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Genomic analysis of allelopathic response to low nitrogen and barnyardgrass competition in rice (Oryza sativa L.)

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Abstract

To explore the molecular mechanism of allelopathic rice in response to low nitrogen (N) supply or accompanying weed stress, allelopathic rice PI 312777 and its counterpart Lemont were grown under low N supply or co-cultured with barnyardgrass [Echinochloa crus-galli (L.) Beauv.] in hydroponics. The suppression subtractive hybridization (SSH) technique was employed to isolate the up-regulated genes in the treated rice accession. The results indicated that the expression of the genes associated with N utilization was significantly up-regulated in allelopathic rice PI 312777, and the higher efficiency of N uptake and its utilization were also detected in PI 312777 than that in Lemont when the two rice accessions were exposed to low N supply. This result suggested that the allelopathic rice had higher ability to adapt to low N stress than its non-allelopathic counterpart. However, a different response was observed when the allelopathic rice was exposed to accompanying weed (barnyardgrass) co-cultured in full Hoagland solution (normal N supply). It showed that the expression of the genes associated with allelochemical synthesis and its detoxification were all up-regulated in the allelopathic rice when co-cultured with the target weed under normal N supply. The results suggested that the allelopathic rice should be a better competitor in the rice-weed co-culture system, which could be attributed to increasing de novo biosynthesis and detoxification of allelochemicals in rice, consequently resulting in enhanced allelopathic effect on the target and preventing the autotoxicity in this process. These findings suggested that the accompanying weed, barnyardgrass is not only the stressful factor, but also one of the triggers in activating allelopathy in rice. This implies that the allelopathic rice is sensible of the existing target in chemical communication.

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Abbreviations

AOC:

Allene oxide cyclase

4CL:

4-coumarate-CoA ligase

ER:

Endoplasmic reticulum

GDH:

Glutamate dehydrogenase

GST:

Glutathione S-transferase

JA:

Jasmonic acid

MT:

Metallothionein-like protein

MYB:

V-myb avian myeloblastosis viral oncogene homolog

N:

Nitrogen

NUE:

Nitrogen use efficiency

P450s:

Cytochrome P450 monooxygenase

PAL:

Phenylalanine ammonia-lyase

SSH:

Suppression subtractive hybridization

TRAP:

Translocon-associated protein complex

References

  • Anterola AM, Jeon JH, Davin LB, Lewis NG (2002) Transcriptional control of monolignol biosynthesis in Pinus taeda: factors affecting monolignol ratios and carbon allocation in phenylpropanoid metabolism. J Biol Chem 277:18272–18280

    Article  CAS  PubMed  Google Scholar 

  • Belz RG (2007) Allelopathy in crop/weed interactions—an update. Pest Manag Sci 63:308–326

    Article  CAS  PubMed  Google Scholar 

  • Belz RG, Hurle K (2004) A novel laboratory screening bioassay for crop seedling allelopathy. J Chem Ecol 30:175–198

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Bole-Feysot C, Perret E, Roustan P, Bouchard B, Kelly PA (2000) Analysis of prolactin-modulated gene expression profiles during the Nb2 cell cycle using differential screening techniques. Genome Biol 1: research0008.1–0008.15

    Google Scholar 

  • Chaopongpang S, Pornpattkul C, Pitaksutheepong J, Limpananont PC, Boonjawat J (1992) The role of lectin in association between rice and nitrogen-fixing bacteria. In: Mongkolsuk S, Lovett PS, Trempy JE (eds) Biotechnology and environmental science: molecular approaches. Plenum Press, New York, pp 81–88

    Chapter  Google Scholar 

  • Chen MJ, Ni M (2006) RFI2, a RING-domain zinc finger protein, negatively regulates CONSTANS expression and photoperiodic flowering. Plant J 46:823–833

    Article  CAS  PubMed  Google Scholar 

  • Dalisay RF, Kuc JA (1995) Persistence of induced resistance and enhanced peroxidase and chitinase activities in cucumber plants. Physiol Plant Pathol 47:315–327

