Comprehensive quantification and genome survey reveal the presence of novel phytohormone action modes in red seaweeds

Journal of Applied Phycology

Volumn 28, Issue 4, 2016, Pages 2539-2548

  Mikami, Koji ^a   Mori, Izumi C ^b   Matsuura, Takakazu ^b   Ikeda, Yoko ^b   Kojima, Mikiko ^c   Sakakibara, Hitoshi ^c   Hirayama, Takashi ^b  

^a HOKKAIDO UNIVERSITY   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

^c Elements Chemistry Laboratory   (Japan)

Author keywords

Bangia fuscopurpurea; Comparative genomics; Liquid chromatography tandemmass spectrometry; Phytohormone; Pyropia yezoensis; Quantitative profiling

Indexed keywords

EID: 85032076703     PISSN: 09218971     EISSN: 15735176     Source Type: Journal    
DOI: 10.1007/s10811-015-0759-2     Document Type: Article

References (58)

1. Ashen JB, Cohen JD, Goff LJ (1999) GC-SIM-MS detection and quantification of free indole-3-acetic acid in bacterial galls on the marine alga Prionitis lanceolata (Rhodophyta). J Phycol 35:493-500
2. Basu S, Sun H, Brian L, Quatrano RL, Muday GK (2002) Early embryo development in Fucus distichus is auxin sensitive. Plant Physiol 130:292-302
3. Craigie JS (2011) Seaweed extract stimuli in plant science and agriculture. J Appl Phycol 23:371-393
4. Chan CX, Blouin NA, Zhuang Y, Zäuner S, Prochnik SE, Lindquist E, Lin S, Benning C, Lohr M, Yarish C, Gantt E, Grossman AR, Lu S, Müller K, Stiller J, Brawley SH, Bhattacharya D (2012a) Porphyra (Bangiophyceae) transcriptomes provide insights into red algal development and metabolism. J Phycol 48:1328-1342
5. Chan CX, Zäuner S, Wheeler GL, Grossman AR, Prochnik SE, Blouin NA, Zhuang Y, Benning C, Berg GM, Yarish C, Eriksen RL, Klein AS, Lin S, Levine I, Brawley SH, Bhattacharya D (2012b) Analysis of Porphyra membrane transporters demonstrates gene transfer among photosynthetic eukaryotes and numerous sodium-coupled transport systems. Plant Physiol 158:2001-2012
6. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651-679
7. Davidson FF (1950) The effects of auxin on the growth of marine algae. Am J Bot 37:502-510
8. De Smet I, Voß U, Lau S, Wilson M, Shao N, Timme RE, Swarup R, Kerr I, Hodgman C, Bock R, Bennett M, Jürgens G, Beeckman T (2011) Unraveling the evolution of auxin signaling. Plant Physiol 155:209-221
9. Dorrell RG, Smith AG (2011) Do red and green make brown?: perspectives on plastid acquisitions within chromalveolates. Eukaryot Cell 10:856-868
10. Endo A, Nelson KM, Thoms K, Abrams SR, Nambara E, Sato Y (2014) Functional characterization of xanthoxin dehydrogenase in rice. J Plant Physiol 171:1231-1240
11. Esteban R, Martínez B, Fernández-Marín B, Becerril JM, García-Plazaola JI (2009) Carotenoid composition in Rhodophyta: insights into xanthophyll regulation in Corallina elongata. Eur J Phycol 44:221-230
12. Gupta V, Kumar M, Brahmbhatt H, Reddy CR, Seth A, Jha B (2011) Simultaneous determination of different endogenetic plant growth regulators in common green seaweeds using dispersive liquid-liquid microextraction method. Plant Physiol Biochem 49:1259-1263
13. Hirata R, Takahashi M, Saga N, Mikami K (2011) Transient gene expression system established in Porphyra yezoensis is widely applicable in Bangiophycean algae. Mar Biotechnol 13:1038-1047
14. Izumi Y, Okazawa A, Bamba T, Kobayashi A, Fukusaki E (2009) Development of a method for comprehensive and quantitative analysis of plant hormones by highly sensitive nanoflow liquid chromatography-electrospray ionization-ion trapmass spectrometry. Anal Chim Acta 648:215-225
15. Jacobs WP, Falkenstein K, Hamilton RH (1985) Nature and amount of auxin in algae. IAA from extracts of Caulerpa paspaloides (Siphonales). Plant Physiol 78:844-848
16. Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182-193
