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Botanica Marina

Editor-in-Chief: Dring, Matthew J.


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Volume 60, Issue 2

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Phytohormones in red seaweeds: a technical review of methods for analysis and a consideration of genomic data

Izumi C. Mori
  • Institute of Plant Science and Resources, Okayama University, 2-20-1 Chuo, 710-0046 Kurashiki, Japan
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Yoko Ikeda
  • Institute of Plant Science and Resources, Okayama University, 2-20-1 Chuo, 710-0046 Kurashiki, Japan
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Takakazu Matsuura
  • Institute of Plant Science and Resources, Okayama University, 2-20-1 Chuo, 710-0046 Kurashiki, Japan
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Takashi Hirayama
  • Institute of Plant Science and Resources, Okayama University, 2-20-1 Chuo, 710-0046 Kurashiki, Japan
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Koji Mikami
  • Corresponding author
  • Faculty of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, 041-8611 Hakodate, Japan
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2017-03-30 | DOI: https://doi.org/10.1515/bot-2016-0056

Abstract

Emerging studies suggest that seaweeds contain phytohormones; however, their chemical entities, biosynthetic pathways, signal transduction mechanisms, and physiological roles are poorly understood. Until recently, it was difficult to conduct comprehensive analysis of phytohormones in seaweeds because of the interfering effects of cellular constituents on fine quantification. In this review, we discuss the details of the latest method allowing simultaneous profiling of multiple phytohormones in red seaweeds, while avoiding the effects of cellular factors. Recent studies have confirmed the presence of indole-3-acetic acid (IAA), N6-(Δ2-isopentenyl)adenine (iP), (+)-abscisic acid (ABA), and salicylic acid, but not of gibberellins and jasmonate, in Pyropia yezoensis and Bangia fuscopurpurea. In addition, an in silico genome-wide homology search indicated that red seaweeds synthesize iP and ABA via pathways similar to those in terrestrial plants, although genes homologous to those involved in IAA biosynthesis in terrestrial plants were not found, suggesting the epiphytic origin of IAA. It is noteworthy that these seaweeds also lack homologues of known factors involved in the perception and signal transduction of IAA, iP, and ABA. Thus, the modes of action of these phytohormones in red seaweeds are unexpectedly dissimilar to those in terrestrial plants.

Keywords: epiphytes; genome-wide survey; hormone metabolism; liquid chromatography–mass spectrometry; phytohormone; red seaweed; simultaneous analysis

References

  • Abel, S., P.W. Oeller and A. Theologis. 1994. Early auxin-induced genes encode short-lived nuclear proteins. Proc. Natl. Acad. Sci. USA 91: 326–330.Google Scholar

  • Abel, S., M.D. Nguyen and A. Theologis. 1995. The PS-IAA4/5-like family of early auxin-inducible mRNAs in Arabidopsis thaliana. J. Mol. Biol. 251: 533–549.Google Scholar

  • Alcazar, R., T. Altabella, F. Marco, C. Bortolotti, M. Reymond, C. Koncz, P. Carrasco and A.F. Tiburcio. 2010. Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231: 1237–1249.Google Scholar

  • Amin, S.A., L.R. Hmelo, H.M. van Tol, B.P. Durham, L.T. Carlson, K.R. Heal, R.L. Morales, C.T. Berthiaume, M.S. Parker, B. Djunaedi, A.E. Ingalls, M.R. Parsek, M.A. Moran and E.V. Armbrust. 2015. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522: 98–101.Google Scholar

  • Banerjee, S. and S. Mazumdar. 2012. Electrospray ionization mass spectrometry: a technique to access the information beyond the molecular weight of the analyte. Int. J. Anal. Chem. 2012: 282574.Google Scholar

  • Barber, M., R.S. Bordoli, G.J. Elliott, R.D. Sedgwick and A.N. Tyler. 1982. Fast atom bombardment mass spectrometry. Ana. Chem. 58: 2949–2954.Google Scholar

  • Basu, S., H. Sun, L. Brian, R.L. Quatrano and G.K. Muday. 2002. Early embryo development in Fucus distichus is auxin sensitive. Plant Physiol. 130: 292–302.Google Scholar

  • Bennett, M.J., A. Marchant, H.G. Green, S.T. May, S.P. Ward, P.A. Millner, A.R. Walker, B. Schulz and K.A. Feldmann. 1996. Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273: 948–950.Google Scholar

  • Blakey, C.R. and M.L. Vestal. 1983. Thermospray interface for liquid chromatography/mass spectrometry. Anal. Chem. 55: 750–754.Google Scholar

  • Blechschmidt, S., U. Castel, P. Gaskin, P. Hedden, J.E. Graebe and J. MacMillan. 1984. GC/MS analysis of the plant hormones in seeds of Cucubita maxima. Phytochemistry 23: 553–558.Google Scholar

