Abstract
The defense characteristics of allelopathic rice accession PI312777 and its counterpart Lemont induced by exogenous salicylic acid (SA) to suppress troublesome weed barnyardgrass (BYG) were investigated using the methods of suppression subtractive hybridization (SSH) and real-time fluorescence quantitative PCR (qRT-PCR). The results showed that exogenous SA could induce the allelopathic effect of rice on BYG and this inducible defense was SA dose-respondent and treatment time-dependent. PI312777 exhibited higher inhibitory effect than Lemont on BYG after treated with different concentrations of SA. The activities of cell protective enzymes including SOD, POD and CAT in the BYG plants co-cultured with PI312777 treated by SA were highly depressed compared with the control (co-cultured with rice without SA-treatment). Similar but lower depression on these enzymes except for CAT was also observed in the BYG plants when co-cultured with Lemont treated by SA. It is therefore suggested that allelopathic rice should be more sensitive than non-allelopathic rice to exogenous SA. Seventeen genes induced by SA were obtained by SSH analysis from PI312777. These genes encode receptor-kinase proteins, ubiquitin carrier proteins, proteins related to phenylpropanoid metabolism, antioxidant related proteins and some growth-mediating proteins. The differential expressions of these genes were validated in part by qRT-PCR in the two rice accessions. Our work elucidated that allelopathic rice possesses an active chemical defense and auto-detoxifying enzyme system such as the up-regulated enzymes involved in de novo biosynthesis of phenolic allelochemicals and the glutathione-S-transferase (GST) associated with xenobiotic detoxification.
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Abbreviations
- SSH:
-
Suppression subtractive hybridization
- qRT-PCR:
-
Real-time fluorescent quantitative polymerase chain reaction
- SA:
-
Salicylic acid
- PAL:
-
Phenylalanine ammonia-lyase
- GST:
-
Glutathione-S-transferase
- CCR:
-
Cinnamoyl-CoA reductase
- POD:
-
Peroxidase
- SOD:
-
Superoxide dismutase
- CAT:
-
Catalase
References
Baerson SR, Moreiras AS, Bonjoch NP, Schulz M, Kagan IA, Agarwal AK et al (2005) Detoxification and transcriptome response in Arabidopsis seedlings exposed to the allelochemical benzoxazolin-2(3H)-one (BOA). J Biol Chem 280:21867–21881. doi:10.1074/jbc.M500694200
Balke NE, Hodges TK (1979) Comparison of reduction in adenosine triphosphate content, plasma membrane-associated adenosine triphosphase activity and potassium absorption in oat root by diethylstilbestrol. Plant Physiol 63:53–56
Belz RG (2007) Allelopathy in crop/weed interactions: an update. Pest Manag Sci 63:308–326. doi:10.1002/ps.1320
Belz RG, Hurle K (2004) A novel laboratory screening bioassay for crop seedling allelopathy. J Chem Ecol 30:175–198. doi:10.1023/B:JOEC.0000013190.72062.3d
Bi HH, Zeng RS, Su LM, An M, Luo SM (2007) Rice allelopathy induced by methyl jasmonate and methyl salicylate. J Chem Ecol 33:1089–1103. doi:10.1007/s10886-007-9286-1
Bob BB, Wilhelm G, Russell LJ (eds) (2000) Biochemistry & molecular biology of plants. American Society of Plant Physiologists, Maryland
Bryant JP, Chapin FSIII, Reichardt PB, Clausen TP (1987) Response of winter chemical defense in Alaska paper birch and green alder to manipulation of plant carbon/nutrient balance. Oecologia 72:510–514. doi:10.1007/BF00378975
Dhindsa RS, Dhindsa PP, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–96. doi:10.1093/jxb/32.1.93
Diatchenko L, Lau YFC, Campbell AP, Chenchik A, Moqadam F, Huang B et al (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025–6030. doi:10.1073/pnas.93.12.6025
