Circadian changes in endogenous concentrations of indole-3-acetic acid, melatonin, serotonin, abscisic acid and jasmonic acid in characeae (Chara australis brown)

Plant Signaling and Behavior

Volumn 10, Issue 11, 2015, Pages

  Beilby, Mary J ^a   Turi, Christina E ^b   Baker, Teesha C ^b   Tymm, Fiona J M ^b   Murch, Susan J ^b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Abscisic acid; Characeae; Circadian rhythm; Indole 3 acetic acid; Jasmonic acid; Melatonin; Metabolic pathways; Serotonin

Indexed keywords

ABSCISIC ACID; CYCLOPENTANE DERIVATIVE; INDOLEACETIC ACID; INDOLEACETIC ACID DERIVATIVE; JASMONIC ACID; MELATONIN; OXYLIPIN; SEROTONIN;

ACCLIMATIZATION; CHARA; CIRCADIAN RHYTHM; MASS SPECTROMETRY; METABOLISM; PHOTOPERIODICITY; SEASON;

ABSCISIC ACID; ACCLIMATIZATION; CHARA; CIRCADIAN RHYTHM; CYCLOPENTANES; INDOLEACETIC ACIDS; MASS SPECTROMETRY; MELATONIN; OXYLIPINS; PHOTOPERIOD; SEASONS; SEROTONIN;

EID: 84959023945     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.1080/15592324.2015.1082697     Document Type: Article

References (75)

