J., Bosch, M., Ings, J., Smirnoff, N., and Franklin-Tong, V. E. (2011). Reactive oxygen species and nitric oxide mediate actin reorganization and programmed cell death in the selfincompatibility response of Papaver. Plant Physiol. 156, 404–416. doi: 10.1104/pp.110.167510
209. Wilkins, K. A., Bosch, M., Haque, T., Teng, N., Poulter, N. S., and Franklin- Tong, V. E. (2015). Self-incompatibility-induced programmed cell death in field poppy pollen involves dramatic acidification of the incompatible pollen tube cytosol. Plant Physiol. 167, 766–779. doi: 10.1104/pp.114.252742
210. Willems, P., Mhamdi, A., Stael, S., Storme, V., Kerchev, P., Noctor, G., et al. (2016). The ROS wheel: refining ROS transcriptional footprints in Arabidopsis. Plant Physiol. 171, 1720–1733. doi: 10.1104/pp.16.00420
211. Wolf, S., and Höfte, H. (2014). Growth control: a saga of cell walls, ROS, and peptide receptors. Plant Cell 26, 1848–1856.
212. Wong, H. L., Sakamoto, T., Kawasaki, T., Umemura, K., and Shimamoto, K. (2004). Down-regulation of metallothionein, a reactive oxygen scavenger, by the small GTPase OsRac1 in rice. Plant Physiol. 135, 1447–1456. doi: 10.1104/pp.103.036384
213. Wrzaczek, M., Brosche, M., and Kangasjarvi, J. (2013). ROS signaling loops: production, perception, regulation. Curr. Opin. Plant Biol.16, 575–582. doi: 10.1016/j.pbi.2013.07.002
214. Wu, G., Shortt, B. J., Lawrence, E. B., Leon, J., Fitzsimmons, K. C., Levine, E. B., et al. (1997). Activation of host defense mechanisms by elevated production of H2O2 in transgenic plants. Plant Physiol. 115, 427–435.
215. 2+-permeable channels and pollen tube growth. Plant J. 63, 1042–1053. doi: 10.1111/j.1365-313X.2010.04301.x
216. Xie, H. T., Wan, Z. Y., Li, S., and Zhang, Y. (2014). Spatiotemporal production of reactive oxygen species by NADPH oxidase is critical for tapetal programmed cell death and pollen development in Arabidopsis. Plant Cell 26, 2007–2023. doi: 10.1105/tpc.114.125427
217. Xu, J., Yin, H., Li, Y., and Liu, X. (2010). Nitric oxide is associated with longterm zinc tolerance in Solanum nigrum. Plant Physiol. 154, 1319–1334. doi: 10.1104/pp.110.162982
218. Xu, R., and Li, Y. (2011). Control of final organ size by mediator complex subunit 25 in Arabidopsis thaliana. Development 138, 4545–4554. doi: 10.1242/dev.071423
219. Yadegari, R., and Drews, G. N. (2004). Female gametophyte development. Plant Cell 16, S133–S141. doi: 10.1105/tpc.018192
220. Ye, N., Zhu, G., Liu, Y., Zhang, A., Li, Y., Liu, R., et al. (2012). Ascorbic acid and reactive oxygen species are involved in the inhibition of seed germination by abscisic acid in rice seeds. J. Exp. Bot. 63, 1809–1822. doi: 10.1093/jxb/err336
221. Zafra, A., Rodríguez-García, M. I., and Alché, J. D. (2010). Cellular localization of ROS and NO in olive reproductive tissues during flower development. BMC Plant Biol. 10:36. doi: 10.1186/1471-2229-10-36
222. Zhang, L., Ren, F., Zhang, Q., Chen, Y., Wang, B., and Jiang, J. (2008). The TEAD/TEF family of transcription factor Scalloped mediates Hippo signaling in organ size control. Dev. Cell 14, 377–387. doi: 10.1016/j.devcel.2008.01.006
223. Zhu, Y., Yan, J., Liu, W., Liu, L., Sheng, Y., Sun, Y., et al. (2016). Phosphorylation of a NAC transcription factor by ZmCCaMK regulates abscisic acid-induced antioxidant defense in maize. Plant Physiol. 171, 1651–1664. doi: 10.1104/pp.16.00168