Planteose as a storage carbohydrate required for early stage of germination of Orobanche minor and its metabolism as a possible target for selective control.

Takatoshi Wakabayashi,Atsushi Okazawa,Satoru Muranaka,Shuhei Yasumoto,Kazuo Harada,Takeshi Bamba,Yukihiro Sugimoto,Toshiya Muranaka,Toshio Aoki,Tomoyoshi Akashi,Yasutomo Takeuchi,Benesh Joseph,Koichi Yoneyama,Eiichiro Fukusaki

doi:10.1093/jxb/erv116

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.

Highlights

Root parasitic weeds in Orobanchaceae are among the most destructive agricultural weeds
These results suggest that planteose is a Abbreviations: CWI, cell wall invertase; CS, castanospermine; DAG, days after GR24 treatment; DGJ, 1-deoxygalactonojirimycin; DIA, 1,4-dideoxy-1,4-iminoarabinitol; DNJ, 1-deoxynojirimycin; ELSD, evaporative light scattering detector; GC-TOF-MS, Gas chromatography combined with time-of-flight mass spectrometry; HPLC, high-performance liquid chromatography; INV, invertase; mode(s) of action (MOA), mode of action; NJ, nojirimycin bisulfite; PC, principal component; PCA, principal component analysis; PVPP, polyvinylpolypyrrolidone; RFO raffinose family oligosaccharides; SAI, soluble acid invertase; SNI, soluble neutral invertase; SUS, sucrose synthase; UDP, uridine diphosphate; UPLC, ultra-performance liquid chromatography
The results show that planteose metabolism is involved in the early stage of germination

Summary

Introduction

Root parasitic weeds in Orobanchaceae are among the most destructive agricultural weeds Within this family, Orobanche spp., Phelipanche spp., and Striga spp. cause devastating damage to agricultural crops worldwide. Striga is estimated to cause losses of at least US$7 billion per year (Elzein and Kroschel, 2003; Aly, 2007; Heide-Jørgense, 2008; Parker, 2009) These root parasitic weeds have evolved many parasitic adaptations; they have unique life cycles that are tightly coupled with the ecological behaviours of the host plants. The seeds of root parasitic weeds in Orobanchaceae require host-derived germination stimulants, such as strigolactones, to germinate (López-Ráez et al, 2009; Yoneyama et al, 2009). Root parasitic weeds have often caused irreversible damage by the time the infestation is detected from the above ground emergence of their shoots

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Conclusion