1. Covington MF, Harmer SL. The circadian clock regulates auxin signaling and responses in Arabidopsis. Plos Biol 2007; 5(8):e222; http://dx.doi.org/10.1371/journal.pbio.0050222.
2. Pavlova L, Krekule J. Fluctuation of free IAA under inductive and non-inductive photoperiods in Chenopodium rubrum. Plant Growth Regulation 1984; 2:91-98; http://dx.doi.org/10.1007/BF00024857.
3. Jouve J, Gaspar T, Kevers C, Greppin H, Degli Agosti R. Involvement of indole-3-acetic acid in the circadian growth of the first internode of Arabidopsis. Planta 1999; 209:136-142; PMID:10467040; http://dx.doi.org/10.1007/s004250050615.
4. Novakova M, Motyka V, Dobrev PI, Malbeck J, Gaudinova A, Vankova R. Diurnal variation of cytokinin, auxin and abscisic acid levels in tobacco leaves. J Experimental Botany 2005; 56:2877-2883; PMID:16157652; http://dx.doi.org/10.1093/jxb/eri282.
5. Cuin TA. Molecular aspects of the Arabidopsis circadian clock In “Rhytms in Plants,” Editors Mancuso S, Shabala S, Chapter 12, pp, 2007. 245-264. Springer Berlin, Heidelberg, New York
6. Dodd AN, Belbin FE, Frank A, Webb AR. Interactions between circadian clocks and photosynthesis for the temporal and spatial coordination of metabolism. Frontiers Plant Science 2015; 6:1–7; PMID:25657654.
7. Blatt MR. Potassium channel currents in intact stomatal guard cells: rapid enhancement by abscisic acid. Planta 1990; 180:445-455; PMID:24202027; http://dx.doi.org/10.1007/BF01160403.
8. Chater C, Kamisugi Y, Movahedi M, Fleming A, Cuming AC, Gray JE, Beerling DJ. Regulatory mechanism controlling stomatal behavior conserved across 400 million years of land plant evolution. Curr Biol 2011; 21:1025-1029; PMID:21658944; http://dx.doi.org/10.1016/j.cub.2011.04.032.
9. Hartung W. The evolution of abscisic acid (ABA) and ABA function in lower plants, fungi and lichen. Functional Plant Biol 2010; 37:806-812; http://dx.doi.org/10.1071/FP10058.
10. Brzezinski A. Melatonin in Humans. N Eng J Med 1997; 336:186-195; PMID:8988899; http://dx.doi.org/10.1056/NEJM199701163360306.
11. Hattori A, Migitaka, H, Masayake I, Itoh M, Yamamoto K, Ohtani-Kaneko R, Hara M, Suzuki, T, Reiter RJ. Identification of melatonin in plant seed its effects on plasma melatonin levels and binding to melatonin receptors invertebrates. Biochemistry Mol Biol International 1995; 35:627-34; PMID:7773197.
12. Dubbels R, Reiter RJ, Klenke E, Goebel A, Schnakenberg E, Ehlers C, Schiwara, HW, Schloot W. Melatonin in edible plants identified by radioimmunoassay and high-performance liquid chromatograph-mass spectrometry. J Pineal Res 1995; 18:28-31; PMID:7776176; http://dx.doi.org/10.1111/j.1600-079X.1995.tb00136.x
13. Murch SJ, Simmons CB, Saxena PX. Melatonin in feverfew and other medicinal plants. Lancet 1997; 350:1598-99; PMID:9393344; http://dx.doi.org/10.1016/S0140-6736(05)64014-7.
14. Murch SJ, Krishnara JS, Saxena PK. Tryptophan is a precursor for melatonin and serotonin biosynthesis in in vitro regenerated St. John’s wort (Hypericum perforatum L. cv. Anthos) plants. Plant Cell Reports 2000; 19:698-704; http://dx.doi.org/10.1007/s002990000206.
15. Murch SJ, Saxena PK. Mammalian neurohormones: Potential significance in reproductive physiology of St. John’s wort (Hypericum perforatum L.). Naturwissenschaften 2002; 89:555-560. PMID:12536277.
16. Tan D-X, Manchester LC, Rosales-Corral SA, Acuna-Castroviejo D, Reiter RJ. Mitochondria and chloroplasts as the original sites of melatonin synthesis: a hypothesis related to melatonin’s primary function and evolution in eukaryotes. J Pineal Res 2013; 54:127-138; http://dx.doi.org/10.1111/jpi.12026.
17. Park S, Lee D-E, Jang H, Byeon Y, Kim Y-S, Back K. Melatonin-rich rice plants exhibit resistance to herbicide-induced oxidative stress. J Pineal Res 2013; 54:258-263; http://dx.doi.org/10.1111/j.1600-079X.2012.01029.x
18. Okazaki M, Higuchi K, Aouinia A, Ezura H. Lowering inter-cellular melatonin levels by transgenic analysis of indoleamine 2,3-dioxygenase from rice in tomato plants. J Pineal Res 2010; 49:239-247; PMID:20609074; http://dx.doi.org/10.1111/j.1600-079X.2010.00788.x
