Biochemical characterization of allene oxide synthases from the liverwort Marchantia polymorpha and green microalgae Klebsormidium flaccidum provides insight into the evolutionary divergence of the plant CYP74 family

Planta

Volumn 242, Issue 5, 2015, Pages 1175-1186

  Koeduka, Takao ^a   Ishizaki, Kimitsune ^b   Mwenda, Cynthia Mugo ^c   Hori, Koichi ^d   Sasaki Sekimoto, Yuko ^d   Ohta, Hiroyuki ^d   Kohchi, Takayuki ^e   Matsui, Kenji ^a,c  

^a YAMAGUCHI UNIVERSITY   (Japan)

^b KOBE UNIVERSITY   (Japan)

^c YAMAGUCHI UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^e KYOTO UNIVERSITY   (Japan)

Author keywords

Allene oxide synthase; C8 volatiles; CYP74; Hydroperoxide lyase; Plant evolution

Indexed keywords

CYTOCHROME P450; DIVINYL ETHER SYNTHASE; HYDROPEROXIDE ISOMERASE; ISOMERASE; VEGETABLE PROTEIN;

ENZYMOLOGY; GENETICS; MARCHANTIA; METABOLISM; MICROALGA; MOLECULAR EVOLUTION;

CYTOCHROME P-450 ENZYME SYSTEM; EVOLUTION, MOLECULAR; INTRAMOLECULAR OXIDOREDUCTASES; MARCHANTIA; MICROALGAE; PLANT PROTEINS;

EID: 84941940034     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-015-2355-8     Document Type: Article

References (44)

