Nitric Oxide(II) in Biology of Chlorophyta

封面

如何引用文章

全文:

开放存取 开放存取
受限制的访问 ##reader.subscriptionAccessGranted##
受限制的访问 订阅存取

详细

NO is a gaseous signaling redox-active molecule that functions in various eukaryotes. However, its synthesis, turnover, and effects in cells are specific in plants in several aspects. Compared with higher plants, the role of NO in Chlorophyta has not been investigated enough. Yet, some of the mechanisms for controlling levels of this signaling molecule have been characterized in model green algae. In Chlamydomonas reinhardtii, NO synthesis is carried out by a dual system comprising nitrate reductase and NO-forming nitrite reductase. Other mechanisms that might produce NO from nitrite are associated with components of mitochondrial electron-transport chain. In addition, NO formation in some green algae proceeds by oxidative mechanism similar to that in mammals. Recent discovery of L-arginine-dependent NO synthesis in colorless alga Polytomella parva suggests the existence of a protein complex with enzyme activity that are similar to animal nitric oxide synthase. This latter finding paves the way for further research into potential members of the NO synthases family in Chlorophyta. Beyond synthesis, the regulatory processes to maintain intracellular NO levels are also an integral part for its function in cells. Members of the truncated hemoglobins family with dioxygenase activity can convert NO to nitrate, as was shown for C. reinhardtii. In addition, the implication of NO reductases in NO scavenging has also been described. Even more intriguing, unlike in animals, the typical NO/cGMP signaling module appears not to be used by green algae. S-nitrosylated glutathione, which is considered the main reservoir for NO, provides NO signals to proteins. In Chlorophyta, protein S-nitrosation is one of the key mechanisms of action of the redox molecule. In this review, we discuss the current state-of-the-art and possible future directions related to the biology of NO in green algae.