17. Johri MM (2008) Hormonal regulation in green plant lineage families. Physiol Mol Biol Plants 14:23-38
18. Kanno Y, Jikumaru Y, Hanada A, Nambara E, Abrams SR, Kamiya Y, Seo M (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
19. Khan W, Rayirath UP, Subramanian S, Jithesh MN, Rayorath P, Mark Hodges D, Critchley AT, Craigie JS, Norrie J, Prithiviraj B (2009) Seaweed extracts as biostimulants of plant growth and development. J Plant Growth Regul 28:386-399
20. Kiseleva AA, Tarachovskaya ER, Shishova MF (2012) Biosynthesis of phytohormones in algae. Russ J Plant Physiol 59:595-610
21. Kitade Y, Fukuda S, Nakajima M, Watanabe T, Saga N (2002) Isolation of a cDNA encoding a homologue of actin from Porphyra yezoensis (Rhodophyta). J Appl Phycol 14:135-141
22. Klingler JP, Batelli G, Zhu JK (2010) ABA receptors: the START of a new paradigm in phytohormone signalling. J Exp Bot 61:3199-3210
23. Kojima M, Kamada-Nobusada T, Komatsu H, Takei K, Kuroha T, Mizutani M, Ashikari M, Ueguchi-Tanaka M, Matsuoka M, Suzuki K, Sakakibara H (2009) Highly sensitive and highthroughput 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
24. Kuroha T, Tokunaga H, Kojima M, Ueda N, Ishida T, Nagawa S, Fukuda H, Sugimoto K, Sakakibara H (2009) Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. Plant Cell 21:3152-3169
25. Lau S, Shao N, Bock R, Jürgens G, De Smet I (2009) Auxin signaling in algal lineages: fact or myth? Trends Plant Sci 14:182-188
26. Le Bail A, Billoud B, Kowalczyk N, Kowalczyk M, Gicquel M, Le Panse S, Stewart S, Scornet D, Cock JM, Ljung K, Charrier B (2010) Auxin metabolism and function in the multicellular brown alga Ectocarpus siliculosus. Plant Physiol 153:128-144
27. Le Corguillé G, Pearson G, Valente M, Viegas C, Gschloessl B, Corre E, Bailly X, Peters AF, Jubin C, Vacherie B, Cock JM, Leblanc C (2009) Plastid genomes of two brown algae, Ectocarpus siliculosus and Fucus vesiculosus: further insights on the evolution of red-algal derived plastids. BMC Evol Biol 9:253. doi:10.1186/1471-2148-9-253
28. Lin R, Stekoll MS (2007) Effects of plant growth substances on the conchocelis phase of Alaskan Porphyra (Bangiales, Rhodophyta) species in conjunction with environmental variables. J Phycol 43: 1094-1103
29. Mikami K, Hosokawa M (2013) Biosynthetic pathway and health benefits of fucoxanthin, an algae-specific xanthophyll in brown seaweeds. Int J Mol Sci 14:13763-13781
30. Mikami K, Kanesaki Y, Suzuki I, Murata N (2002) The histidine kinase Hik33 perceives osmotic stress and cold stress in Synechocystis sp. PCC 6803. Mol Microbiol 46:905-915
31. Mikami K, Murata N (2003) Membrane fluidity and the perception of environmental signals in cyanobacteria and plants. Prog Lipid Res 42:527-543
32. Nakamura Y, Sasaki N, Kobayashi M, Ojima N, Yasuike M, Shigenobu Y, Satomi M, Fukuma Y, Shiwaku K, Tsujimoto A, Kobayashi T, Nakayama I, Ito F, Nakajima K, Sano M, Wada T, Kuhara S, Inouye K, Gojobori T, Ikeo K (2013) The first symbiont-free genome sequence of marine red alga, Susabi-nori (Pyropia yezoensis). PLoS ONE 8:e57122
33. Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165-185
34. Nozaki H, Maruyama S, Matsuzaki M, Nakada T, Kato S, Misawa K (2009) Phylogenetic positions of Glaucophyta, green plants (Archaeplastida) and Haptophyta (Chromalveolata) as deduced from slowly evolving nuclear genes. Mol Phylogenet Evol 53: 872-880
35. Puthiyaveetil S, Allen JF (2009) Chloroplast two-component systems: evolution of the link between photosynthesis and gene expression. Proc R Soc B 276:2133-2145
36. Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431-449