1. Aleem AM, Jankun J, Dignam JD, Walther M, Kühn H, Svergun DI, Skrzypczak-Jankun E (2008) Human platelet 12-lipoxygenase, new findings about its activity, membrane binding and low-resolution structure. J Mol Biol 376:193–209
2. Arimura G, Matsui K, Takabayashi J (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant Cell Physiol 50:911–923
3. Buse T, Ruess L, Filser J (2013) New trophic biomarkers for Collembola reared on algal diets. Pedobiologia 56:153–159
4. Fauconnier ML, Marlier M (1996) An efficient procedure for the production of fatty acid hydroperoxides from hydrolyzed flax seed oil and soybean lipoxygenase. Biotechnol Tech 10:839–844
5. Galliard T, Phillips DR (1971) Lipoxygenase from potato tubers. Partial purification and properties of an enzyme that specifically oxygenates the 9-position of linoleic acid. Biochem J 124:431–438
6. Gogolev YV, Gorina SS, Gogoleva NE, Toporkova YY, Chechetkin IR, Grechkin AN (2012) Green leaf divinyl ether synthase: gene detection, molecular cloning and identification of a unique CYP74B subfamily member. Biochim Biophys Acta 1821:287–294
7. Holopainen JK, Blande JD (2012) Molecular plant volatile communication. Adv Exp Med Biol 739:17–31
8. Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N, Seo M, Sato S, Yamada T, Mori H, Tajima N, Moriyama T, Ikeuchi M, Watanabe M, Wada H, Kobayashi K, Saito M, Masuda T, Sasaki-Sekimoto Y, Mashiguchi K, Awai K, Shimojima M, Masuda S, Iwai M, Nobusawa T, Narise T, Kondo S, Saito H, Sato R, Murakawa M, Ihara Y, Oshima-Yamada Y, Ohtaka K, Satoh M, Sonobe K, Ishii M, Ohtani R, Kanamori-Sato M, Honoki R, Miyazaki D, Mochizuki H, Umetsu J, Higashi K, Shibata D, Kamiya Y, Sato N, Nakamura Y, Tabata S, Ida S, Kurokawa K, Ohta H (2014) Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat Commun 5:3978
9. Hughes RK, Belfield EJ, Ashton R, Fairhurst SA, Göbel C, Stumpe M, Feussner I, Casey R (2006) Allene oxide synthase from Arabidopsis thaliana (CYP74A1) exhibits dual specificity that is regulated by monomer-micelle association. FEBS Lett 580:4188–4194
10. Ishizaki K, Chiyoda S, Yamato KT, Kohchi T (2008) Agrobacterium-mediated transformation of the haploid liverwort Marchantia polymorpha L., an emerging model for plant biology. Plant Cell Physiol 49:1084–1091
11. Kajikawa M, Matsui K, Ochiai M, Tanaka Y, Kita Y, Ishimoto M, Kohzu Y, Shoji S, Yamato KT, Ohyama K, Fukuzawa H, Kohchi T (2008) Production of arachidonic and eicosapentaenoic acids in plants using bryophyte fatty acid Δ6-desaturase, Δ6-elongase, and Δ5-desaturase genes. Biosci Biotechnol Biochem 72:435–444
12. Kanamoto H, Takemura M, Ohyama K (2012) Cloning and expression of three lipoxygenase genes from liverwort, Marchantia polymorpha L., in Escherichia coli. Phytochemistry 77:70–78
13. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780
14. Kihara H, Tanaka M, Yamato KT, Horibata A, Yamada A, Kita S, Ishizaki K, Kajikawa M, Fukuzawa H, Kohchi T, Akakabe Y, Matsui K (2014) Arachidonic acid-dependent carbon-eight volatile synthesis from wounded liverwort (Marchantia polymorpha). Phytochemistry 107:42–49
15. Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2007) Volatile 1-octen-3-ol induces a defensive response in Arabidopsis thaliana. J Gen Plant Pathol 73:35–37
16. Koeduka T, Stumpe M, Matsui K, Kajiwara T, Feussner I (2003) Kinetics of barley FA hydroperoxide lyase are modulated by salts and detergents. Lipids 38:1167–1172
17. Koeduka T, Kajiwara T, Matsui K (2007) Cloning of lipoxygenase genes from a cyanobacterium, Nostoc punctiforme, and its expression in Eschelichia coli. Curr Microbiol 54:315–319
18. Koeduka T, Louie GV, Orlova I, Kish CM, Ibdah M, Wilkerson CG, Bowman ME, Baiga TJ, Noel JP, Dudareva N, Pichersky E (2008) The multiple phenylpropene synthases in both Clarkia breweri and Petunia hybrida represent two distinct protein lineages. Plant J 54:362–374
19. Kongrit D, Jisaka M, Iwanaga C, Yokomichi H, Katsube T, Nishimura K, Nagaya T, Yokota K (2007) Molecular cloning and functional expression of soybean allene oxide synthases. Biosci Biotechnol Biochem 71:491–498
20. Lang I, Feussner I (2007) Oxylipin formation in Nostoc punctiforme (PCC73102). Phytochemistry 68:347–357
21. Laudert D, Pfannschmidt U, Lottspeich F, Holländer-Czytko H, Weiler EW (1996) Cloning, molecular and functional characterization of Arabidopsis thaliana allene oxide synthase (CYP 74), the first enzyme of the octadecanoid pathway to jasmonates. Plant Mol Biol 31:323–335
22. Lee DS, Nioche P, Hamberg M, Raman CS (2008) Structural insights into the evolutionary paths of oxylipin biosynthetic enzymes. Nature 455:363–368