作者简介

E. Ermilova

Saint-Petersburg State University

编辑信件的主要联系方式.
Email: e.ermilova@spbu.ru
Russia, 199034, Saint-Petersburg

参考

  1. Wendehenne D., Durner J., Klessig D.F. (2004) Nitric oxide: a new player in plant signalling and defence responses. Curr. Opin. Plant Biol. 7(4), 449–455.
  2. Wendehenne D., Pugin A., Klessig D.F., Durner J. (2001) Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends Plant Sci. 6(4), 177–183.
  3. Bredt D.S., Snyder S.H. (1992) Nitric oxide, a novel neuronal messenger. Neuron. 8(1), 3–11.
  4. Ignarro L.J., Buga G.M., Wood K.S., Byrns R.E., Chaudhuri G. (1987) Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. USA. 84(24), 9265–9269.
  5. Palmer R.M., Ferrige A.G., Moncada S. (1987) Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 327(6122), 524–526.
  6. Cox M.A., Bassi C., Saunders M.E., Nechanitzky R., Morgado-Palacin I., Zheng C., Mak T.W. (2020) Beyond neurotransmission: acetylcholine in immunity and inflammation. J. Intern. Med. 287(2), 120–133.
  7. Astier J., Gross I., Durner J. (2018) Nitric oxide production in plants: an update. J. Exp. Bot. 69(14), 3401–3411.
  8. Kolbert Z.S., Barroso J.B., Brouquisse R., Corpas F.J., Gupta K.J., Lindermayr C., Loake G.J., Palma J.M., Petřivalský M., Wendehenne D., Hancock J.T. (2019) A forty year journey: the generation and roles of NO in plants. Nitric Oxide. 93, 53–70.
  9. Yu M., Lamattina L., Spoel S.H., Loake G.J. (2014) Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytol. 202(4), 1142–1156.
  10. He Y., Tang R.H., Hao Y., Stevens R.D., Cook C.W., Ahn S.M., Jing L., Yang Z., Chen L., Guo F., Fiorani F., Jackson R.B., Crawford N.M., Pei Z.M. (2004) Nitric oxide represses the Arabidopsis floral transition. Science. 305(5692), 1968–1971.
  11. Bethke P.C., Libourel I.G., Jones R.L. (2006) Nitric oxide reduces seed dormancy in Arabidopsis. J. Exp. Bot. 57(3), 517–526.
  12. Sun C., Lu L., Liu L., Liu W., Yu Y., Liu X., Hu Y., Jin C., Lin X. (2014) Nitrate reductase-mediated early nitric oxide burst alleviates oxidative damage induced by aluminum through enhancement of antioxidant defenses in roots of wheat (Triticum aestivum). New Phytol. 201(4), 1240–1250.
  13. Neill S., Barros R., Bright J., Desikan R., Hancock J., Harrison J., Morris P., Ribeiro D., Wilson I. (2008) Nitric oxide, stomatal closure, and abiotic stress. J. Exp. Bot. 59(2), 165–176.
  14. Qiao W., Fan L.M. (2008) Nitric oxide signaling in plant responses to abiotic stresses. J. Integr. Plant Biol. 50(10), 1238–1246.
  15. Fancy N.N., Bahlmann A.K., Loake G.J. (2017) Nitric oxide function in plant abiotic stress. Plant Cell Environ. 40(4), 462–472.
  16. González-Gordo S., Bautista R., Claros M.G., Cañas A., Palma J.M., Corpas F.J. (2019) Nitric oxide-dependent regulation of sweet pepper fruit ripening. J. Exp. Bot. 70(17), 4557–4570.
  17. Berger A., Boscari A., Frendo P., Brouquisse R. (2019) Nitric oxide signaling, metabolism and toxicity in nitrogen-fixing symbiosis. J. Exp. Bot. 70(17), 4505–4520.
  18. Gupta K.J., Fernie A.R., Kaiser W.M., van Dongen J.T. (2011) On the origins of nitric oxide. Trends Plant Sci. 16(3), 160–168.
  19. Astier J., Lindermayr C. (2012) Nitric oxide-dependent posttranslational modification in plants: an update. Int. J. Mol. Sci. 13(11), 15193–15208.
  20. Corpas F.J., Chaki M., Leterrier M., Barroso J.B. (2009) Protein tyrosine nitration: a new challenge in plants. Plant Signal. Behav. 4(10), 920–923.
  21. Corpas F.J., Palma J.M., Río L.A.D., Barroso J.B. (2009) Evidence supporting the existence of L-arginine-dependent nitric oxide synthase activity in plants. New Phytol. 184, 9–14.