19. Kang S, Kang K, Lee K, Back K. Characterization of rice tryptophan decarboxylases and their direct involvement in serotonin biosynthesis in transgenic rice. Planta 2007; 227:263-272; PMID:17763868; http://dx.doi.org/10.1007/s00425-007-0614-z
20. Kang K, Kong K, Park S, Natsagdorj U, Kim YS, Back K. Molecular cloning of a plant N-acetylserotonin methyltransferase and its expression characteristics in rice. J Pineal Res 2011; 50:304-309; PMID:21210840; http://dx.doi.org/10.1111/j.1600-079X.2010.00841.x
21. Kang K, Lee K, Park S, Byeon Y, Back K. Molecular cloning of rice serotonin N_acetyltransferase, the penultimate gene in plant melatonin biosynthesis. J Pineal. Res 2012; 55:7-13; PMID:22998587;http://dx.doi.org/10.1111/jpi.12011.
22. Park S, Lee K, Kim YS, Back K. Tryptamine 5-hydroxylase-deficient Sekiguchi rice induces synthesis of 5-hydroxytryptophan and N-acetyltryptamine but decreases melatonin biosynthesis during senescence process of detached leaves. J Pineal Res 2011; 52:211-216; PMID:21884550; http://dx.doi.org/10.1111/j.1600-079X.2011.00930.x
23. Reiter RJ, Tan D-X, Zhou Z, Coelho Cruz MH, Fuentes-Broto L, Galano A. Phytomelatonin: Assisting plants to survive and thrive. Molecules 2015; 20:7396-7437; PMID:25911967; http://dx.doi.org/10.3390/molecules20047396.
24. Murch SJ, Campbell SSB, Saxena PK. The role of serotonin and melatonin in plant morphogenesis: regulation of auxin-induced root organogenesis in in vitro cultured explants of St. John’s wort (Hypericum perforatum L.). Vitro Cell Dev Biol 2001; 37:786-793; http://dx.doi.org/10.1007/s11627-001-0130-y
25. Murch SJ, Saxena PK. Role of indoleamines in regulation of morphogenesis in in vitro cultures of St. John’s wort (Hypericum perforatum L.) Acta Horticulturae 2004:629: 26 International Horticultural Congress: The Future for Medicinal and Aromatic Plants
26. Jones MPA, Yi Z, Murch SJ, Saxena PK. Thidiazuroninduced regeneration of Echinacea purpurea L.: Micropropagation in solid and liquid culture systems. Plant Cell Reports 2007; 26:13-19; PMID:16897009; http://dx.doi.org/10.1007/s00299-006-0209-3.
27. Murch SJ, Ali AR, Cao J, Saxena PK. Melatonin and serotonin in flowers and fruits of Datura metel L. J Pineal Res 2009; 47:277-83; PMID:19732299; http://dx.doi.org/10.1111/j.1600-079X.2009.00711.x
28. Murch SJ, Hall BA, Le CH, Saxena PK. Changes in the levels of indoleamine phytochemicals in v_eraison and ripening of wine grapes. J Pineal Res 2010; 49:95-100; PMID:20536685.
29. Tan D-X, Mancheste R LC, Terron MP, Flores LJ, Reiter RJ. One molecule, many derivatives: a neverending interaction of melatonin with reactive oxygen and nitrogen species? J Pineal Res 2007; 42:28-42; http://dx.doi.org/10.1111/j.1600-079X.2006.00407.x
30. Brown PN, Turi CE, Shipley PR, Murch SJ. Phytochemical discovery in large cranberry (Vaccinium macrocarpon Ait.) and small cranberry (Vaccinium oxycoccus L. and Vaccinium vitis-idaea L.) in British Columbia. Planta Medica 2012; 78:1-11; http://dx.doi.org/10.1055/s-0031-1280418.
31. Wang P, Yin L, Liang D, Li CH, Ma F, Yue Z. Delayed senescence of apple leaves by exogenous melatonin treatment: toward regulating the ascorbate–glutathione J Pineal Res 2012; 53:11-20; PMID:21988707; http://dx.doi.org/10.1111/j.1600-079X.2011.00966.x
32. Zhang N, Zhao B, Zhang H-J, Weeda S, Yang C, Yang Z-C, Ren S, Guo Y-D. Melatonin promotes waterstress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L.). J Pineal Res 2013; 54:15-23.
33. Lazár D, Murch SJ, Beilby MJ, Al Khazaaly S. Exogenous melatonin affects photosynthesis in Characeae Chara australis. Plant Signal Behav 2013; 8(3):1–5: e23279i
34. Poeggeler B, Balzer I, Hardeland R, Lerchl A. Pineal hormone melatonin oscillates also in the dinoflagellate Gonyaulax polyedra. Naturwissenschaften 1991; 78, 268-9; http://dx.doi.org/10.1007/BF01134354.
35. Wolf K, Kolář J, Witters E, Van Dongen W, Van Onckelen H, Macháčková I. Daily profile of melatonin levels in Chenopodium rubrum L. depends on photoperiod. J Plant Physiol 2001; 158:1491-93; http://dx.doi.org/10.1078/0176-1617-00561.