  • Bruins, A.P., R.R. Covey and J.D. Henion. 1987. Ion spray interface for combined liquid chromatography/atmospheric pressure ionization mass spectrometry. Anal. Chem. 59: 2642–246.Google Scholar

  • Cantwell, F.F. and M. Losier. 2002. Liquid–liquid extraction. In: (D. Barcelo ed.) Sampling and sample preparation for field and laboratory. Comprehensive analytical chemistry. Elsevier. Vol. 37. pp. 297–340.Google Scholar

  • Caprioli, R.M. and T. Fan. 1986. Continuous-flow sample probe for fast arom bombardment mass spectrometry. Anal Chem. 58: 2949–2954.Google Scholar

  • Carreno-Lopez, R. N. Campos-REalis, C. Elmerich and B.E. Baca. 2000. Physiological evidence for differently regulated tryptophan-dependent pathways for indole–3–acetic acid synthesis in Azopirillum brasilense. Mol. Gen. Genet. 264: 521–530.Google Scholar

  • Chan, C.X., N.A. Blouin, Y. Zhuang, S. Zäuner, S.E. Prochnik, E. Lindquist, S. Lin, C. Benning, M. Lohr, C. Yarish, E. Gantt, A.R. Grossman, S. Lu, K. Müller, J. Stiller, S.H. Brawley and D. Bhattacharya. 2012a. Porphyra (Bangiophyceae) transcriptomes provide insights into red algal development and metabolism. J Phycol. 48: 1328–1342.Google Scholar

  • Chan, C.X., S. Zäuner, G.L. Wheeler, A.R. Grossman, S.E. Prochnik, N.A. Blouin, Y. Zhuang, C. Benning, G.M. Berg, C. Yarish, R.L. Eriksen, A.S. Klein, S. Lin, I. Levine, S.H. Brawley and D. Bhattacharya. 2012b. Analysis of Porphyra membrane transporters demonstrates gene transfer among photosynthetic eukaryotes and numerous sodium-coupled transport systems. Plant Physiol. 158: 2001–2012.Google Scholar

  • Chen, K.H., A.N. Miller, G.W. Patterson and J.D. Cohen. 1988. A rapid and simple procedure for purification of indole-3-acetic acid prior to GC-SIM-MS analysis. Plant Physiol. 86: 822–825.Google Scholar

  • Chiwocha, S.D.S., S.R. Abrams, S.J. Ambrose, A.J. Cutler, M. Loewen, A.R.S. Ross and A.R. Kermode. 2003. A method for profiling classes of plant hormones and their metabolites using liquid chromatography-electrospray ionization tandem mass spectrometry: an analysis of hormone regulation of thermodormancy of lettuce (Lactuca sativa L.) seeds. Plant J. 35: 405–417.Google Scholar

  • Cock, J.M., L. Sterck, P. Rouzé, D. Scornet, A.E. Allen, G. Amoutzias, V. Anthouard, F. Artiguenave, J.M. Aury, J.H. Badger, B. Beszteri, K. Billiau, E. Bonnet, J.H. Bothwell, C. Bowler, C. Boyen, C. Brownlee, C.J. Carrano, B. Charrier, G.Y. Cho, S.M. Coelho, J. Collén, E. Corre, C. Da Silva, L. Delage, N. Delaroque, S.M. Dittami, S. Doulbeau, M. Elias, G. Farnham, C. M. Gachon, B. Gschloessl, S. S. Heesch, K. Jabbari, C. Jubin, H. Kawai, K. Kimura, B. Kloareg, F.C. Küpper, D. Lang, A. Le Bail, C. Leblanc, P. Lerouge, M. Lohr, P.J. Lopez, C. Martens, F. Maumus, G. Michel, D. Miranda-Saavedra, J. Morales, H. Moreau, T. Motomura, C. Nagasato, C.A. Napoli, D.R. Nelson, P. Nyvall-Collén, A.F. Peters, C. Pommier, P. Potin, J. Poulain, H. Quesneville, B. Read, S.A. Rensing, A. Ritter, S. Rousvoal, M. Samanta, G. Samson, D.C. Schroeder, B. Ségurens, M. Strittmatter, T. Tonon, J.W. Tregear, K. Valentin, P. von Dassow, T. Yamagishi, Y. Van de Peer and P. Wincker. 2010. The Ectocarpus genome and the independent evolution of multicellularity in the brown algae. Nature 465: 617–621.Google Scholar