  22. Foresi N., Correa-Aragunde N., Parisi G., Calo G., Salerno G., 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(11), 3816–3830.
  23. Lapina T., Statinov V., Puzanskiy R., Ermilova E. (2022) Arginine-dependent nitric oxide generation and S-nitrosation in the non-photosynthetic unicellular alga Polytomella parva. Antioxidants. 11(5), 949.
  24. Astier J., Mounier A., Santolini J., Jeandroz S., Wendehenne D. (2019) The evolution of nitric oxide signalling diverges between animal and green lineages. J. Exp. Bot. 70(17), 4355–4364.
  25. Chamizo-Ampudia A., Sanz-Luque E., Llamas A., Galvan A., Fernandez E. (2017) Nitrate reductase regulates plant nitric oxide homeostasis. Trends Plant Sci. 22(2), 163–174.
  26. Mallick N., Rai L.C., Mohn F.H., Soeder C.J. (1999) Studies on nitric oxide (NO) formation by the green alga Scenedesmus obliquus and the diazotrophic cyanobacterium Anabaena doliolum. Chemosphere. 39(10), 1601–1610.
  27. Stuehr D.J., Santolini J., Wang Z.Q., Wei C.C., Adak S. (2004) Update on mechanism and catalytic regulation in the NO synthases. J. Biol. Chem. 279(35), 36167–36170.
  28. Daff S. (2010) NO synthase: structures and mechanisms. Nitric Oxide. 23(1), 1–11.
  29. Li H., Poulos T.L. (2005) Structure–function studies on nitric oxide synthases. J. Inorg. Biochem. 99(1), 293–305.
  30. Di Dato V., Musacchia F., Petrosino G., Patil S., Montresor M., Sanges R., Ferrante M.I. (2015) Transcriptome sequencing of three pseudo-nitzschia species reveals comparable gene sets and the presence of nitric oxide synthase genes in diatoms. Sci. Rep. 5(1), 12329.
  31. Kumar A., Castellano I., Patti F.P., Palumbo A., Buia M.C. (2015) Nitric oxide in marine photosynthetic organisms. Nitric Oxide. 47, 34–39.
  32. Weisslocker-Schaetzel M., André F., Touazi N., Foresi N., Lembrouk M., Dorlet P., Frelet-Barrand A., Lamattina L., Santolini J. (2017) The NOS-like protein from the microalgae Ostreococcus tauri is a genuine and ultrafast NO-producing enzyme. Plant Sci. 265, 100–111.
  33. Jeandroz S., Wipf D., Stuehr D.J., Lamattina L., Melkonian M., Tian Z., Zhu Y., Carpenter E.J., Wong G.K.S., Wendehenne D. (2016) Occurrence, structure, and evolution of nitric oxide synthase-like proteins in the plant kingdom. Sci. Signal. 9(417), re2.
  34. Santolini J., André F., Jeandroz S., Wendehenne D. (2017) Nitric oxide synthase in plants: where do we stand? Nitric Oxide. 63, 30–38.
  35. Foresi N., Mayta M.L., Lodeyro A.F., Scuffi D., Correa-Aragunde N., García-Mata C., Casalongué C., Carrillo N., Lamattina L. (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(5), 806–821.
  36. Chatelain P., Astier J., Wendehenne D., Rosnoblet C., Jeandroz S. (2021) Identification of partner proteins of the algae Klebsormidium nitens NO synthases: toward a better understanding of NO signaling in eukaryotic photosynthetic organisms. Front. Plant Sci. 12, 3068.
  37. Tun N.N., Santa-Catarina C., Begum T., Silveira V., Handro W., Floh E.I.S., Scherer G.F. (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol. 47(3), 346–354.
  38. Campbell M.G., Smith B.C., Potter C.S., Carragher B., Marletta M.A. (2014) Molecular architecture of mammalian nitric oxide synthases. Proc. Natl. Acad. Sci. USA. 111(35), E3614–E3623.
  39. Desikan R., Griffiths R., Hancock J., 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. USA. 99(25), 16314–16318.
  40. Yamasaki H., Sakihama Y., Takahashi S. (1999) An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends Plant Sci. 4(4), 128–129.