    Article  CAS  Google Scholar 

  • Diatchenko L, Lau YFC, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD (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

    Article  CAS  PubMed  Google Scholar 

  • Duguin JL, Dinauer MC (1990) Library subtraction of in vitro cDNA libraries to identify differentially expressed genes in scrapie infection. Nucleic Acids Res 18:2789–2792

    Article  Google Scholar 

  • Edreva A (2005) Pathogenesis-related proteins: research progress in the last 15 years. Gen Appl Plant Physiol 31:105–124

    CAS  Google Scholar 

  • Einhellig FA (1999) An integrated view of allelochemicals amid multiple stresses. In: Inderjit, Dakshin KMM, Foy CL (eds) Principles and practices in plant ecology: allelochemical interactions. CRC Press, Boca Raton, pp 479–494

    Google Scholar 

  • Errebhi M, Rosen CJ, Lauer FI, Martin MW, Bamberg JB (1999) Evaluation of tuber-bearing Solanum species for nitrogen use efficiency and biomass partitioning. Am J Potato Res 76:143–151

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Fang CX, Wu XC, Zhang HL, Xiong J, Wu WX, Lin WX (2009a) UV-induced differential gene expression in rice cultivars analyzed by SSH. Plant Growth Regul 59:245–253

    Article  CAS  Google Scholar 

  • Fang CX, Xiong J, Qiu L, Wang HB, Song BQ, He HB, Lin RY, Lin WX (2009b) Analysis of gene expressions associated with increased allelopathy in rice (Oryza sativa L.) induced by exogenous salicylic acid. Plant Growth Regul 57:163–172

    Article  CAS  Google Scholar 

  • Grace JB, Tilman D (1990) Perspectives on plant competition. Academic Press, San Diego

    Google Scholar 

  • Gross GG, Zenk MH (1974) Isolation and properties of hydroxycinnamate: CoA ligase from lignifying tissue of Forsythia. Eur J Biochem 42:453–459

    Article  CAS  PubMed  Google Scholar 

  • Guterman A, Hajouj T, Gepstein S (2003) Senescence-associated mRNAs that may participate in signal transduction and protein trafficking. Physiol Plant 118:439–446

    Article  CAS  Google Scholar 

  • Hammerschmidt R, Nuckles EM, Kuc J (1982) Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Collectotrchum lagenarium. Physiol Mol Plant Pathol 20:73–82

    Article  CAS  Google Scholar 

  • Harper JL (1977) Population biology of plants. Academic Press, New York

    Google Scholar 

  • He HB (2009) Change in allelopathic potential of rice and its molecular mechanism in the responses to barnyardgrass stress. Dissertation, Fujian Agriculture and Forestry University, Fuzhou

  • Kang JY, Choi HI, Im MY, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357

    Article  CAS  PubMed  Google Scholar 

  • Khanh TD, Chung IM, Tawata S, Xuan TD (2007) Allelopathy for weed management in sustainable agriculture. CAB Rev, CABI. http://www.cabi.org/cabreviews/default.aspx. Accessed 16 May 2007

  • Kim KU, Shin DH (2008) Progress and prospect of rice allelopathy research. In: Zeng RS, Mallik AU, Luo SM (eds) Allelopathy in sustainable agriculture and forestry. Springer, New York, pp 189–233

    Chapter  Google Scholar 

  • Kim SY, Madrid AV, Park ST, Yang SJ, Olofsdotter M (2005) Evaluation of rice allelopathy in hydroponics. Weed Res 45:74–79

    Article  Google Scholar 

  • Kizil G, Wilks K, Wells D, AlàAldeen DA (2000) Detection and characterisation of the genes encoding glyoxalase I and II from Neisseria meningitidis. J Med Microbiol 49:669–673

    CAS  PubMed  Google Scholar 

  • Landschulz WH, Johnson PF, McKnight SL (1988) The leucine zipper: a hypothetical structure common to a new class of DNA-binding proteins. Science 240:1759–1764

    Article  CAS  PubMed  Google Scholar 

  • Leung J, Merlot S, Giraudat J (1997) The Arabidopsis abscisic acid-insensitive 2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9:759–771

