Abstract
Proanthocyanidins (PAs) are the end products of the flavonoid biosynthetic pathway in many seeds, but their biological function is rarely unknown during seed germination. In the present study, we observed that PAs pretreatment accelerated cucumber seeds germination with maximum efficiency at 0.15% by measuring germination percentage and radical length. Using inhibitors of abscisic acid (ABA), gibberellins (GA) and alternative oxidase (AOX) and H2O2 scavenger pretreatment and gene expression analysis, we found that the accelerated effect of 0.15% PAs on seed germination was due to the decreased ABA biogenesis and enhanced GA production. ROS are induced by PAs pretreatment. Then, the enhanced ROS contributed to GA and ethylene accumulation and ABA decrease in seeds. Moreover, the improvement of GA was involved in the further induction of antioxidant enzymes activities. Therefore, our findings uncover a novel role of PAs in seed germination and clarify the relationships between ROS, ABA, GA and ethylene during seed germination.
Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Bahin E, Bailly C, Sotta B, Kranner I, Corbineau F, Leymarie J (2011) Crosstalk between reactive oxygen species and hormonal signalling pathways regulates grain dormancy in barley. Plant Cell Environ 34:980–993
Barba-Espén G, Diaz-vivancos P, Job D, Belghazi M, Job C, Hernández JA (2011) Understanding the role of H2O2 during pea seed germination: a combined proteomic and hormone profiling approach. Plant Cell Environ 34:1907–1919
Bethke PC, Jones RL (2001) Cell death of barley aleurone protoplasts is mediated by reactive oxygen species. Plant J 25:19–29
Bethke PC, Libourel IG, Jones RL (2006) Nitric oxide reduces seed dormancy in Arabidopsis. J Exp Bot 57:517–526
Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066
Chen ML, Huang YQ, Liu JQ, Yuan BF, Feng YQ (2011) Highly sensitive profiling assay of acidic plant hormones using a novel mass probe by capillary electrophoresis-time of flight-mass spectrometry. J Chromatogr 879:938–944
Debeaujon I, Nesi N, Perez P, Devic M, Grandjean O, Caboche M, Lepiniec L (2003) Proanthocyanidin-accumulating cells in Arabidopsis testa: regulation of differentiation and role in seed development. Plant Cell 15:2514–2531
Dixon RA, Xie DY, Sharma SB (2005) Proanthocyanidins–a final frontier in flavonoid research? New Phytol 165:9–28
Dong CJ, Li L, Shang QM, Liu XY, Zhang ZG (2014) Endogenous salicylic acid accumulation is required for chilling tolerance in cucumber (Cucumis sativus L.) seedlings. Planta 240:687–700
Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523
Geraldes-Laakso S, Arrabaça J (1997) Respiration and heat production by soybean hypocotyl and cotyledon mitochondria. Plant Physiol Biochem 35:897–903
Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y, McCourt P (2000) Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. Plant Cell 12:1117–1126
Han SY, Kitahata N, Sekimata K, Saito T, Kobayashi M, Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K, Yoshida S, Asami T (2004) A novel inhibitor of 9-cis-epoxycarotenoid dioxygenase in abscisic acid biosynthesis in higher plants. Plant Physiol 135:1574–1582
Hilhorst HW (1995) A critical update on seed dormancy. I. primary dormancy. Seed Sci Res 5:61–73
Ishibashi Y, Koda Y, Zheng SH, Yuasa T, Iwaya-Inoue M (2013) Regulation of soybean seed germination through ethylene production in response to reactive oxygen species. Ann Bot 111:95–102
Jia LG, Sheng ZW, Xu WF, Li YX, Liu YG, Xia YJ, Zhang JH (2012) Modulation of anti-oxidation ability by proanthocyanidins during germination of Arabidopsis thaliana seeds. Mol Plant 5:472–481
Jie S, Kentian Z (1993) Organic substance metabolism during seed germination of Pinus bungeana. J Forest Res 4:70–75
Julliard J, Maldiney R, Sotta B, Miginiac E, Kerhoas L, Einhorn J (1994) HPLC-ELISA and MS as complementary techniques to study plant hormone metabolites. Analusis 22:483–489
Kitahata N, Saito S, Miyazawa Y, Umezawa T, Shimada Y, Min YK, Mizutani M, Hirai N, Shinozaki K, Yoshida S (2005) Chemical regulation of abscisic acid catabolism in plants by cytochrome P450 inhibitors. Bioorg Med Chem 13:4491–4498
Kucera B, Cohn MA, Leubner-Metzger G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Sci Res 15:281–307
Lee YP, Baek KH, Lee HS, Kwak SS, Bang JW, Kwon SY (2010) Tobacco seeds simultaneously over-expressing Cu/Zn-superoxide dismutase and ascorbate peroxidase display enhanced seed longevity and germination rates under stress conditions. J Exp Bot 61:2499–2506
Lei T, Feng H, Sun X, Dai QL, Zhang F, Liang HG, Lin HH (2010) The alternative pathway in cucumber seedlings under low temperature stress was enhanced by salicylic acid. Plant Growth Regul 60:35–42
