Abstract
Cis-cinnamic acid (CA) is one of many cis-phenylpropanoids found in both monocots and dicots. It is produced in planta via sunlight-mediated isomerization of trans-cinnamic acid. This pair of isomers plays a differential role in regulation of plant growth. A functional proteomics approach has been adopted to identify genes of cis/trans-CA mixture-enhanced expression. Out of 1,241 proteins identified by mass spectrometry, 32 were CA-enhanced and 13 repressed. Further analysis with the molecular biology approach revealed 2 cis-CA (Zusammen-CA)-Enhanced genes, named ZCE1 and ZCE2, which encode members of the major latex protein-like (MLPL) gene family. The transcript accumulation of both genes is positively correlated with the amount of cis-CA applied externally, ranging from 1 to 100 μM. ZCE1 transcript accumulation is enhanced largely by cis-CA and slightly by other cis-phenylpropanoids. Treatment of several well-characterized plant growth regulator perception-deficient mutants with cis-CA is able to promote ZCE1 transcript accumulation, suggestive of distinct signaling pathways regulating cis-CA response. The zce1 loss-of-function mutant produced via the RNA-interference technique produces an earlier bolting phenotype in Arabidopsis, suggesting that ZCE1 plays a role in promoting vegetative growth and delay flowering.
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Aggelis A, John I, Karvouni Z, Grierson D (1997) Characterization of two cDNA clones for mRNAs expressed during ripening of melon (Cucumis melo L) fruits. Plant Mol Biol 33:313–322
Bandurski RS, Schulze A (1974) Concentration of indole-3-acetic acid and its esters in Avena and Zea. Plant Physiol 54:257–262
Bandurski RS, Schulze A (1977) Concentration of indole-3-acetic acid and its derivatives in plants. Plant Physiol 60:211–213
Bleecker AB, Estelle MA, Somerville C, Kende H (1988) Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241:1086–1089
Brabham DE, Giggs RH (1981) Cis-trans photoisomerization of abscisic acid. Photochem Photobiol 34:33–37
Braun J, Tevini M (1993) Regulation of UV-protective pigment synthesis in the epidermal layer of rye seedlings (Secale-Cereale L-Cv Kustro). Photochem Photobiol 57:318–323
Canovas FM, Recorbet EDG, Jorrin J, Mock HP, Rossignol M (2004) Plant proteome analysis. Proteomics 4:285–298
Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57–63
Chaves N, Sosa T, Alias JC, Escudero JC (2001) Identification and effects of interaction phytotoxic compounds from exudates of cistus ladanifer leaves. J Chem Ecol 27:611–621
Chen G, Bi YR, Li N (2005a) EGY1 encodes a membrane-associated and ATP independent metalloprotease that is required for chloroplast development. Plant J 41:364–375
Chen MJ, Vijaykumar V, Lu BW, Xia B, Li N (2005b) Cis- and trans-cinnamic acid have different effects on the catalytic properties of Arabidopsis phenylalanine ammonia lyases PAL1, PAL2 and PAL4. J Integr Plant Biol 47:67–75
Chernushevich IV, Loboda AV, Thomson A (2001) An introduction to quadrupole-time-of-flight mass spectrometry. J. Mass Spectr 36:849–865
Chiang HH, Hwang I, Goodman HM (1995) Isolation of the Arabidopsis GA4 locus. Plant Cell 7:195–201
Chong J, Pierrel MA, Atanassova R, Werck-Reichhart D, Fritig B, Saindrenan P (2001) Free and conjugated benzoic acid in tobacco plants and cell cultures. Induced accumulation upon elicitation of defense responses and role as salicylic acid precursors. Plant Physiol 125:318–328
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Cochrane FC, Davin LB, Lewis NG (2004) The Arabidopsis phenylalanine ammonia lyase gene family: kinetic characterization of the four PAL isoforms. Phytochem 65:1557–1564
