Nitric oxide function during oxygen deprivation in physiological and stress processes

  1. Sánchez-Vicente, Inmaculada 1
  2. Lorenzo, Oscar 1
  3. Manrique-Gil, Isabel 1
  4. Torres-Quezada, Isabel 1
  1. 1 Departamento de Botánica y Fisiología Vegetal, Instituto Hispano-Luso de Investigaciones Agrarias (CIALE), Facultad de Biología, Universidad de Salamanca. C/ Río Duero 12, Salamanca, Spain
Revista:
Journal of Experimental Botany

ISSN: 0022-0957,  1460-2431

Año de publicación: 2020

Volumen: 72

Número: 3

Páginas: 904-916

Tipo: Artículo

DOI: 10.1093/JXB/ERAA442 GOOGLE SCHOLAR

Otras publicaciones en: Journal of Experimental Botany

Resumen

Abstract Plants are aerobic organisms that have evolved to maintain specific requirements for oxygen (O2), leading to a correct respiratory energy supply during growth and development. There are certain plant developmental cues and biotic or abiotic stress responses where O2 is scarce. This O2 deprivation known as hypoxia may occur in hypoxic niches of plant-specific tissues and during adverse environmental cues such as pathogen attack and flooding. In general, plants respond to hypoxia through a complex reprogramming of their molecular activities with the aim of reducing the impact of stress on their physiological and cellular homeostasis. This review focuses on the fine-tuned regulation of hypoxia triggered by a network of gaseous compounds that includes O2, ethylene, and nitric oxide. In view of recent scientific advances, we summarize the molecular mechanisms mediated by phytoglobins and by the N-degron proteolytic pathway, focusing on embryogenesis, seed imbibition, and germination, and also specific structures, most notably root apical and shoot apical meristems. In addition, those biotic and abiotic stresses that comprise hypoxia are also highlighted.

