title: Planteose as a storage carbohydrate required for early stage of germination of Orobanche minor and its metabolism as a possible target for selective control.
abstract: Root parasitic weeds in Orobanchaceae cause serious damage to worldwide agriculture. Germination of the parasites requires host-derived germination stimulants, such as strigolactones, as indicators of host roots within reach of the parasite's radicles. This unique germination process was focused on to identify metabolic pathways required for germination, and to design a selective control strategy. A metabolomic analysis of germinating seeds of clover broomrape, Orobanche minor, was conducted to identify its distinctive metabolites. Consequently, a galactosyl-sucrose trisaccharide, planteose (α-d-galactopyranosyl-(1→6)-β-d-fructofuranosyl-(2→1)-α-d-glucopyranoside), was identified as a metabolite that decreased promptly after reception of the germination stimulant. To investigate the importance of planteose metabolism, the effects of several glycosidase inhibitors were examined, and nojirimycin bisulfite (NJ) was found to alter the sugar metabolism and to selectively inhibit the germination of O. minor. Planteose consumption was similar in NJ-treated seeds and non-treated germinating seeds; however, NJ-treated seeds showed lower consumption of sucrose, a possible intermediate of planteose metabolism, resulting in significantly less glucose and fructose. This inhibitory effect was recovered by adding glucose. These results suggest that planteose is a storage carbohydrate required for early stage of germination of O. minor, and NJ inhibits germination by blocking the supply of essential glucose from planteose and sucrose. Additionally, NJ selectively inhibited radicle elongation of germinated seeds of Orobanchaceae plants (Striga hermonthica and Phtheirospermum japonicum). Thus, NJ will be a promising tool to develop specific herbicides to the parasites, especially broomrapes, and to improve our understanding of the molecular mechanisms of this unique germination.
authors.affiliation: Department of Biotechnology, Graduate School of Engineering, Osaka University, 2-1 Yamadaoka, Suita, Osaka 565-0871, Japan.
authors.forename: Takatoshi
authors.initials: T
authors.lastname: Wakabayashi
authors.affiliation: Department of Biotechnology, Graduate School of Engineering, Osaka University, 2-1 Yamadaoka, Suita, Osaka 565-0871, Japan.
authors.forename: Benesh
authors.initials: B
authors.lastname: Joseph
authors.affiliation: Department of Biotechnology, Graduate School of Engineering, Osaka University, 2-1 Yamadaoka, Suita, Osaka 565-0871, Japan.
authors.forename: Shuhei
authors.initials: S
authors.lastname: Yasumoto
authors.affiliation: Department of Applied Biological Science, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-8510, Japan.
authors.forename: Tomoyoshi
authors.initials: T
authors.lastname: Akashi
authors.affiliation: Department of Applied Biological Science, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-8510, Japan.
authors.forename: Toshio
authors.initials: T
authors.lastname: Aoki
authors.affiliation: Applied Environmental Biology, Graduate School of Pharmaceutical Science, Osaka University, 1-6 Yamadaoka, Suita, Osaka 565-0871, Japan.
authors.forename: Kazuo
authors.initials: K
authors.lastname: Harada
authors.affiliation: International Institute of Tropical Agriculture Kano, PMB3112, Sabo Bakin Zuwo Road, Kano, Nigeria.
authors.forename: Satoru
authors.initials: S
authors.lastname: Muranaka
authors.affiliation: Department of Biotechnology, Graduate School of Engineering, Osaka University, 2-1 Yamadaoka, Suita, Osaka 565-0871, Japan.
authors.forename: Takeshi
authors.initials: T
authors.lastname: Bamba
authors.affiliation: Department of Biotechnology, Graduate School of Engineering, Osaka University, 2-1 Yamadaoka, Suita, Osaka 565-0871, Japan.
authors.forename: Eiichiro
authors.initials: E
authors.lastname: Fukusaki
authors.affiliation: Weed Science Center, Utsunomiya University, 350 Mine-machi, Utsunomiya 321-8505, Japan.
authors.forename: Yasutomo
authors.initials: Y
authors.lastname: Takeuchi
authors.affiliation: Weed Science Center, Utsunomiya University, 350 Mine-machi, Utsunomiya 321-8505, Japan.
authors.forename: Koichi
authors.initials: K
authors.lastname: Yoneyama
authors.affiliation: Department of Biotechnology, Graduate School of Engineering, Osaka University, 2-1 Yamadaoka, Suita, Osaka 565-0871, Japan.
authors.forename: Toshiya
authors.initials: T
authors.lastname: Muranaka
authors.affiliation: Department of Biofunctional Chemistry, Graduate School of Agricultural Science, Kobe University, 1-1 Rokkodai, Nada-ku, Kobe 657-8501, Japan.
