Accessible Requires Authentication Published by De Gruyter March 30, 2017

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

Izumi C. Mori, Yoko Ikeda, Takakazu Matsuura, Takashi Hirayama and Koji Mikami
From the journal Botanica Marina

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.

Acknowledgments

The authors are grateful for support received from the Joint Research Program at the Institute of Plant Science and Resources, Okayama University, and the Japan Advanced Plant Science Network. This work was supported in part by a KAKENHI grant-in-aid for the support of scientific research (no. 15H0453905) and the Ohara Foundation for Agricultural Research.

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. Search in 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. Search in 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. Search in 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. Search in 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. Search in 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. Search in 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. Search in 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. Search in Google Scholar

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

Wieling, J. 2002. LC–MS–MS experiences with internal standards. Chromatographa 55: S107–S113. Search in Google 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. Search in 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. Search in 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. Search in 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. Search in Google Scholar

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

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

Received: 2016-6-20
Accepted: 2017-2-23
Published Online: 2017-3-30
Published in Print: 2017-4-24

©2017 Walter de Gruyter GmbH, Berlin/Boston