23. Matsui K, Ujita C, Fujimoto S, Wilkinson J, Hiatt B, Knauf V, Kajiwara T, Feussner I (2000a) Fatty acid 9- and 13-hydroperoxide lyases from cucumber. FEBS Lett 481:183–188
24. Matsui K, Miyahara C, Wilkinson J, Hiatt B, Knauf V, Kajiwara T (2000b) Fatty acid hydroperoxide lyase in tomato fruits: cloning and properties of a recombinant enzyme expressed in Escherichia coli. Biosci Biotechnol Biochem 64:1189–1196
25. Mwenda CM, Matsuki A, Nishimura K, Koeduka T, Matsui K (2015) Spatial expression of the Arabidopsis hydroperoxide lyase gene is controlled differently form that of the allene oxide synthase gene. J Plant Interact 10:1–10
26. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542
27. Scalschi L, Sanmartín M, Camañes G, Troncho P, Sánchez-Serrano JJ, García-Agustín P, Vicedo B (2015) Silencing of OPR3 in tomato reveals the role of OPDA in callose deposition during the activation of defense responses against Botrytis cinerea. Plant J 81:304–315
28. Scholz J, Brodhun F, Hornung E, Herrfurth C, Stumpe M, Beike AK, Faltin B, Frank W, Reski R, Feussner I (2012) Biosynthesis of allene oxides in Physcomitrella patens. BMC Plant Biol 12:228
29. Shinmen Y, Katoh K, Shimizu S, Jareonkitmongkol S, Yamada H (1991) Production of arachidonic acid and eicosapentaenoic acids by Marchantia polymorpha in cell culture. Phytochemistry 30:3255–3260
30. Splivallo R, Novero M, Bertea CM, Bossi S, Bonfante P (2007) Truffle volatiles inhibit growth and induce an oxidative burst in Arabidopsis thaliana. New Phytol 175:417–424
31. Stumpe M, Kandzia R, Göbel C, Rosahl S, Feussner I (2001) A pathogen-inducible divinyl ether synthase (CYP74D) from elicitor-treated potato suspension cells. FEBS Lett 507:371–376
32. Stumpe M, Bode J, Göbel C, Wichard T, Schaaf A, Frank W, Frank M, Reski R, Pohnert G, Feussner I (2006) Biosynthesis of C9-aldehydes in the moss Physcomitrella patens. Biochim Biophys Acta 1761:301–312
33. Stumpe M, Göbel C, Faltin B, Beike AK, Hause B, Himmelsbach K, Bode J, Kramell R, Wasternack C, Frank W, Reski R, Feussner I (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
34. Sugimoto K, Matsui K, Iijima Y, Akakabe Y, Muramoto S, Ozawa R, Uefune M, Sasaki R, Alamgir KM, Akitake S, Nobuke T, Galis I, Aoki K, Shibata D, Takabayashi J (2014) Intake and transformation to a glycoside of (Z)-3-hexenol from infested neighbors reveals a mode of plant odor reception and defense. Proc Natl Acad Sci USA 111:7144–7149
35. Taki N, Sasaki-Sekimoto Y, Obayashi T, Kikuta A, Kobayashi K, Ainai T, Yagi K, Sakurai N, Suzuki H, Masuda T, Takamiya K, Shibata D, Kobayashi Y, Ohta H (2005) 12-oxo-phytodienoic acid triggers expression of a distinct set of genes and plays a role in wound-induced gene expression in Arabidopsis. Plant Physiol 139:1268–1283
36. Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577
37. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
38. Toporkova YY, Gogolev YV, Mukhtarova LS, Grechkin AN (2008) Determinants governing the CYP74 catalysis: conversion of allene oxide synthase into hydroperoxide lyase by site-directed mutagenesis. FEBS Lett 582:3423–3428
39. Toporkova YY, Ermilova VS, Gorina SS, Mukhtarova LS, Osipova EV, Gogolev YV, Grechkin AN (2013) Structure-function relationship in the CYP74 family: conversion of divinyl ether synthases into allene oxide synthases by site-directed mutagenesis. FEBS Lett 587:2552–2558
40. Wu J, Hettenhausen C, Meldau S, Baldwin IT (2007) Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19:1096–1122
41. Yamamoto Y, Ohshika J, Takahashi T, Ishizaki K, Kohchi T, Matusuura H, Takahashi K (2015) Functional analysis of allene oxide cyclase, MpAOC, in the liverwort Marchantia polymorpha. Phytochemistry 116:48–56
42. Yamato KT, Ishizaki K, Fujisawa M, Okada S, Nakayama S, Fujishita M, Bando H, Yodoya K, Hayashi K, Bando T, Hasumi A, Nishio T, Sakata R, Yamamoto M, Yamaki A, Kajikawa M, Yamano T, Nishide T, Choi SH, Shimizu-Ueda Y, Hanajiri T, Sakaida M, Kohno K, Takenaka M, Yamaoka S, Kuriyama C, Kohzu Y, Nishida H, Brennicke A, Shin-i T, Kohara Y, Kohchi T, Fukuzawa H, Ohyama K (2007) Gene organization of the liverwort Y chromosome reveals distinct sex chromosome evolution in a haploid system. Proc Natl Acad Sci USA 104:6472–6477
43. Yanagi K, Sugimoto K, Matsui K (2011) Oxylipin-specific cytochrome P450s (CYP74s) in Lotus japonicus: their implications in response to mechanical wounding and nodule formation. J Plant Interact 6:255–264
44. Zhu Z, Qian F, Yang R, Chen J, Luo Q, Chen H, Yan X (2015) A lipoxygenase from red alga Pyropia haitanensis, a unique enzyme catalyzing the free radical reactions of polyunsaturated fatty acids with triple ethylenic bonds. PLoS ONE 10:e0117351