Referencias bibliográficas

  • Abbas, (2015), Current Biology, 25, pp. 1483, 10.1016/j.cub.2015.03.060
  • Albertos, (2015), Nature Communications, 6, pp. 8669, 10.1038/ncomms9669
  • Appleby, (1983), Science, 220, pp. 951, 10.1126/science.220.4600.951
  • Armstrong, (2019), Journal of Plant Physiology, 239, pp. 92, 10.1016/j.jplph.2019.04.010
  • Arredondo-Peter, (1998), Plant Physiology, 118, pp. 1121, 10.1104/pp.118.4.1121
  • Bachmair, (1986), Science, 234, pp. 179, 10.1126/science.3018930
  • Badri, (2009), Plant, Cell & Environment, 32, pp. 666, 10.1111/j.1365-3040.2009.01926.x
  • Begara-Morales, (2014), Journal of Experimental Botany, 65, pp. 527, 10.1093/jxb/ert396
  • Benech-Arnold, (2006), Journal of Experimental Botany, 57, pp. 1423, 10.1093/jxb/erj122
  • Borisjuk, (2007), New Phytologist, 176, pp. 813, 10.1111/j.1469-8137.2007.02226.x
  • Cantrel, (2011), New Phytologist, 189, pp. 415, 10.1111/j.1469-8137.2010.03500.x
  • Chen, (2015), Autophagy, 11, pp. 2233, 10.1080/15548627.2015.1112483
  • Conrath, (2006), Plant Signaling & Behavior, 1, pp. 179, 10.4161/psb.1.4.3221
  • Correa-Aragunde, (2004), Planta, 218, pp. 900, 10.1007/s00425-003-1172-7
  • Correa-Aragunde, (2006), Nitric oxide in plant growth, development and stress, pp. 581, 10.1007/7089_2006_087
  • Darwent, (2003), Russian Journal of Plant Physiology, pp. 722, 10.1023/B:RUPP.0000003269.31706.ed
  • Davison, (1993), Phytopathology, 84, pp. 335, 10.1094/Phyto-84-335
  • Delledonne, (1998), Nature, 394, pp. 585, 10.1038/29087
  • de Marchi, (2016), Scientific Reports, 6, pp. 26020, 10.1038/srep26020
  • Dordas, (2003), The Plant Journal, 35, pp. 763, 10.1046/j.1365-313X.2003.01846.x
  • Dordas, (2004), Planta, 219, pp. 66, 10.1007/s00425-004-1212-y
  • Durner, (1998), Proceedings of the National Academy of Sciences, USA, 95, pp. 10328, 10.1073/pnas.95.17.10328
  • Elhiti, (2018), Frontiers in Plant Science, 9, pp. 1477, 10.3389/fpls.2018.01477
  • Elhiti, (2013), In Vitro Cellular & Developmental Biology – Plant, 49, pp. 631, 10.1007/s11627-013-9547-3
  • Ellis, (1999), Plant Physiology, 119, pp. 57, 10.1104/pp.119.1.57
  • Fehér, (2014), Biochimica et Biophysica Acta, 1849, pp. 385, 10.1016/j.bbagrm.2014.07.005
  • Fehér, (2003), Plant Cell, Tissue and Organ Culture, 74, pp. 201, 10.1023/A:1024033216561
  • Fernández-Marcos, (2011), Proceedings of the National Academy of Sciences, USA, 108, pp. 18506, 10.1073/pnas.1108644108
  • Finkelstein, (2000), The Plant Cell, 12, pp. 599, 10.1105/tpc.12.4.599
  • Garrocho-Villegas, (2008), Molecular Biology and Evolution, 25, pp. 1482, 10.1093/molbev/msn096
  • Gendall, (2001), Cell, 107, pp. 525, 10.1016/S0092-8674(01)00573-6
  • Gibbs, (2011), Nature, 479, pp. 415, 10.1038/nature10534
  • Gibbs, (2014), Molecular Cell, 53, pp. 369, 10.1016/j.molcel.2013.12.020
  • Gibbs, (2018), Nature Communications, 9, pp. 5438, 10.1038/s41467-018-07875-7
  • Gibbs, (1998), Australian Journal of Plant Physiology, 25, pp. 745
  • Godee, (2017), Journal of Experimental Botany, 68, pp. 1013, 10.1093/jxb/erx003
  • Gopalasubramaniam, (2008), Proteins, 72, pp. 252, 10.1002/prot.21917
  • Govrin, (2000), Current Biology, 10, pp. 751, 10.1016/S0960-9822(00)00560-1
  • Graciet, (2010), The Plant Journal, 61, pp. 741, 10.1111/j.1365-313X.2009.04099.x
  • Graciet, (2009), Proceedings of the National Academy of Sciences, USA, 106, pp. 13618, 10.1073/pnas.0906404106
  • Gravot, (2016), BMC Plant Biology, 16, pp. 251, 10.1186/s12870-016-0941-y
  • Gupta, (2011), FEBS Letters, 585, pp. 3843, 10.1016/j.febslet.2011.10.036
  • Gupta, (2016), Frontiers in Plant Science, 7, pp. 369, 10.3389/fpls.2016.00369
  • Gupta, (2012), Journal of Experimental Botany, 63, pp. 1773, 10.1093/jxb/ers053
  • Gupta, (2005), Journal of Experimental Botany, 56, pp. 2601, 10.1093/jxb/eri252