  • Collén, J., B. Porcel, W. Carré, S.G. Ball, C. Chaparro, T. Tonon, T. Barbeyron, G. Michel, B. Noel, K. Valentin, M. Elias, F. Artiguenave, A. Arun, J.M. Aury, J.F. Barbosa-Neto, J.H. Bothwell, F.Y. Bouget, L. Brillet, F. Cabello-Hurtado, S. Capella-Gutiérrez, B. Charrier, L. Cladière, J.M. Cock, S.M. Coelho, C. Colleoni, M. Czjzek, C. Da Silva, L. Delage, F. Denoeud, P. Deschamps, S.M. Dittami, T. Gabaldón, C.M. Gachon, A. Groisillier, C. Hervé, K. Jabbari, M. Katinka, B. Kloareg, N. Kowalczyk, K. Labadie, C. Leblanc, P.J. Lopez, D.H. McLachlan, L. Meslet-Cladiere, A. Moustafa, Z. Nehr, P. Nyvall-Collén, O. Panaud, F. Partensky, J. Poulain, S.A. Rensing, S. Rousvoal, G. Samson, A. Symeonidi, J. Weissenbach, A. Zambounis, P. Wincker and C. Boyen. 2013. Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc. Natl. Acad. Sci. USA 110: 5247–5252.Google Scholar

  • Crozier, A., K. Loferski, J.B. Zaerr and R.O. Morris. 1980. Analysis of picogram quantities of indole-3-acetic acid by high performance liquid chromatography-fluorescence procedures. Planta 150: 366–370.Google Scholar

  • Cutler, S.R., P.L. Rodriguez, R.R. Finkelstein and S.R. Abrams. 2010. Abscisic acid: emergence of a core signaling network. Ann. Rev. Plant Biol. 61: 651–679.Google Scholar

  • De Meyer, G. and M. Höfte. 1997. Salicylic acid produced by the Rhizobacterium Pseudomonas aeruginosa 7NSK2 induces resistance to leaf infection by Botrytis cinerea on bean. Phytopathol. 87: 588–593.Google Scholar

  • De Smet, I., U. Voß, S. Lau, M. Wilson, N. Shao, R.E. Timme, R. Swarup, I. Kerr, C. Hodgman, R. Bock, M. Bennett, G. Jürgens and T. Beeckman. 2011. Unraveling the evolution of auxin signaling. Plant Physiol. 155: 209–221.Google Scholar

  • Ding, J., L.J. Mao, B.F. Yuan and Y.Q. Feng. 2013. A selective retreatment method for determination of endogenous active brassinosteroids in plant tissues: double layered solid phase extraction combined with boronate affinity polymer monolith microextraction. Plant Methods 9: 13.Google Scholar

  • Dharmasiri, N., S. Dharmasiri and M. Estelle. 2005. The F-box protein TIR1 is an auxin receptor. Nature 435: 441–445.Google Scholar

  • Dodds, S.C., O. Garrod and S.A. Simpson. 1956. Endocrinology (The hormones). Ann. Rev. Med. 7: 41–88.Google Scholar

  • Egan, S., T. Harder, C. Burke, P. Steinberg, S. Kjelleberg and T. Thomas. 2013. The seaweed holobiont: understanding seaweed-bacteria interactions. FEMS Microbiol. Review 37: 462–476.Google Scholar

  • Fenselau, C. and R.J. Cotter. 1987. Chemical aspects of fast atom bombardment. Chem. Rev. 87: 501–512.Google Scholar

  • Forcat, S., M.H. Bennett, J.W. Mansfield and M.R. Grant. 2008. A rapid and robust method for simultaneously measuring changes in the phytohormones ABA, JA and SA in plants following biotic and abiotic stress. Plant Methods 4: 16.Google Scholar

  • Fries, L. 1975. Some observations on the morphology of Enteromorpha linza (L.) J. Ag. and Enteromorpha compressa (L.) Grev. in axenic culture. Bot. Mar. 18: 251–253.Google Scholar

  • Galston, A.W. and R.K. Sawhney. 1990. Polyamines in plant physiology. Plant Physiol. 94: 406–410.Google Scholar

  • Gälweiler, L., C. Guan, A. Müller, E. Wisman, K. Mendgen, A. Yephremov and K. Palme. 1998. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282: 2226–2230.Google Scholar

  • Garcia-Jimenez, P., O. Brito-Romano and R.R. Robaina. 2013. Production of volatiles by the red seaweed Gelidium arbuscula (Rhodophyta): emission of ethylene and dimethyl sulfide. J. Phycol. 49: 661–669.Google Scholar

  • Gergov, M., T. Nenoen, I. Ojanpera and R.A. Ketola. 2015. Compensation of matrix effects in a standard addition method for metformin in postmortem blood using liquid chromatography–electrospray–tandem mass spectrometry. J. Anal. Toxicol. 39: 359–364.Google Scholar