36. Hardeland R, Baker I, Poeggeler B, Fuhrberg B, Uria H, Behrmann G, Wolf R, Meyer TJ, Reiter RJ. On the primary functions of melatonin in evolution: Mediation of photoperiodic signals in a unicell, photooxidation, and scavenging of free radicals. J Pineal Res 1995; 18:104-111; PMID:7629689; http://dx.doi.org/10.1111/j.1600-079X.1995.tb00147.x
37. Roopin M. Yacobi YZ, Levy O. Occurrence, diel patterns, and the influence of melatonin on the photosynthetic performance of cultured Symbiodinium. J Pineal Res 2013; 55:89-100; http://dx.doi.org/10.1111/jpi.12046.
38. Van Tassel DL, Roberts N, Lewy A, O’Neil SD. Melatonin in plant organs. J Pineal Res 2001; 31:8-15; PMID:11485009; http://dx.doi.org/10.1034/j.1600-079X.2001.310102.x
39. Tan D-X, Manchester LC, Di Mascio P, Martinez GR, Prado FM, Reiter RJ. Novel rhythms of N1-acetyl-N2-formyl-5-methoxykynuramine and its precursor melatonin in water hyacinth: importance for phytoremediation. FASEB J 2007; 21:1724-29; PMID:17314136; http://dx.doi.org/10.1096/fj.06-7745com
40. Boccalandro HE, Gonzalez CV, Wunderlin DA, Silva MF. Melatonin levels, determined by LC-ESI-MS/MS, fluctuate during the day/night cycle in Vitis vinifera cv Malbec: evidence of its antioxidant role in fruits. J Pineal Res 2011; 51:226-232; PMID:21605162; http://dx.doi.org/10.1111/j.1600-079X.2011.00884.x
41. Tal O, Haim A, Harel O, Gerchman Y. Melatonin as an antioxidant and its semi-lunar rhythm in green macroalga Ulva sp. J Exp Bot 2011; 62:1903-1910; PMID:21220782;http://dx.doi.org/10.1093/jxb/erq378.
42. Arnao MB, Hernandez-Ruiz J. Functions of melatonin in plants: a review. J Pineal Res, early online view 2015; 59(2):133-50; PMID:26094813.
43. Kolář J, Macháčková I. Melatonin in higher plants: occurrence and possible functions. J Pineal Res 2005; 39:333-41; http://dx.doi.org/10.1111/j.1600-079X.2005.00276.x
44. Clabeaux BL, Bisson MA. Developmental patterns in Chara australis (Characeae, Charophyceae): apical dominance, pH and auxin. Charophytes 2009; 1:68-72.
45. Boot K, Libbenga KR, Hille SC, Offringa R, Van Duijn B. Polar auxin transport: an early invention. J Exp Bot 2012; 63:4213-4218; PMID:22473986; http://dx.doi.org/10.1093/jxb/ers106.
46. Raven JA. Polar auxin transport in relation to long-distance transport of nutrients in the Charales. J Exp Bot 2013; 64:1-9; PMID:23264638; http://dx.doi.org/10.1093/jxb/ers358.
47. Beilby MJ, AL Khazaaly S, Bisson MA. Salinity-Induced noise in membrane potential of Characeae Chara australis: Effect of exogenous melatonin. J Membrane Biol 2014; 248:93-102; PMID:25378124; http://dx.doi.org/10.1007/s00232-014-9746-9.
48. McCourt RM, Delwiche CF, Karol KG. Charophyte algae and land plant origins. Trends Ecol Evol 2004; 19:661-666; PMID:16701329; http://dx.doi.org/10.1016/j.tree.2004.09.013.
49. Hope AB, Walker NA. The Physiology of Giant Algal Cells. Cambridge University Press, UK. 1975.
50. Beilby MJ, Casanova MT. The Physiology of Characean Cells. Springer, Heidelberg, New York, Dodrecht, London. 2013.
51. Shimmen, T. The sliding theory of cytoplasmic streaming: fifty years of progress. J Plant Res 2007; 120:31-43; http://dx.doi.org/10.1007/s10265-006-0061-0.
52. Braun M, Limbach C. Rhizoids and protonemata of characeaen algae: model cells for research on polarized growth and plant gravity sensing. Protoplasma 2006; 229:133-142; PMID:17180494;http://dx.doi.org/10.1007/s00709-006-0208-9.
53. Zhao Y, Tan D-X, Lei Q, Chen H, Wang L, Li Q, Gao Y, Kong J. Melatonin and it potential biological functions in the fruits of sweet cherry. J Pineal Res 2012; 55:79-88; http://dx.doi.org/10.1111/jpi.12044.
54. Shi H, Reiter RJ, Tan D-X, Chan Z. Indole-3-acetic acid inducible 17 positively modulates natural leaf senescence through melatonin-mediated pathway in Arabidopsis. J Pineal Res 2015; 58:26-33; http://dx.doi.org/10.1111/jpi.12188.
55. Braun M, Richter P. Relocalization of the calcium gradient and a dihydropyridine receptor is involved in upward bending by bulging of Chara protonemata, but not in downward bending by bowing of Chara rhizoids. Planta 1999; 209:414-423; http://dx.doi.org/10.1007/s004250050744.