    Article  CAS  PubMed  Google Scholar 

  • Liang P, Pardee AB (1992) Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257:967–971

    Article  CAS  PubMed  Google Scholar 

  • Maiti MK, Krishnasamy S, Owen HA, Makaroff CA (1997) Molecular characterization of glyoxalase II from Arabidopsis thaliana. Plant Mol Biol 35:471–481

    Article  CAS  PubMed  Google Scholar 

  • Mallik A (2005) Allelopathy: advances, challenges and opportunities. Fourth world congress on allelopathy. The Regional Institute Limited publishing. http://www.regional.org.au/au/allelopathy. Accessed 21 Aug 2005

  • Manning G, Plowman GD, Hunter T, Sudarsanam S (2002) Evolution of protein kinase signaling from yeast to man. Trends Biochem Sci 27:514–520

    Article  CAS  PubMed  Google Scholar 

  • Mesbah K, Camus A, Babinet C, Barra J (2006) Mutation in the Trap/Ssr1 gene, encoding translocon-associated protein, results in outflow tract morphogenetic defects. Mol Cell Biol 26:7760–7771

    Article  CAS  PubMed  Google Scholar 

  • Moll RH, Kamprath EJ, Jackson WA (1982) Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization. Agron J 74:562–564

    Article  Google Scholar 

  • Morris DL (1948) Quantitative determination of carbohydrate with dreywoods anthrone reagent. Science 107:254–255

    Article  CAS  PubMed  Google Scholar 

  • Ni HW, Zhang CX (2005) Use of allelopathy for weed management in China—a review. Allelopath J 15:3–12

    Google Scholar 

  • Nkonge C, Ballance GM (1982) A sensitive colorimetric procedure for nitrogen determination in micro-Kjeldahl digests. J Agric Food Chem 30:416–420

    Article  CAS  Google Scholar 

  • Peng JY, Li ZH, Huang YP (2007) Plant species specific defense signal communication differentially regulates glutathione S-transferase activity and gene expression in the Helicoverpa armigera (Hubner). J Plant Interact 2:93–99

    Article  CAS  Google Scholar 

  • Rice EL (1984) Allelopathy, 2nd edn. Academic Press, New York

    Google Scholar 

  • Rice EL (1995) Biological control of weeds and plant diseases. University of Oklahoma Press, Norman

    Google Scholar 

  • Robert C, Gagné D, Bousquet D, Barnes FL, Sirard M (2001) Differential display and suppressive subtractive hybridization used to identify granulosa cell messenger RNA associated with bovine oocyte developmental competence. Biol Reprod 64:1812–1820

    Article  CAS  PubMed  Google Scholar 

  • Robinson SA, Slade AP, Fox GG, Phillips R, Ratcliffe RG, Stewart GR (1991) The role of glutamate dehydrogenase in plant nitrogen metabolism. Plant Physiol 95:509–516

    Article  CAS  PubMed  Google Scholar 

  • Sano H, Ohashi Y (1995) Involvement of small GTP-binding proteins in defense signal-transduction pathways of higher plants. Proc Natl Acad Sci USA 92:4138–4144

    Article  CAS  PubMed  Google Scholar 

  • Shen LH, Lin WX (2007) Effects of phosphorus levels on allelopathic potential of rice co-cultured with barnyardgrass. Allelopath J 19:393–402

    Google Scholar 

  • Song BQ, Xiong J, Fang CX, Qiu L, Lin RY, Liang YY, Lin WX (2008) Allelopathic enhancement and differential gene expression in rice under low nitrogen treatment. J Chem Ecol 34:688–695

    Article  CAS  PubMed  Google Scholar 

  • Stenzel I, Hause B, Miersch O, Kramell R, Kurz T, Maucher H, Weichert H, Ziegler J, Feussner I, Wasternack C (2003) Jasmonate biosynthesis and the allene oxide cyclase family of Arabidopsis thaliana. Plant Mol Biol 51:895–911