  • Halim, (2006), Plant Biology, 8, pp. 307, 10.1055/s-2006-924025
  • Hargrove, (1997), Journal of Molecular Biology, 266, pp. 1032, 10.1006/jmbi.1996.0833
  • Hartman, (2019), Nature Communications, 10, pp. 1, 10.1038/s41467-019-12045-4
  • Hebelstrup, (2006), Physiologia Plantarum, 127, pp. 157, 10.1111/j.1399-3054.2006.00653.x
  • Hebelstrup, (2007), Gene, 398, pp. 86, 10.1016/j.gene.2007.01.039
  • Hebelstrup, (2008), Planta, 227, pp. 917, 10.1007/s00425-007-0667-z
  • Hebelstrup, (2012), Journal of Experimental Botany, 63, pp. 5581, 10.1093/jxb/ers210
  • Heckmann, (2006), Plant Molecular Biology, 61, pp. 769, 10.1007/s11103-006-0048-1
  • Hill, (2016), F1000Research, 5, pp. 212, 10.12688/f1000research.8133.1
  • Holman, (2009), Proceedings of the National Academy of Sciences, USA, 106, pp. 4549, 10.1073/pnas.0810280106
  • Hoy, (2008), Plant Physiology and Biochemistry, 46, pp. 371, 10.1016/j.plaphy.2007.12.016
  • Hsu, (2011), PLoS One, 6, pp. e28888, 10.1371/journal.pone.0028888
  • Hu, (2005), Nature, 437, pp. 981, 10.1038/nature04027
  • Hunt, (2002), Proceedings of the National Academy of Sciences, USA, 99, pp. 17197, 10.1073/pnas.212648799
  • Hunt, (2001), Plant Molecular Biology, 47, pp. 677, 10.1023/A:1012440926982
  • Igamberdiev, (2005), Annals of Botany, 96, pp. 557, 10.1093/aob/mci210
  • Jacobsen-Lyon, (1995), The Plant Cell, 7, pp. 213
  • Jiménez, (2001), Revista Brasileira de Fisiologia Vegetal, 13, pp. 196, 10.1590/S0103-31312001000200008
  • Kim, (2018), Frontiers in Plant Science, 9, pp. 1675, 10.3389/fpls.2018.01675
  • Kozlowski, (1997), Tree Physiology, 17, pp. 490, 10.1093/treephys/17.7.490
  • Labandera, (2020), New Phytologist
  • Li, (2016), Frontiers in Plant Science, 6, pp. 1, 10.3389/fpls.2015.01203
  • Licausi, (2011), Nature, 479, pp. 419, 10.1038/nature10536
  • Lira-Ruan, (2002), Plant Physiology and Biochemistry, 40, pp. 199, 10.1016/S0981-9428(02)01365-7
  • Liu, (2001), Nature, 410, pp. 490, 10.1038/35068596
  • Liu, (2017), New Phytologist, 213, pp. 1242, 10.1111/nph.14259
  • Liu, (2015), Plant Physiology, 168, pp. 343, 10.1104/pp.15.00030
  • Lopez-Molina, (2001), Proceedings of the National Academy of Sciences, USA, 98, pp. 4782, 10.1073/pnas.081594298
  • Lozano-Juste, (2011), Journal of Experimental Botany, 62, pp. 3501, 10.1093/jxb/err042
  • Ma, (2016), Frontiers in Plant Science, 7, pp. 138, 10.3389/fpls.2016.00138
  • Magalhaes, (2000), Physiology and Molecular Biology of Plants, 6, pp. 117
  • Masson, (2019), Science, 365, pp. 65, 10.1126/science.aaw0112
  • Millar, (1996), FEBS Letters, 398, pp. 155, 10.1016/S0014-5793(96)01230-6
  • Mira, (2016), Journal of Experimental Botany, 67, pp. 5901, 10.1093/jxb/erw259
  • Mira, (2016), Plant Physiology, 172, pp. 2044, 10.1104/pp.16.01150
  • Mira, (2017), Journal of Experimental Botany, 68, pp. 5653, 10.1093/jxb/erx371
  • Mugnai, (2012), Plant & Cell Physiology, 53, pp. 912, 10.1093/pcp/pcs034
  • Mukhi, (2017), Nitric Oxide, 68, pp. 150, 10.1016/j.niox.2017.03.004
  • Mur, (2013), Frontiers in Plant Science, 4, pp. 215, 10.3389/fpls.2013.00215
  • Mur, (2012), Journal of Experimental Botany, 63, pp. 4375, 10.1093/jxb/ers116
  • Ott, (2005), Current Biology, 15, pp. 531, 10.1016/j.cub.2005.01.042
  • Ötvös, (2005), The Plant Journal, 43, pp. 849, 10.1111/j.1365-313X.2005.02494.x
  • Pasternak, (2002), Plant Physiology, 129, pp. 1807, 10.1104/pp.000810
  • Perazzolli, (2004), The Plant Cell, 16, pp. 2785, 10.1105/tpc.104.025379
  • Planchet, (2005), The Plant Journal, 41, pp. 732, 10.1111/j.1365-313X.2005.02335.x
  • Pré, (2008), Plant Physiology, 147, pp. 1347, 10.1104/pp.108.117523
  • Rolletschek, (2003), Plant Physiology, 132, pp. 1196, 10.1104/pp.102.017376