Lepiniec L, Debeaujon I, Routaboul JM, Baudry A, Pourcel L, Nesi N, Caboche M (2006) Genetics and biochemistry of seed flavonoids. Annu Rev Plant Biol 57:405–430
Liu SJ, Wei HM, Li ZY, Li S, Yan H, He Y, Tian ZH (2015) Effects of graphene on germination and seedling morphology in rice. J Nanosci Nanotechnol 15:2695–2701
Liu Y, Ye N, Liu R, Chen M, Zhang J (2010) H2O2 mediates the regulation of ABA catabolism and GA biosynthesis in Arabidopsis seed dormancy and germination. J Exp Bot 61:2979–2990
Matilla A, Matilla-Vazquez M (2008) Involvement of ethylene in seed physiology. Plant Sci 175:87–97
Nassiri-Asl M, Hosseinzadeh H (2009) Review of the pharmacological effects of Vitis vinifera (grape) and its bioactive compounds. Phytother Res 23:1197–204
Nicolás C, Nicolás G, Rodréguez D (1996) Antagonistic effects of abscisic acid and gibberellic acid on the breaking of dormancy of Fagus sylvatica seeds. Physiol Plantarum 96:244–250
Ogawa Ki, Iwabuchi M (2001) A mechanism for promoting the germination of Zinnia elegans seeds by hydrogen peroxide. Plant Cell Physiol 42:286–291
Oracz K, El-Maarouf-Bouteau H, Kranner I, Bogatek R, Corbineau F, Bailly C (2009) The mechanisms involved in seed dormancy alleviation by hydrogen cyanide unravel the role of reactive oxygen species as key factors of cellular signaling during germination. Plant Physiol 150:494–505
Peng X, Ma J, Chao J, Sun Z, Chang RCC, Tse I, Li ET, Chen F, Wang M (2010) Beneficial effects of cinnamon proanthocyanidins on the formation of specific advanced glycation endproducts and methylglyoxal-induced impairment on glucose consumption. J Agric Food Chem 58:6692–6696
Porter LJ, Hrstich LN, Chan BG (1985) The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25:223–230
Proteggente AR, Saija A, De Pasquale A, Rice-Evans CA (2003) The compositional characterisation and antioxidant activity of fresh juices from sicilian sweet orange (Citrus sinensis L. Osbeck) varieties. Free Radical Res 37:681–687
Routaboul JM, Kerhoas L, Debeaujon I, Pourcel L, Caboche M, Einhorn J, Lepiniec L (2006) Flavonoid diversity and biosynthesis in seed of Arabidopsis thaliana. Planta 224:96–107
Spencer JP, Kuhnle GG, Williams RJ, Rice-Evans C (2003) Intracellular metabolism and bioactivity of quercetin and its in vivo metabolites. Biochem J 372:173–181
Stewart RR, Bewley JD (1980) Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiol 65:245–248
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66
Vranová E, Inzé D, Van Breusegem F (2002) Signal transduction during oxidative stress. J Exp Bot 53:1227–1236
Wang J, Ho L, Zhao W, Ono K, Rosensweig C, Chen L, Humala N, Teplow DB, Pasinetti GM (2008) Grape-derived polyphenolics prevent Aβ oligomerization and attenuate cognitive deterioration in a mouse model of Alzheimer’s disease. J Neurosci 28:6388–6392
Wang SD, Zhu F, Yuan S, Yang H, Xu F, Shang J, Xu MY, Jia SD, Zhang ZW, Wang JH, Xi DH, Lin HH (2011) The roles of ascorbic acid and glutathione in symptom alleviation to SA-deficient plants infected with RNA viruses. Planta 234:171–181
Xi DM, Liu WS, Yang GD, Wu CA, Zheng CC (2010) Seed-specific overexpression of antioxidant genes in Arabidopsis enhances oxidative stress tolerance during germination and early seedling growth. Plant Biotechnol J 8:796–806
Xie DY, Sharma SB, Paiva NL, Ferreira D, Dixon RA (2003) Role of anthocyanidin reductase, encoded by BANYULS in plant flavonoid biosynthesis. Science 299:396–399
Xu F, Zhang DW, Zhu F, Tang H, Lv X, Cheng J, Xie HF, Lin HH (2012) A novel role for cyanide in the control of cucumber (Cucumis sativus L.) seedlings response to environmental stress. Plant Cell Environ 35:1983–1997
Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514
Zhang HJ, Zhang N, Yang RC, Wang L, Sun QQ, Li DB, Cao YY, Weeda S, Zhao B, Ren S (2014) Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA4 interaction in cucumber (Cucumis sativus L.). J Pineal Res 57:269–279
Zhang KM, Yu HJ, Shi K, Zhou YH, Yu JQ, Xia XJ (2010) Photoprotective roles of anthocyanins in Begonia semperflorens. Plant Sci 179:202–208
Zhou L, Jang JC, Jones TL, Sheen J (1998) Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucoseinsensitive mutant. Pro Natl Acad Sci USA 95:10294–10299
Zhu F, Zhang P, Meng YF, Xu F, Zhang DW, Cheng J, Lin HH, Xi DH (2013) Alpha-momorcharin, a RIP produced by bitter melon, enhances defense response in tobacco plants against diverse plant viruses and shows antifungal activity in vitro. Planta 237:77–88
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Zhu, Lj., Deng, Xg., Zou, Lj. et al. Proanthocyanidins accelerate the germination of cucumber (Cucumis sativus L.) seeds. J. Plant Biol. 59, 143–151 (2016). https://doi.org/10.1007/s12374-016-0510-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12374-016-0510-9