Dilday RH, Yan WG, Moldenhauer KAK, Gravois KA (1998) Allelopathic activity in rice for controlling major aquatic weeds. In: Olofsdotter M (ed) Allelopathy in rice. International Rice Research Institute, Manila, pp 7–26
Dilday RH, Mattice JD, Moldenhauer KA (2000) An overview of rice allelopathy in the USA. In: Kim KU, Shin DH (eds) Rice allelopathy. Kyungpook National University, Taegu, pp 15–26
Dunham CW (1958) Use of methylene blue to evaluate rooting of cuttings. Proc Am Soc Hortic Sci 72:450–453
Ebana K, Yan WG, Dilday RH, Namai H, Okuno K (2001) Analysis of QTL associated with the allelopathic effect of rice using water-soluble extracts. Breed Sci 51:47–51. doi:10.1270/jsbbs.51.47
Fajer ED, Bowers MD, Bazzaz FA (1992) The effect of nutrients and enriched CO2 environments on production of carbon-based allelochemicals in plantago: a test of the carbon/nutrient balance. Am Nat 140:702–723. doi:10.1086/285436
Gong HB, Jiao YX, Hu WW, Pua EC (2005) Expression of glutathione-S-transferase and its role in plant growth and development in vivo and shoot morphogenesis in vitro. Plant Mol Biol 57:53–66. doi:10.1007/s11103-004-4516-1
He HQ, Dong ZH, Liang YY, Lin SW, Lin WX (2002) New advance of research on allelopathy in rice (Oryza sativa L.). Res Agric Mod 23:140–143 (in Chinese)
He HQ, Shen LH, Xiong J, Jia XL, Lin WX, Wu H (2004) Conditional genetic effect of allelopathy in rice (Oryza sativa L.) under different environmental conditions. Plant Growth Regul 44:211–218. doi:10.1007/s10725-004-5107-5
Jensen LB, Courtois B, Shin LS, Li ZK, Olofsdotter M, Mauleon RP (2001) Locating genes controlling allelopathic effects against barnyardgrass in upland rice. Agron J 93:21–26
Kenneth J, Thomas D (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−△△Ct method. Methods 25:402–408. doi:10.1006/meth.2001.1262
Kim SY, Madrid AV, Park ST, Yang SJ, Olofsdotter M (2005) Evaluation of rice allelopathy in hydroponics. Weed Res 45:74–79. doi:10.1111/j.1365-3180.2004.00438.x
Kovacik J, Klejdus B, Backor M, Repca M (2007) Phenylalanine ammonia-lyase activity and phenolic compounds accumulation in nitrogen-deficient Matricaria chamomilla leaf rosettes. Plant Sci 172:393–399. doi:10.1016/j.plantsci.2006.10.001
Lee SB, Seo KI, Koo JH, Hur HS, Shin JC (2005) QTLs and molecular markers associated with rice allelopathy. In: Haper JDI, An M, Kent JH (eds) Proceedings of the fourth world congress on allelopathy “Establishing the scientific base”, Charles Sturt University, Wagga Wagga, NSW, Australia, pp 505–507
Lin WX, Kim KU, Shin DH (2000) Allelopathic potential in rice (Oryza sativa L.) and its modes of action on barnyardgrass (Echinochloa crusgalli L.). Allelopath J 7:215–224
Lin WX, He HQ, Guo YC, Liang YY, Chen FY (2001) Rice allelopathy and its physiobiochemical characteristics. Chin J Appl Ecol 12:871–875 (in Chinese)
Lin WX, He HQ, Kim KU (2003) The performance of allelopathic heterosis in rice (Oryza sativa L.). Allelopath J 2:179–188
Ling ZP, Hu YL (1997) Stress resistance of plants induced via the salicylic acid-mediated signal transduction pathway. Acta Bot Sin 39:l85–188 (in Chinese)
Ohtake Y, Takahashi T, Komeda Y (2000) Salicylic acid induces the expression of a number of receptor-like kinase genes in Arabidopsis thaliana. Plant Cell Physiol 41:1038–1044. doi:10.1093/pcp/pcd028
Olofsdotter M (1998) Allelopathy in rice. In: Olofsdotter M (ed) Allelopathy in rice. International Rice Research Institute, Manila, pp 1–5
Pfaff MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002–2007