56. Slovin JP, Cohen JD. Levels of indole-3-acetic acid in Lemna gibba G-3 and in a large Lemna mutant regenerated from tissue culture. Plant Physiology 1988; 86:522-526; PMID:16665940; http://dx.doi.org/10.1104/pp.86.2.522.
57. Casanova MT. Vegetative and reproductive responses of charophytes to water-level fluctuactions in permanent and temporary wetlands of Australia. Australian Marine Freshwater Res 1994; 45:1409-1419; http://dx.doi.org/10.1071/MF9941409.
58. Hackenbeg D, Pandey S. Heterotrimeric G proteins in green algae. Plant Signaling Behavior 2014; 9:e28457; http://dx.doi.org/10.4161/psb.28457.
59. Du H, Liu H, Xiong L. Endogenous auxin and jasmonic acid levels are differentially modulated by abiotic stresses in rice. Frontiers Plant Sci 2013; 4:4; PMID:23355843.
60. Kanno Y, Jikumaru Y, Hanada A, Nambara E, Abrams SR, Kamiya Y, Seo M. Comprehensive Hormone Profiling in Developing Arabidopsis Seeds: Examination of the Site of ABA Biosynthesis, ABA Transport and Hormone Interactions. Plant Cell Physiol 2010; 51:1988-2001; PMID:20959378; http://dx.doi.org/10.1093/pcp/pcq158.
61. Liu J, Wang X-J. An integrative analysis of the effects of auxin on jasmonic acid biosynthesis in Arabidopsis thaliana. J Integrative Plant Biol 2006; 4:99-103; http://dx.doi.org/10.1111/j.1744-7909.2006.00206.x
62. Ljung K. Auxin metabolism and homeostasis during plant development. Development 2013; 140:943-950; PMID:23404103; http://dx.doi.org/10.1242/dev.086363.
63. Normanly J. Approaching cellular and molecular resolution of auxin biosynthesis and metabolism. Cold Spring Harbor Perspectives Biol 2010; 2, a001594; PMID:20182605;http://dx.doi.org/10.1101/cshperspect.a001594.
64. Ludwick-Müller J. Auxin conjugates: their role for plant development and in the evolution of land plants. J Exp Botany 2011; 62:1757-1773; PMID:21307383; http://dx.doi.org/10.1093/jxb/erq412.
65. Sztein AE, Cohen JD, Cooke TJ. Evolutionary patterns in the auxin metabolism of green plants. International J Plant Science 2000; 161:849-859; http://dx.doi.org/10.1086/317566.
66. Mano Y, Nemoto K. The pathway of auxin biosynthesis in plants. J Exp Botany 2012; 63:2853-72; PMID:22447967;http://dx.doi.org/10.1093/jxb/ers091.
67. Karol KG, McCourt RM, Cimino MT, Delwiche CF. The closest living relatives of land plants. Science 2001; 294:2351-2353. PMID:11743201; http://dx.doi.org/10.1126/science.1065156.
68. Wodniok S, Brinkmann H, Glockner G, Heidel AJ, Philippe H, Melkonian M, Becker B. Origin of land plants: Do conjugating green algae hold the key? BMC Evolutionary Biol 2011; 11:104-114. PMID:21501468; http://dx.doi.org/10.1186/1471-2148-11-104.
69. Timme RE, Bachvaroff TR, Delwiche CHF. Broad phylogenomic sampling and the sister lineage of land plants. PloS One. 2012; 7:1–8:e29696; PMID:22253761;http://dx.doi.org/10.1371/journal. pone.0029696.
70. Wang C, Liu Y, Li S-S, Han G-Z. Insights into the origin and evolution of the plant hormone signaling machinery. Plant Physiol 2015; 167:872-886; PMID:25560880; http://dx.doi.org/10.1104/pp.114.247403.
71. Sakayama H, Toyoda A, Suzuki Y, Fujiyama A, Rensing SA, Nishiyama T. The Chara braunii genome sheds light on the origin of land plants. 2015; https://pag.confex.com/pag/xxiii/webprogram/Paper15915.html
72. Felle H, Brummer B, Bertl A, Parish RW. Indole-3-acetic acid and fusicoccin cause cytosolic acidification of corn coleoptile cells. Proc Natl Acad Sci USA 1986; 83:8992-8995; http://dx.doi.org/10.1073/pnas.83.23.8992.
73. Felle H, Peters W, Palme K. The electrical response of maize to auxins. Biochimica Et Biophysica Acta 1991; 1064:199-204; PMID:1827995; http://dx.doi.org/10.1016/0005-2736(91)90302-O
74. Kwiatkowska M, Poptonńska K, Gosek A, Malinowski S. Circadian rhythm of protein synthesis in generative and non-generative antheridial cells of Chara vulgaris L. Biological Rhythm Res 1995; 26:55-67; http://dx.doi.org/10.1080/09291019509360324.
75. Turi CE, Axwik KE, Smith A, Jones AMP, Saxena PK, Murch SJ. Galanthamine, an anti-cholinesterase drug, effects plant growth and development in Artemisia tridentata Nutt via modulation of auxin and neurotransmitter signaling. Plant Signaling Behavior 2014; 9:e28645; http://dx.doi.org/10.4161/psb.28645