  • Grueneberg, J., A.H. Engelen, R. Costa and T. Wichard. 2016. Macroalgal morphogenesis induced by waterborne compounds and bacteria in coastal seawater. PLoS ONE 11: e0146307.Google Scholar

  • Guilfoyle, T.J., T. Ulmasov and G. Hagen. 1998. The ARF family of transcription factors and their role in plant hormone-responsive transcription. Cell Mol. Life Sci. 54: 619–627.Google Scholar

  • Hayashi, K., K. Horie, Y. Hiwatashi, H. Kawaide, S. Yamaguchi, A. Handa, T. Nakashima, M. Nakajima, L.M. Mander, H. Yamane, M. Hasebe, H. Nozaki. 2010. Endogenous diterpenes derived from ent-kaurene, a common gibberellin precursor, regulate protonema differentiation of the moss Physcomitrella patens. Plant Physiol. 153: 1085–1097.Google Scholar

  • Hedden, P. 1993. Modern methods for the quantitative analysis of plant hormones. Annu. Rev. Plant Physiol. Plant Mol. Biol. 44: 107–129.Google Scholar

  • Hisano, H., T. Matsuura, I.C. Mori, M. Yamane and K. Sato. 2016. Endogenous hormone levels affect the regeneration ability of callus derived from different organs in barley. Plant Physiol. Biochem. 99: 66–72.Google Scholar

  • Iehisa, J.C.M., T. Matsuura, I.C. Mori and S. Takumi. 2013. Identification of quantitative trait locus for abscisic acid responsiveness on chromosome 5A and association with dehydration tolerance in common wheat seedlings. J. Plant Physiol. 171: 25–34.Google Scholar

  • Iehisa, J.C.M., T. Matsuura, I.C. Mori, H. Yokota, F. Kobayashi and S. Takumi. 2014. Identification of quantitative trait loci for abscisic acid responsiveness in the D-genome of hexaploid wheat. J. Plant Physiol. 171: 830–841.Google Scholar

  • Inoue, T., M. Higuchi, Y. Hashimoto, M. Seki, M. Kobayashi, T. Kato, S. Tabata, K. Shinozaki and T. Kakimoto. 2001. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409: 1060–1063.Google Scholar

  • Jaillais, Y. and J. Chory. 2010. Unraveling the paradoxes of plant hormone signaling integration. Nat. Struct. Mol. Biol. 17: 642–645.Google Scholar

  • Joint, I., K. Tait and G. Wheeler. 2007. Cross-kingdom signalling: exploitation of bacterial quorum sensing molecules by the green seaweed Ulva. Philos. Trans. R. Soc, Lond. B Biol. Sci. 362: 1223–1233.Google Scholar

  • Kamboj, J. S., G. Browning, P.S. Blake, J.D. Quinlan and D.A. Baker. 1999. GC-MS-SIM analysis of abscisic acid and indole-3-acetic acid in shoot bark of apple roostocks. Plant Growth Regul. 28: 21–27.Google Scholar

  • Kamiya, Y. 2010. Plant hormones: versatile regulators of plant growth and developement. Annu. Rev. Plant Biol. 61. Special Online Compilation.Google Scholar

  • Kanno, Y., Y. Jikumaru, A. Hanada, E. Nambara, S.R. Abrams, Y. Kamiya and M. Seo. 2010. Comprehensive hormone profiling in developing Arabidopsis seeds: examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant Cell Physiol. 51: 1988–2001.Google Scholar

  • Kawakami, N., Y. Miyake and K. Noda. 1997. ABA insensitivity and low ABA levels during seed development of non-dormant wheat mutants. J. Exp. Bot. 48: 1415–1421.Google Scholar

  • Kende, H. and J.A.D. Zeevaart. 1997. The five “classical” plant hormones. Plant Cell 9: 1197–1210.Google Scholar

  • Klingler, J.P., G. Batelli and J.K. Zhu. 2010. ABA receptors: the START of a new paradigm in phytohormone signalling. J. Exp. Bot. 61: 3199–3210.Google Scholar

  • Kojima, M., T. Kamada-Nobusada, H. Komatsu, K. Takei, T. Kuroha, M. Mizutani, M. Ashikari, M. Ueguchi-Tanaka, M. Matsuoka, K. Suzuki and H. Sakakibara. 2009. Highly sensitive and high-throughput analysis of plant hormones using MS-probe modification and liquid chromatography-tandem mass spectrometry: an application for hormone profiling in Oryza sativa. Plant Cell Physiol. 50: 1201–1214.Google Scholar

  • Lau, S., N. Shao, R. Bock, G. Jürgens and I. De Smet. 2009. Auxin signaling in algal lineages: fact or myth? Trends Plant Sci. 14: 182–188.Google Scholar