  • Rubio, (2019), The Plant Journal, 100, pp. 38, 10.1111/tpj.14422
  • Sainz, (2015), The Plant Journal, 81, pp. 723, 10.1111/tpj.12762
  • Sánchez-Vicente, (2019), Molecular Plant, 12, pp. 1425, 10.1016/j.molp.2019.09.005
  • Sánchez-Vicente, (2019), Journal of Experimental Botany, 70, pp. 4441, 10.1093/jxb/erz339
  • Sanz, (2015), Journal of Experimental Botany, 66, pp. 2857, 10.1093/jxb/erv213
  • Sanz, (2014), Plant Physiology, 166, pp. 1972, 10.1104/pp.114.247445
  • Sasidharan, (2018), Plant Physiology, 176, pp. 1106, 10.1104/pp.17.01232
  • Scheler, (2013), Current Opinion in Plant Biology, 16, pp. 534, 10.1016/j.pbi.2013.06.020
  • Shukla, (2019), Molecular Plant, 12, pp. 538, 10.1016/j.molp.2019.01.007
  • Simontacchi, (2004), Plant Science, 167, pp. 839, 10.1016/j.plantsci.2004.05.028
  • Singh, (2018), Plant Signaling & Behavior, 13, pp. e1473683, 10.1080/15592324.2018.1473683
  • Spyrakis, (2011), IUBMB Life, 63, pp. 355, 10.1002/iub.470
  • Suprasanna, (2005), Plant Cell Monographs, 2, pp. 305, 10.1007/7089_038
  • Taiz, (2014), Plant physiology
  • Taylor, (1994), Plant Molecular Biology, 24, pp. 853, 10.1007/BF00014440
  • Thaler, (2004), Plant Physiology, 135, pp. 530, 10.1104/pp.104.041566
  • Thiel, (2011), BMC Plant Biology, 11, pp. 48, 10.1186/1471-2229-11-48
  • Thorpe, (2001), Current trends in the embryology of angiosperms, pp. 279, 10.1007/978-94-017-1203-3_12
  • Till, (2019), Plant Direct, 3, pp. e00194, 10.1002/pld3.194
  • Tiso, (2012), Biochemistry, 51, pp. 5285, 10.1021/bi300570v
  • Torres, (2006), Plant Physiology, 141, pp. 373, 10.1104/pp.106.079467
  • Trevaskis, (1997), Proceedings of the National Academy of Sciences, USA, 94, pp. 12230, 10.1073/pnas.94.22.12230
  • Turrión Gómez, (2011), Molecular Plant Pathology, 12, pp. 606, 10.1111/j.1364-3703.2010.00695.x
  • Turrión Gómez, (2010), Fungal Genetics and Biology, 47, pp. 484, 10.1016/j.fgb.2010.03.001
  • Valeri, (2020), New Phytologist
  • Vandelle, (2016), Advances in Botanical Research, 77, pp. 219, 10.1016/bs.abr.2015.10.013
  • Varshavsky, (2011), Protein Science, 20, pp. 1298, 10.1002/pro.666
  • Vicente, (2017), Current Biology, 27, pp. 3183, 10.1016/j.cub.2017.09.006
  • Vicente, (2019), New Phytologist, 221, pp. 988, 10.1111/nph.15387
  • Vigeolas, (2011), Plant Physiology, 155, pp. 1435, 10.1104/pp.110.166462
  • Wang, (2005), Fungal Genetics and Biology, 42, pp. 284, 10.1016/j.fgb.2004.12.006
  • Wang, (2015), Plant Signaling & Behavior, 10, pp. e1031939, 10.1080/15592324.2015.1031939
  • Wang, (2000), The Plant Cell, 12, pp. 1491, 10.1105/tpc.12.8.1491
  • Watts, (2001), Proceedings of the National Academy of Sciences, USA, 98, pp. 10119, 10.1073/pnas.191349198
  • Weits, (2014), Nature Communications, 5, pp. 3425, 10.1038/ncomms4425
  • Weits, (2019), Nature, 569, pp. 714, 10.1038/s41586-019-1203-6
  • Weits, (2020), New Phytologist
  • White, (2018), Journal of Biological Chemistry, 293, pp. 11786, 10.1074/jbc.RA118.003496
  • Wildermuth, (2001), Nature, 414, pp. 562, 10.1038/35107108
  • Wittenberg, (1975), Annals of the New York Academy of Sciences, 244, pp. 28, 10.1111/j.1749-6632.1975.tb41519.x
  • Wojtaszek, (1997), The Biochemical Journal, 322, pp. 681, 10.1042/bj3220681
  • Yoshida, (2002), The Plant Journal, 32, pp. 129, 10.1046/j.1365-313X.2002.01407.x
  • Zarban, (2019), Molecules, 24, pp. 2691, 10.3390/molecules24152691
  • Zavattieri, (2010), Electronic Journal of Biotechnology, 13, 10.2225/vol13-issue1-fulltext-4
  • Zhan, (2018), Molecular Cell, 71, pp. 142, 10.1016/j.molcel.2018.05.024
  • Zhang, (2018), New Phytologist, 218, pp. 1106, 10.1111/nph.14909
  • Zhang, (2018), Scientific Reports, 8, pp. 15192, 10.1038/s41598-018-33630-5
  • Zhao, (2012), New Phytologist, 195, pp. 450, 10.1111/j.1469-8137.2012.04160.x