Putnam AR, Tang CS (1986) Allelopathy: state of science. In: Putnam AR, Tang CS (eds) The science of allelopathy. Wiley, New York, pp 43–56
Rasbin I (1992) Salicylate, a new plant hormone. Plant Physiol 99:799–803
Razal RA, Ellis S, Santokh S, Lewis NG, Towers GHN (1996) Nitrogen recycling in phenylpropanoid metabolism. Phytochemistry 41:31–35. doi:10.1016/0031-9422(95)00628-1
Schuler MA (1996) Plant cytochrome P450 monooxygenases. Crit Rev Plant Sci 15:235–284. doi:10.1080/713608134
Shen LH, Lin WX (2007) Effects of phosphorus levels on allelopathic potential of rice co-cultured with barnyardgrass. Allelopath J 19:23–32
Shen LH, Xiong J, Lin WX (2008) Rice allelopathy research in china. In: Zeng RS, Mallik AU, Luo SM (eds) Allelopathy in sustainable agriculture and forestry. Springer, New York, pp 215–233
Song BQ, Xiong J, Fang CX, Qiu L, Lin RY, Liang YY et al (2008) Allelopathic enhancement and differential gene expression in rice under low nitrogen treatment. J Chem Ecol 34:688–695. doi:10.1007/s10886-008-9455-x
Takao M, Akazawa T, Fukuchi S (1970) Enzymic mechanism of starch breakdown in germinating rice seeds.III.α-amylase isozymes. Plant Physiol 46:650–654
Tsai CJ, Harding SA, Tschaplinski TJ, Lindroth RL, Yuan YN (2006) Genome-wide analysis of the structural genes regulating defense phenylpropanoid metabolism in Populus. New Phytol 172:47–62. doi:10.1111/j.1469-8137.2006.01798.x
Weidenhame JD (1996) Distinguishing resource competition and chemical interference: overcoming the method-ological impasse. Agron J 88:866–875
Wen PF, Chen JY, Kong WF, Pan QH, Wan SB, Huang WD (2005) Salicylic acid induced the expression of phenylalanine ammonia-lyase gene in grape berry. Plant Sci 169:928–934. doi:10.1016/j.plantsci.2005.06.011
Xiang CB, Miao ZH, Lam E (1996) Coordinated activation of as-1-type elements and a tobacco glutathione S-transferase gene by auxins, salicylic acid, methyl-jasmonate and hydrogen peroxide. Plant Mol Biol 32:415–426. doi:10.1007/BF00019093
Xiong J, Lin WX, Zhou JJ, Wu MH, Chen XX, He HQ (2005) Studies on biointerference between barnyardgrass and rice accessions at different nitrogen regimes. In: Harper JDI, An M, Wu H, Kent JH (eds) Proceedings fourth world congress on allelopathy, Charles Sturt University, Wagga Wagga, NSW, Australia, pp 501–504
Xiong J, Jia XL, Deng JY, Jiang BY, He HB, Lin WX (2007a) Analysis of epistatic effect and QTL interactions with environment for allelopathy in rice (Oryza sativa L.). Allelopath J 20:259–268
Xiong J, Wang HB, Fang CX, Qiu L, Wu WX, He HB et al (2007b) The differential expression of the genes of the key enzymes involved in phenolic compound metabolism in rice (Oryza sativa L.) under different nitrogen supply. J Plant Physiol Mol Biol 33:387–394 (in Chinese)
Xu ZH, Yu LQ, Zhao M (2003) Rice allelopathy to barnyardgrass. Chin J Appl Ecol 14:737–740 (in Chinese)
Zeng DL, Qian Q, Teng S, Dong G, Fujimoto H, Yasufumi K et al (2003) Genetic analyses on rice allelopathy. Chin Sci Bull 48:70–73
Acknowledgments
This work was supported by The National Natural Science Foundation of China (No.30471028) and Provincial Natural Science Foundation of Fujian, China (No.20020F012, K04038). The authors thank Dr. W.R. Wu for his critical reading of the manuscript.
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Fang, CX., Xiong, J., Qiu, L. et al. Analysis of gene expressions associated with increased allelopathy in rice (Oryza sativa L.) induced by exogenous salicylic acid. Plant Growth Regul 57, 163–172 (2009). https://doi.org/10.1007/s10725-008-9333-0
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DOI: https://doi.org/10.1007/s10725-008-9333-0