  • Le Bail, A., B. Billoud, N. Kowalczyk, M. Kowalczyk, M. Gicquel, S. Le Panse, S. Stewart, D. Scornet, J.M. Cock, K. Ljung and B. Charrier. 2010. Auxin metabolism and function in the multicellular brown alga Ectocarpus siliculosus. Plant Physiol. 153: 128–144.Google Scholar

  • Lemiere, F. 2001. Interfaces for LC–MS. Guide to LC–MS. LC-GC Europe. pp. 29–35.Google Scholar

  • Liu, X., K. Bogaert, A.H. Englen, F. Leliaert, M.Y. Roleda and O. De Clerck. 2017. Seaweed reproductive biology: environmental and genetic controls. Bot. Mar. 60: 89–108.Google Scholar

  • Lu, Y., Y. Sasaki, X.W. Li, I.C. Mori, T. Matsuura, T. Hirayama, T. Sato and J. Yamaguchi. 2015. ABI1 regulates carbon/nitrogen-nutrient signal transduction independent of ABA biosynthesis and canonical ABA signaling pathways in Arabidopsis. J. Exp. Bot. 66: 2763–2771.Google Scholar

  • Mano, Y. and K. Nemoto. 2012. The pathway of auxin biosynthesis in plants. J. Exp. Bot. 63: 2853–2872.Google Scholar

  • Manulis, S., A. Haviv-Chesner, M.T. Brandl, S.E. Lindow and I Barash. 1998. Differential involvement of indole-3-acetic acid biosynthetic pathways in pathogenicity and epiphytic fitness of Erwinia hebicola pv. gypsophilae. Mol. Plant-Microb. Interact. 11: 634–642.Google Scholar

  • Marchant, A., J. Kargul, S.T. May, P. Muller, A. Delbarre, C. Perrot-Rechenmann and M.J. Bennett. 1999. AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J. 18: 2066–2073.Google Scholar

  • Matsubayashi, Y. and Y. Sakagami. 2006. Peptide hormones in Plants. Ann. Rev. Plant Biol. 57: 649–674.Google Scholar

  • Meuwly, P. and J.P. Metraux. 1993. Ortho-anisic acid as internal standard for the simultaneous quantification of salicylic acid and its putative biosynthetic precursors in cucumber leaves. Anal. Biochem. 214: 500–505.Google Scholar

  • Mikami, K. and M. Hosokawa. 2013. Biosynthetic pathway and health benefits of fucoxanthin, an algae-specific xanthophyll in brown seaweeds. Int. J. Mol. Sci. 14: 13763–13781.Google Scholar

  • Mikami, K., I.C. Mori, T. Matsuura, Y. Ikeda, M. Kojima, H. Sakakibara and T. Hirayama. 2016. Comprehensive quantification and genome survey reveal the presence of novel phytohormone action modes in red seaweeds. J. Appl. Phycol. 28: 2539–2548.Google Scholar

  • Miyazaki, S., H. Toyoshima, M. Natsume, M. Nakajima and H. Kawaide. 2014. Blue-light irradiation up-regulates the ent-kaurene synthase gene and affects the avoidance response of protonemal growth in Physcomitrella patens. Planta 240: 117–124.Google Scholar

  • Miyazaki, S., M. Nakajima, M. and H. Kawaide. 2015. Hormonal diterpenoids derived from ent-kaurenoic acid are involved in the blue-light avoidance response of Physcomitrella patens. Plant Signal. Behave. 10: e989046.Google Scholar

  • Monroe-Augustus, M., B.K. Zolman and B. Bartel. 2003. IBR5, a dual-specificity phosphatase-like protein modulating auxin and abscisic acid responsiveness in Arabidopsis. Plant Cell 15: 2979–2991.Google Scholar

  • Müller, M. and S. Munné-Bosch. 2011. Rapid and sensitive hormonal profiling of complex plant samples by liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Plant Methods 7: 37.Google Scholar

  • Nakamura, Y., N. Sasaki, M. Kobayashi, N. Ojima, M. Yasuike, Y. Shigenobu, M. Satomi, Y. Fukuma, K. Shiwaku, A. Tsujimoto, T. Kobayashi, I. Nakayama, F. Ito, K. Nakajima, M. Sano, T. Wada, S. Kuhara, K. Inouye, T. Gojobori and K. Ikeo. 2013. The first symbiont-free genome sequence of marine red alga, Susabi-nori (Pyropia yezoensis). PLoS One 8: e57122.Google Scholar

  • Nambara, E. and A. Marion-Poll. 2005. Abscisic acid biosynthesis and catabolism. Ann. Rev. Plant Biol. 56: 165–185.Google Scholar