  41. Rockel P., Strube F., Rockel A., Wildt J., Kaiser W.M. (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J. Exp. Bot. 53(366), 103–110.
  42. Tejada-Jimenez M., Llamas A., Galván A., Fernández E. (2019) Role of nitrate reductase in NO production in photosynthetic eukaryotes. Plants. 8(3), 56.
  43. Tischner R., Planchet E., Kaiser W.M. (2004) Mitochondrial electron transport as a source for nitric oxide in the unicellular green alga Chlorella sorokiniana. FEBS Lett. 576(1–2), 151–155.
  44. Chamizo-Ampudia A., Sanz-Luque E., Llamas Á., Ocaña-Calahorro F., Mariscal V., Carreras A., Barroso J.B., Galván A., Fernández E. (2016) A dual system formed by the ARC and NR molybdoenzymes mediates nitrite-dependent NO production in Chlamydomonas. Plant Cell Environ. 39(10), 2097–2107.
  45. Minaeva E., Zalutskaya Z., Filina V., Ermilova E. (2017) Truncated hemoglobin 1 is a new player in Chlamydomonas reinhardtii acclimation to sulfur deprivation. PLoS One. 12(10), e0186851.
  46. Zalutskaya Z., Korkina S., Ermilova E. (2023) Second nitrate reductase of Dunaliella salina: functional redundancy or greatly? Protistology. 17(1), 16–29.
  47. Hemschemeier A., Düner M., Casero D., Merchant S.S., Winkler M., Happe T. (2013) Hypoxic survival requires a 2-on-2 hemoglobin in a process involving nitric oxide. Proc. Natl. Acad. Sci. USA. 110(26), 10854–10859.
  48. Gupta K.J., Igamberdiev A.U. (2011) The anoxic plant mitochondrion as a nitrite: NO reductase. Mitochondrion. 11(4), 537–543.
  49. Vishwakarma A., Kumari A., Mur L.A., Gupta K.J. (2018) A discrete role for alternative oxidase under hypoxia to increase nitric oxide and drive energy production. Free Radic. Biol. Med. 122, 40–51.
  50. Ostroukhova M., Ermilova E. (2019) New insights into NO generation and AOX1 upregulation in Chlamydomonas. Protistology. 13(1), 19–25.
  51. Sanz-Luque E., Chamizo-Ampudia A., Llamas A., Galvan A., Fernandez E. (2015) Understanding nitrate assimilation and its regulation in microalgae. Front. Plant Sci. 6, 899.
  52. Stewart J.J., Coyne K.J. (2011) Analysis of raphidophyte assimilatory nitrate reductase reveals unique domain architecture incorporating a 2/2 hemoglobin. Plant Mol. Biol. 77, 565–575.
  53. Filina V., Grinko A., Ermilova E. (2019) Truncated hemoglobins 1 and 2 are implicated in the modulation of phosphorus deficiency-induced nitric oxide levels in Chlamydomonas. Cells. 8(9), 947.
  54. Grinko A., Alqoubaili R., Lapina T., Ermilova E. (2021) Truncated hemoglobin 2 modulates phosphorus deficiency response by controlling of gene expression in nitric oxide-dependent pathway in Chlamydomonas reinhardtii. Planta. 254, 1–15.
  55. Plouviez M., Wheeler D., Shilton A., Packer M.A., McLenachan P.A., Sanz-Luque E., Ocaña-Calahorro F., Fernández E., Guieysse B. (2017) The biosynthesis of nitrous oxide in the green alga Chlamydomonas reinhardtii. Plant J. 91(1), 45–56.
  56. Plouviez M., Shilton A., Packer M.A., Guieysse B. (2019) Nitrous oxide emissions from microalgae: potential pathways and significance. J. Appl. Phycol. 31, 1–8.
  57. Burlacot A., Richaud P., Gosset A., Li-Beisson Y., Peltier G. (2020) Algal photosynthesis converts nitric oxide into nitrous oxide. Proc. Natl. Acad. Sci. USA. 117(5), 2704–2709.
  58. Zalutskaya Z., Dukhnov S., Leko N., Ermilova E. (2021) Nitric oxide levels and CYP55 expression in Chlamydomonas reinhardtii under normoxia and hypoxia. Protistology. 15(3), 153–160.
  59. Frungillo L., Skelly M.J., Loake G.J., Spoel S.H., Salgado I. (2014) S-nitrosothiols regulate nitric oxide production and storage in plants through the nitrogen assimilation pathway. Nat. Commun. 5(1), 5401.