    Article  CAS  PubMed  Google Scholar 

  • Stillman TJ, Baker PJ, Britton KL, Rice DW (1993) Conformational flexibility in glutamate dehydrogenase role of water in substrate recognition and catalysis. J Mol Biol 234:1131–1139

    Article  CAS  PubMed  Google Scholar 

  • Stone JM, Walker JC (1995) Plant protein kinase families and signal transduction. Plant Physiol 108:451–457

    Article  CAS  PubMed  Google Scholar 

  • Sun YJ, Zhou XF, Ma H (2007) Genome-wide analysis of Kelch repeat-containing F-box family. J Integr Plant Biol 49:940–952

    Article  CAS  Google Scholar 

  • Turnbull JJ, Nakajima J, Welford RW, Yamazaki M, Saito K, Schofield CJ (2004) Mechanistic studies on three 2-oxoglutarate-dependent oxygenases of flavonoid biosynthesis: anthocyanidin synthase, flavonol synthase, and flavanone 3β-hydroxylase. J Biol Chem 279:1206–1216

    Article  CAS  PubMed  Google Scholar 

  • Uhlman A, Ebel J (1993) Molecular cloning and expression of 4-coumarate: coenzyme A ligase, an enzyme involved in the resistance response of soybean (Glycine max L.) against pathogen attack. Plant Physiol 102:1147–1156

    Article  Google Scholar 

  • Wang HB, He HB, Chen CY, Lu JC, Chen RS, Guo XK, Liu CH, Lin WX (2009) Physiological responses of allelopathic rice accessions to low phosphorus stress. Allelopath J 23:175–184

    CAS  Google Scholar 

  • Wu H, Pratley J, Lemerle D, Haig T (1999) Crop cultivars with allelopathic capability. Weed Res 39:171–180

    Article  Google Scholar 

  • 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. Fourth world congress on allelopathy. The Regional Institute Limited publishing. http://www.regional.org.au/au/allelopathy. Accessed 21 Aug 2005

  • Yamamoto T, Mori Y, Ishibashi T, Uchiyama Y, Sakaguchi N, Furukawa T, Hashimoto J, Kimura S, Sakaguchi K (2004) Characterization of Rad6 from a higher plant, rice (Oryza sativa L.) and its interaction with Sgt1, a subunit of the SCF ubiquitin ligase complex. Biochem Biophys Res Commun 314:434–439

    Article  CAS  PubMed  Google Scholar 

  • Ziegler J, Stenzel I, Hause B, Maucher H, Hamberg M, Grimm R, Ganal M, Wasternack C (2000) Molecular cloning of allene oxide cyclase. The enzyme establishing the stereochemistry of octadecanoids and jasmonates. J Biol Chem 275:19132–19138

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 30471028) and Provincial Natural Science Foundation of Fujian, China (No. 2009J05045). The authors thank Dr. C.C. Chen for his critical reading of the manuscript.

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Authors and Affiliations

  1. Key Laboratory of Biopesticide and Chemical Biology, Ministry of Education, 350002, Fuzhou, People’s Republic of China

    Chang-Xun Fang, Hai-Bin He, Qing-Shui Wang, Long Qiu, Hai-Bin Wang, Yue-E Zhuang, Jun Xiong & Wen-Xiong Lin

  2. Agroecological Institute/School of Life Sciences, Fujian Agriculture and Forestry University (FAFU), 350002, Fuzhou, People’s Republic of China

    Chang-Xun Fang, Hai-Bin He, Qing-Shui Wang, Long Qiu, Hai-Bin Wang, Yue-E Zhuang, Jun Xiong & Wen-Xiong Lin

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  1. Chang-Xun Fang
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Correspondence to Wen-Xiong Lin.

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Chang-Xun Fang and Hai-Bin He have contributed equally to this work.

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Fang, CX., He, HB., Wang, QS. et al. Genomic analysis of allelopathic response to low nitrogen and barnyardgrass competition in rice (Oryza sativa L.). Plant Growth Regul 61, 277–286 (2010). https://doi.org/10.1007/s10725-010-9475-8

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