  • Nishimura, C., Y. Ohashi, S. Sato, T. Kato, S. Tabata and C. Ueguchi. 2004. Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16: 1365–1377.Google Scholar

  • Okada, K., J. Ueda, M.K. Komaki, C.J. Bell and Y. Shimura. 1991. Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3: 677–684.CrossrefGoogle Scholar

  • Ostrowski, M. and A. Jakubowska. 2014. UDP-glycosyltransferases of plant hormones. Adv. Cell Biol. 4: 43–60.Google Scholar

  • Patten, C.L. and B.R. Glick. 2002. Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl. Environ. Microbiol. 68: 3785–3801.Google Scholar

  • Pichersky, E. and J. Gershenzon. 2002. The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr. Opin. Plant Biol. 5: 237–243.Google Scholar

  • Ponce De León, I., E.A. Schmelz, C. Gaggero, A. Castro, A. Álvarez and M. Montesano. 2012. Physcomitrella patens activates reinforcement of the cell wall, programmed cell death and accumulation of evolutionary conserved defense signals, such as salicylic acid and 12-oxo-phytodienoic acid, but not jasmonic acid, upon Botrytis cinerea infection. Mol. Plant Pathol. 13: 960–974.Google Scholar

  • Press, C.M., M. Wilson, S. Tuzun and J.W. Kloepper. 1997. Salicylic acid produced by Serratia marcescens 90-166 is not the primary determinant of induced systemic resistance in cucumber or tobacco. Mol. Plant Microbe In. 6: 761–768.Google Scholar

  • Prinsen, E., A. Costacurta, K. Michiels, J. Vanderleyden and H. Van Onckelen. 1993. Azospirillum brasilense indole–3–acetic acid biosynthesis: evidence for a non-tryptophan dependent pathway. Mol. Plant-Microb. Interact. 6: 609–615.Google Scholar

  • Rikiishi, K., T. Matsuura, Y. Ikeda and M. Maekawa. 2015. Light inhibition of shoot regeneration is regulated by endogenous abscisic acid level in calli derived from immature barley embryos. PLoS One 10: e0145242.Google Scholar

  • Sakakibara, H. 2006. Cytokinins: activity, biosynthesis, and translocation. Ann. Rev. Plant Biol. 57: 431–449.Google Scholar

  • Schäfer, M., C. Brütting, I.T. Baldwin and M. Kallenbach. 2016. High-throughput quantification of more than 100 primary- and secondary-metabolites, and phytohormones by a single solid-phase extraction based sample preparation with analysis by UHPLC-HESI-MS/MS. Plant Methods 12: 30.Google Scholar

  • Scott, I. M., G.C. Martin, R. Horgan and J.K. Heald. 1982. Mass spectrometric measurement of zeatin glycoside levels in Vinca rosea L. crown gall tissue. Planta 154: 273–276.Google Scholar

  • Seo, M., Y. Jikumaru and Y. Kamiya. 2011. Profiling of hormones and related metabolites in seed dormancy and germination studies. In: (A.R. Kermode Ed.) Seed dormancy methods and protocols. Methods in Molecular Biology 773, Springer NewYork Dordrecht Heidelberg London. pp. 99–111.Google Scholar

  • Singh, R.P. and C.R. Reddy. 2014. Seaweed-microbial interactions: key functions of seaweed-associated bacteria. FEMS Microbiol Ecol. 88: 213–230.Google Scholar

  • Singh, R.P., A.J. Bijo, R.S. Baghel, C.R. Reddy and B. Jha. 2011a. Role of bacterial isolates in enhancing the bud induction in the industrially important red alga Gracilaria dura. FEMS Microbiol. Ecol. 76: 381–392.Google Scholar

  • Singh, R.P., V.A. Mantri, C.R.K. Reddy and B. Jha. 2011b. Isolation of seaweed-associated bacteria and their morhpogenesis-inducing capability in axenic culture of the green alga Ulva fasciata. Aquat. Biol. 12: 13–21.Google Scholar

  • Spoerner, M., T. Wichard, T. Bachhuber, J. Stratmann and W. Oertel. 2012. Growth and thallus morphogenesis of Ulva mutabilis (Chlorophyta) depends on a combination of two bacterial species excreting regulatory factors. J. Phycol. 48: 1433–1447.Google Scholar

  • Steinborner, S. and J. Henion. 1999. Liquid-liquid extraction in the 96-well plate format with SRM LC/MS quantitative determination of methotrexate and its major metabolite in human plasma. Anal. Chem. 71: 2340–2345.Google Scholar

  • Stiller, J.W., J. Perry, L.A. Rymarquis, M. Accerbi, P.J. Green, S. Prochnik, E. Lindquist, C.X. Chan, C. Yarish, S. Lin, Y. Zhuang, N.A. Blouin and S.H. Brawley. 2012. Major developmental regulators and their expression in two closely related species of Porphyra (Rhodophyta). J. Phycol. 48: 883–896.Google Scholar