  60. Jahnová J., Luhová L., Petřivalský M. (2019) S-nitrosoglutathione reductase – the master regulator of protein S-nitrosation in plant NO signaling. Plants. 8(2), 48.
  61. Tagliani A., Rossi J., Marchand C.H., De Mia M., Tedesco D., Gurrieri L., Meloni M., Falini G., Trost P., Lemaire S.D., Fermani S., Zaffagnini M. (2021) Structural and functional insights into nitrosoglutathione reductase from Chlamydomonas reinhardtii. Redox Biol. 38, 101806.
  62. Martínez-Ruiz A., Cadenas S., Lamas S. (2011) Nitric oxide signaling: classical, less classical, and nonclassical mechanisms. Free Radic. Biol. Med. 51(1), 17–29.
  63. de Montaigu A., Sanz-Luque E., Galvan A., Fernandez E. (2010) A soluble guanylate cyclase mediates negative signaling by ammonium on expression of nitrate reductase in Chlamydomonas. Plant Cell. 22(5), 1532–1548.
  64. Horst B.G., Stewart E.M., Nazarian A.A., Marletta M.A. (2019) Characterization of a carbon monoxide-activated soluble guanylate cyclase from Chlamydomonas reinhardtii. Biochemistry. 58(17), 2250–2259.
  65. Astier J., Rossi J., Chatelain P., Klinguer A., Besson-Bard A., Rosnoblet C., Jeandroz S., Nicolas-Francès V., Wendehenne D. (2021) Nitric oxide production and signalling in algae. J. Exp. Bot. 72(3), 781–792.
  66. Smith B.C., Marletta M.A. (2012) Mechanisms of S‑nitrosothiol formation and selectivity in nitric oxide signaling. Curr. Opin. Chem. Biol. 16(5–6), 498–506.
  67. Morisse S., Zaffagnini M., Gao X.H., Lemaire S.D., Marchand C.H. (2014) Insight into protein S-nitrosylation in Chlamydomonas reinhardtii. Antioxid. Redox Signal. 21(9), 1271–1284.
  68. Zaffagnini M., Michelet L., Sciabolini C., di Giacinto N., Morisse S., Marchand C.H., Trost P., Fermani S., Lemaire S.D. (2014) High-resolution crystal structure and redox properties of chloroplastic triosephosphate isomerase from Chlamydomonas reinhardtii. Mol. Plant. 7(1), 101–120.
  69. Berger H., De Mia M., Morisse S., Marchand C.H., Lemaire S.D., Wobbe L., Kruse O. (2016) A light switch based on protein S-nitrosylation fine-tunes photosynthetic light harvesting in Chlamydomonas. Plant Physiol. 171(2), 821–832.
  70. Sanz-Luque E., Ocaña-Calahorro F., Llamas A., Galvan A., Fernandez E. (2013) Nitric oxide controls nitrate and ammonium assimilation in Chlamydomonas reinhardtii. J. Exp. Bot. 64(11), 3373–3383.
  71. Zalutskaya Z., Kochemasova L., Ermilova E. (2018) Dual positive and negative control of Chlamydomonas PII signal transduction protein expression by nitrate/nitrite and NO via the components of nitric oxide cycle. BMC Plant Biol. 18, 1–10.
  72. Wei L., Derrien B., Gautier A., Houille-Vernes L., Boulouis A., Saint-Marcoux D., Malnoë A., Rappaport F., de Vitry C., Vallon O., Choquet Y., Wollman F.A. (2014) Nitric oxide-triggered remodeling of chloroplast bioenergetics and thylakoid proteins upon nitrogen starvation in Chlamydomonas reinhardtii. Plant Cell. 26(1), 353–372.
  73. De Mia M., Lemaire S.D., Choquet Y., Wollman F.A. (2019) Nitric oxide remodels the photosynthetic apparatus upon S-starvation in Chlamydomonas reinhardtii. Plant Physiol. 179(2), 718–731.
  74. Zalutskaya Z., Derkach V., Puzanskiy R., Ermilova E. (2020) Impact of nitric oxide on proline and putrescine biosynthesis in Chlamydomonas via transcriptional regulation. Biol. Plant. 64, 653–659.
  75. Chen X., Tian D., Kong X., Chen Q., Ef A., Hu X., Jia A. (2016) The role of nitric oxide signalling in response to salt stress in Chlamydomonas reinhardtii. Planta. 244, 651–669.

补充文件

附件文件
动作
1. JATS XML
下载
2.

下载 (124KB)
索引源数据
3.

下载 (504KB)
索引源数据

版权所有 © Е.В. Ермилова, 2023

##common.cookie##