37. Sanderson KJ, Jameson PE, Zabkiewicz JA (1987) Auxin in a seaweed extract: identification and quantification of indole-3-aceric acid by gas chromatography-mass spectrometry. J Plant Physiol 129:363-367
38. Stiller JW, Perry J, Rymarquis LA, Accerbi M, Green PJ, Prochnik S, Lindquist E, Chan CX, Yarish C, Lin S, Zhuang Y, Blouin NA, Brawley SH (2012) Major developmental regulators and their expression in two closely related species of Porphyra (Rhodophyta). J Phycol 48:883-896
39. Schubert N, García-Mendoza E, Pacheco-Ruiz I (2006) Carotenoid composition of marine red algae. J Phycol 42:1208-1216
40. van Staden J, Drewes FE (1991) The biological activity of cytokinin derivatives in the soybean callus bioassay. Plant Growth Regul 10: 109-115
41. Stirk WA, Novák O, Strnad M, van Staden J (2003) Cytokinins in macralgae. Plant Growth Regul 40:13-24
42. Stirk WA, Arthur GD, Lourens AF, Novák O, Strnad M, van Staden J (2004) Changes in cytokinin and auxin concentrations in seaweed concentrates when stored at an elevated temperature. J Appl Phycol 16:31-39
43. Stirk WA, Novák O, Hradecká V, Pĕnčík A, Rolčík J, Strnad M, van Staden J (2009) Endogenous cytokinins, auxins and abscisic acid in Ulva fasciata (Chlorophyta) and Dictyota humifusa (Phaeophyta): towards understanding their biosynthesis and homeostasis. Eur J Phycol 44:231-240
44. Stirk WA, Tarkowská D, Turečová V, Strnad M, van Staden J (2014) Abscisic acid, gibberellins and brassinosteroids in Kelpak, a commercial seaweed extract made from Ecklonia maxima. J Appl Phycol 26:561-567
45. Takezawa D, Komatsu K, Sakata Y (2011) ABA in bryophytes: how a universal growth regulator in life became a plant hormone? J Plant Res 124:437-453
46. Tanaka K (2011) Chloroplast transcription machinery of red algae: conservation of four types of transcriptional regulators in non-green chloroplasts. In: Mikami K (ed) Porphyra yezoensis: frontiers in physiological and molecular biological research. Nova Science Publishers, New York, pp 39-60
47. Tay SAB, MacLeod JK, Palni LMS, Letham DS (1985) Detection of cytokinins in a seaweed extract. Phytochem 23:2611-2614
48. To JP, Kieber JJ (2008) Cytokinin signaling: two-components and more. Trends Plant Sci 13:85-92
49. Tokuda M, Jikumaru Y, Matsukura K, Takebayashi Y, Kumashiro S, Matsumura M, Kamiya Y (2013) Phytohormones related to host plant manipulation by a gall-inducing leafhopper. PLoS ONE 8: e62350
50. Vanstraelen M, Benková E (2012) Hormonal interactions in the regulation of plant development. Annu Rev Cell Dev Biol 28:463-487
51. Wang C, Liu Y, Li SS, Han GZ (2015) Insights into the origin and evolution of plant hormone signaling machinery. Plant Physiol. doi: 10.1104/pp.114.247403
52. Wang X, Zhao P, Liu X, Chen J, Xu J, Chen H, Yan X (2014) Quantitative profiling method for phytohormones and betaines in algae by liquid chromatography electrospray ionization tandem mass spectrometry. Biomed Chromatogr 28:275-280
53. Weyers JDB, Paterson NW (2001) Plant hormones and the control of physiological processes. New Phytol 152:375-407
54. Yang LE, Huang XQ, Hang Y, Deng YY, Lu QQ, Lu S (2014) The P450-type carotene hydroxylase PuCHY1 from Porphyra suggests the evolution of carotenoid metabolism in red algae. J Integr Plant Biol 56:902-915
55. Yokoya NS, Handro W (1996) Effects of auxins and cytokinins on tissue culture of Grateloupia dichotoma (Gigartinales, Rhodophyta). Hydrobiologia 326 327:393-400
56. Yokoya NS, Stirk WA, van Staden J, Novák O, Turečková V, Pěnčík A, Strnad M (2010) Endogenous cytokinins, auxins, and abscisic acid in red algae from Brazil. J Phycol 46:1198-1205
57. Yue J, Hu X, Huang J (2014) Origin of plant auxin biosynthesis. Trends Plant Sci 19:764-770
58. Zhang W, Yamane H, Chapman DJ (1993) The phytohormone profile of the red alga Porphyra perforata. Bot Mar 36:257-266