  • Stout, J.S. and A.R. DaCunha. 1985. Simplified moving-belt interface for liquid chromatography/mass spectrometry. Anal. Chem. 57: 1783–1786.Google Scholar

  • Stumpe, M., C. Göbel, B. Faltin, A.K. Beike, B. Hause, K. Himmelsbach, J. Bode, R. Kramell, C. Wasternack, W. Frank, R. Reski and I. Feussner. 2010. The moss Physcomitrella patens contains cyclopentenones but no jasmonates: mutations in allene oxide cyclase lead to reduced fertility and altered sporophyte morphology. New Phytol. 188: 740–749.Google Scholar

  • Suzuki, T., T. Matsuura, N. Kawakami and K. Noda. 2000. Accumulation and leakage of abscisic acid during embryo development and seed dormancy in wheat. Plant Growth Regul. 30: 253–260.Google Scholar

  • Takagi, H., Y. Ishiga, S. Watanabe, T. Konishi, M. Egusa, N. Akiyoshi, T. Matsuura, I.C. Mori, T. Hirayama, H. Kaminaka, H. Shimada and A. Sakamoto. 2016. Allantoin, a stress-related purine metabolite, can activate jasmonate signaling in a MYC2-regulated and abscisic acid-dependent manner. J. Exp Bot. 67: 2519–2532.Google Scholar

  • Takezawa, D., K. Komatsu and Y. Sakata. 2011. ABA in bryophytes: how a universal growth regulator in life become a plant hormone? J. Plant Res. 124: 437–453.Google Scholar

  • Tate, J. and G. Ward. 2004. Interference in immunoassay. Clin. Biochem. Rev. 25: 105–120.Google Scholar

  • Tivendale, N.D., J.J. Ross and J.D. Cohen. 2014. The shifting paradigms of auxin biosyntheis. Trends Plant Sci. 19: 44–51.Google Scholar

  • To, J.P. and J.J. Kieber. 2008. Cytokinin signaling: two-components and more. Trends Plant Sci. 13: 85–92.Google Scholar

  • Tokuda, M., Y. Jikumaru, K. Matsukura, Y. Takebayashi, S. Kumashiro, M. Matsumura and Y. Kamiya. 2013. Phytohormones related to host plant manipulation by a fall-inducing leafhopper. PLoS One 8: e62350.Google Scholar

  • Tsukahara, K., H. Sawada, Y. Kohno, T. Matsuura, I.C. Mori, T. Terao, M. Ioki and M. Tamaoki. 2015. Ozone-induced rice grain yield loss is triggered via a change in panicle morphology that is controlled by AERRANT PANICLE ORGANIZATION 1 gene. PLoS One 10: e0123308.Google Scholar

  • Turnaev, I., K.V. Gunbin and D.A. Afonnikov. 2015. Plant auxin biosynthesis did not originate in carophytes. Trends Plant Sci. 20: 463–465.Google Scholar

  • Turowski, M., N. Yamakawa, J. Meller, K. Kimata, T. Ikegami, K. Hosoya, N. Tanaka and E.R. Thornton. 2003. Deuterium isotoep effects on hydrophobic interactions: the importance of dispersion interactions in the hydrophobic phase. J. Am. Chem. Soc. 125: 13836–13849.Google Scholar

  • Umehara, M., A. Hanada, S. Yoshida, K. Akiyama, T. Arite, N. Takeda-Kamiya, H. Magome, Y. Kamiya, K. Shirasu, K. Yoneyama, J. Kyozuka and S. Yamaguchi. 2008. Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195–200.Google Scholar

  • Ulmasov, T., G. Hagen and T.J. Guilfoyle. 1997. ARF1, a transcription factor that binds to auxin response elements. Science 276: 1865–1868.Google Scholar

  • Van Meulebroek, L., J. Vanden Bussche, K. Steppe and L. Vanhaecke. 2012. Ultra-high performance liquid chromatography coupled to high resolution Orbitrap mass spectrometry for metabolomic profiling of the endogenous phytohormonal status of the tomato plant. J. Chromatogr. A 1260: 67–80.Google Scholar

  • Van Meulebroek, L. J. Vanden Bussche, N., De Clercq and L. Vanhaecke. 2014. Metabolomics approach to unravel the regulating role of phytohormones towards carotenoid metabolism in tomato fruit. Anal. Bioanal. Chem. 406: 2613–2626.Google Scholar

  • Vestal, M.L. 1984. High-performance liquid chromatography-mass spectrometry. Science 226: 275–281.Google Scholar