authors.forename: Yukihiro
authors.initials: Y
authors.lastname: Sugimoto
authors.affiliation: Department of Biotechnology, Graduate School of Engineering, Osaka University, 2-1 Yamadaoka, Suita, Osaka 565-0871, Japan Department of Applied Life Sciences, Graduate School of Life and Environmental Sciences, Osaka Prefecture University, 1-1 Gakuen-cho, Naka-ku, Sakai, Osaka 599-8531, Japan okazawa@plant.osakafu-u.ac.jp.
authors.forename: Atsushi
authors.initials: A
authors.lastname: Okazawa
mesh_terms: D050260:Carbohydrate Metabolism; D002241:Carbohydrates / Q000302:isolation & purification; D008401:Gas Chromatography-Mass Spectrometry; D018525:Germination; D055432:Metabolomics; D031670:Orobanchaceae / Q000469:parasitology*; D031672:Orobanche / Q000254:growth & development / Q000378:metabolism*; D010935:Plant Diseases / Q000469:parasitology*; D018517:Plant Roots / Q000469:parasitology; D057685:Plant Weeds; D012639:Seeds / Q000254:growth & development / Q000378:metabolism
chemical_list: D002241:Carbohydrates
keywords: Broomrapes; metabolomics; nojirimycin; planteose; root parasitic weeds; seed germination; selective control; sugar metabolism.
references.citation: J Exp Bot. 2012 May;63(9):3367-77
references.pmid: 22140246
references.citation: Plant Physiol. 2003 Mar;131(3):1347-59
references.pmid: 12644684
references.citation: Pest Manag Sci. 2009 May;65(5):478-91
references.pmid: 19222046
references.citation: Arch Biochem Biophys. 1983 Mar;221(2):593-7
references.pmid: 6404222
references.citation: Am J Bot. 2006 Jul;93(7):1039-51
references.pmid: 21642169
references.citation: Pest Manag Sci. 2009 May;65(5):566-71
references.pmid: 19266492
references.citation: Plant Physiol. 2005 Oct;139(2):920-34
references.pmid: 16183851
references.citation: Annu Rev Plant Biol. 2006;57:675-709
references.pmid: 16669778
references.citation: J Exp Bot. 2008;59(6):1187-200
references.pmid: 18375607
references.citation: Plant Physiol. 2011 Feb;155(2):932-43
references.pmid: 21098673
references.citation: Trends Plant Sci. 2010 Apr;15(4):227-35
references.pmid: 20153240
references.citation: Mol Plant. 2013 Jan;6(1):18-28
references.pmid: 23155045
references.citation: Pest Manag Sci. 2009 May;65(5):603-14
references.pmid: 19301299
references.citation: J Biochem. 2004 Oct;136(4):525-31
references.pmid: 15625323
references.citation: J Biol Chem. 1982 Dec 10;257(23):14155-61
references.pmid: 6216253
references.citation: J Biosci Bioeng. 2009 Aug;108(2):151-9
references.pmid: 19619864
references.citation: Arch Biochem Biophys. 1959 Dec;85:471-3
references.pmid: 13824854
references.citation: Carbohydr Res. 1986 Nov 1;155:119-29
references.pmid: 3024831
references.citation: Pest Manag Sci. 2009 May;65(5):471-7
references.pmid: 19115242
references.citation: Curr Opin Biotechnol. 2002 Apr;13(2):156-60
references.pmid: 11950569
references.citation: Mol Plant Microbe Interact. 2012 Mar;25(3):402-11
references.pmid: 22088196
references.citation: Pest Manag Sci. 2009 May;65(5):467-70
references.pmid: 19222028
references.citation: J Agric Food Chem. 1999 Apr;47(4):1705-10
references.pmid: 10564042
references.citation: Pest Manag Sci. 2009 May;65(5):453-9
references.pmid: 19206075
references.citation: J Plant Physiol. 2007 Aug;164(8):1093-6
references.pmid: 17258350
references.citation: J Antibiot (Tokyo). 1985 Jan;38(1):116-8
references.pmid: 3918980
references.citation: Biochimie. 2014 Jun;101:39-49
references.pmid: 24374160
references.citation: Curr Opin Plant Biol. 2004 Jun;7(3):235-46
references.pmid: 15134743
references.citation: Biochemistry. 1985 Jul 2;24(14):3530-9
references.pmid: 3929833
references.citation: Physiol Plant. 2004 Feb;120(2):328-337
references.pmid: 15032868
references.citation: Nature. 2005 Jun 9;435(7043):824-7
references.pmid: 15944706
references.citation: Plant Physiol. 1995 Mar;107(3):895-904
references.pmid: 7716246
references.citation: Arch Biochem Biophys. 1959 May;82(1):188-94
references.pmid: 13650653
references.citation: Biosci Biotechnol Biochem. 2005 Jul;69(7):1353-64
references.pmid: 16041142
references.citation: Nature. 2008 Sep 11;455(7210):195-200
references.pmid: 18690207
references.citation: Nature. 2008 Sep 11;455(7210):189-94
references.pmid: 18690209
references.citation: Mol Plant Pathol. 2011 Sep;12(7):638-52
references.pmid: 21726369