  • Wang, C., Y. Liu, S.-S. Li and G.-Z. Han. 2014a. Origin of plant auxin biosynthesis in charophyte algae. Trends Plant Sci. 19: 741–743.Google Scholar

  • Wang, X., P. Zhao, X. Liu, J. Chen, J. Xu, H. Chen and X. Yan. 2014b. Quantitative profiling method for phytohormones and betaines in algae by liquid chromatography electrospray ionization tandem mass spectrometry. Biomed. Chromatogr. 28: 275–280.Google Scholar

  • Wang, C., S.-S. Li and G.-Z. Han. 2016. Plant auxin biosynthesis did not originate in charophytes. Front. Plant Sci. 7: 158.Google Scholar

  • Watanabe, T. and N. Kondo. 1976. Ethylene evolution in marine algae and a proteinaceous inhibitor of ethylene biosysnthesis from red alga. Plant Cell Physiol. 17: 1159–1166.Google Scholar

  • Weiler, E.W. 1982. An enzyme-immunoassay for cis-(+) abscisic acid. Physiol. Plant 54: 510–514.Google Scholar

  • Westfall, C.S., A.M. Muehler and J.M. Jez. 2013. Enzyme action in the regulation of plant hormone responses. J. Biol. Chem. 288: 19304–19311.Google Scholar

  • Wichard, T. 2015. Exploring bacteria-induced growth and morphogenesis in the green macroalga order Ulvales (Chlorophyta). Front. Plant Sci. 6: 86.Google Scholar

  • Wieling, J. 2002. LC–MS–MS experiences with internal standards. Chromatographa 55: S107–S113.CrossrefGoogle Scholar

  • Wu, Y., D. Zhang, J.Y. Chu, P. Boyle, Y. Wang, I.D. Brindle, V. De Luca and C. Despres. 2012. The Arabidopsis NPR1 proteinis a receptor for the plant defense hormone salicylic acid. Cell Rep. 1: 639–647.Google Scholar

  • Yamamoto, Y., J. Ohshika, T. Takahashi, K. Ishizaki, T. Kohchi, M. Matusuura and K. Takahashi. 2015. Functional analysis of allene oxide cyclase, MpAOC, in the liverwort Marchantia polymorpha. Phytochemistry. 116: 48–56.Google Scholar

  • Yokoya, N.S., W.A. Stirk, J. van Staden, O. Novák, V. Turečková, A. Pěnčík and M. Strnad. 2010. Endogenous cytokinins, auxins, and abscisic acid in red algae from Brazil. J. Phycol. 46: 1198–1205.Google Scholar

  • Yoshimoto, K., Y. Jikumaru, Y. Kamiya, M. Kusano, C. Consonni, R. Panstruga, Y. Ohsumo and K. Shirasu. 2009. Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell 21: 2914–2927.Google Scholar

  • Yue, J., X. Hu and J. Huang. 2014. Origin of plant auxin biosynthesis. Trends Plant Sci. 19: 764–770.Google Scholar

  • Zhao, Y. 2014. Auxin biosynthesis. Abaridopsis Book. 12: e0173.Google Scholar

About the article

Izumi C. Mori

Izumi C. Mori obtained his PhD from Nagoya University in 1998. He established the LC–MS equipment in the Institute of Plant Science and Resources, Okayama University, several years ago. His research focuses on phytohormone signaling of stomata.

Yoko Ikeda

Yoko Ikeda got her PhD at Kyoto University in 2007. Her main research interests are plant epigenetic mechanisms in reproduction and environmental response. She also began to work on plant hormone research at Okayama University in 2013.

Takakazu Matsuura

Takakazu Matsuura started to work as technical staff in Institute of Plant Science and Resources, Okayama University, at 1991. He is experienced in LC-MS analysis and research on seed dormancy in wheat.

Takashi Hirayama

Takashi Hirayama obtained his PhD from Kyoto University in 1992. He has been studying plant hormone signaling mechanisms by mainly applying molecular genetic approaches. His current interest is focused on understanding of how plants integrate various physiological and environmental information and choose the best response.

Koji Mikami

Koji Mikami obtained his PhD from Hokkaido University in 1990. His research currently focuses on regulatory machineries of life-cycle, development and abiotic stress responses in seaweeds to understand how multicellular marine organisms acclimate to environmental stress and acquire stress tolerance for supporting their correct developmental programs under strict stress conditions.


Received: 2016-06-20

Accepted: 2017-02-23

Published Online: 2017-03-30

Published in Print: 2017-04-24


Citation Information: Botanica Marina, Volume 60, Issue 2, Pages 153–170, ISSN (Online) 1437-4323, ISSN (Print) 0006-8055, DOI: https://doi.org/10.1515/bot-2016-0056.

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