Dixon RA (2001) Natural products and plant disease resistance. Nature 411:843–847
Friedrich H (1976) Phenylpropanoid constituents of essential oils. Lloydia 39:1–7
Gray WM, Ostin A, Sanberg G, Romano CP, Estelle M (1998) High temperature promotes auxin-mediated hypocotyls elongation in Arabidopsis. Proc Natl Acad Sci USA 95:7197–7202
Guzman P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523
Hahlbrock K, Scheel D (1989) Physiology and molecular-biology of phenylpropanoid metabolism. Annu Rev Plant Physiol Plant Mol Biol 40:347–369
Hall AE, Bleecker AB (2003) Analysis of combinatorial loss-of-function mutants in the Arabidopsis ethylene receptors reveals that the ers1 etr1 double mutant has severe developmental defects that are EIN2 dependent. Plant Cell 15:2032–2041
Haskins FA, Williams LG, Gorz HJ (1964) Light-induced trans to cis conversion of β-D-glucosl o-hydroxycinnamic acid in Melilotus alba leaves. Plant Physiol 39:777–781
Herde O, Pena CH, Wasternack C, Willmitzer L, Fisahn J (1999) Electric signaling and pin2 gene expression on different abiotic stimuli depend on a distinct threshold level of endogenous abscisic acid in several abscisic acid-deficient tomato mutants. Plant Physiol 119:213–218
Hiradate S, Morita S, Furubayashi A, Fujii Y, Harada J (2005) Plant growth inhibition by cis-cinnamoyl glucosides and cis-cinnamic acid. J Chem Ecol 31:591–601
Humphreys JM, Chapple C (2002) Rewriting the lignin roadmap. Curr Opin Plant Biol 5:224–229
Jones CS, Davies HV, McNicol RJ, Taylor MA (1998) Cloning of three genes up-regulated in ripening raspberry fruit (Rubus idaeus cv. Glen clova). J Plant Physiol 153:643–648
Kasahara H, Takei K, Ueda N, Hishiyama S, Yamaya T, Kamiya Y, Yamaguchi S, Sakakibara H (2004) Distinct isoprenoid origins of cis- and trans-zeatin biosyntheses in Arabidopsis. J Biol Chem 279:14049–14054
Kebarle P (2000) A brief overview of the present status of the mechanisms involved in electrospray mass spectrometry. J Mass Spectrom 35:804–817
Klepacka J, Fornal L (2006) Ferulic acid and its position among the phenolic compounds of wheat. Crit Rev Food Sci Nutr 46:639–647
Koepfli JB, Thimann KV, Went FW (1937) Plant hormones: structure and physiology activity. J Biol Chem 12:763–779
Laby RG, Kincaid MS, Kim D, Gilbson SI (2000) The Arabidopsis sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response. Plant J 23:587–596
LeClere S, Schmelz EA, Chourey PS (2007) Cell wall invertase-deficient miniature1 kernels have altered phytohormone levels. Phytochem 69:692–699
Lee HI, Leon J, Raskin I (1995) Biosynthesis and metabolism of salicylic acid. Proc Natl Acad Sci USA 92:4076–4079
Leyser HMO, Lincoln Ca, Timpte C, Lammer D, Turner J, Estelle M (1993) Arabidopsis auxin-resistance gene-Axr1 encodes a protein related to ubiquitin-activating enzyme-E1. Nature 364:161–164
Li X, Gerber SA, Rudner AD, Beausoleil SA et al (2007) Large-scale phosphorylation analysis of α-factor-arrested Saccharomyces cerevisiae. J Proteome Res 6:1190–1197
Li H, Wong WS, Zhu L, Guo HW, Ecker J, Li N (2009) Phosphoproteomic analysis of ethylene-regulated protein phosphorylation in etiolated seedlings of Arabidopsis mutant ein2 using two-dimensional separations coupled with a hybrid quadrupole time-of-flight mass spectrometer. Proteomics 9:1646–1661
Liu H, Sadygov RG, Yates JR (2004) A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 76:4193–4201
Ljung K, Bhalerao RP, Sandberg G (2001) Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant J Cell Mol Biol 28:465–474
Loake GJ, Choudhary AD, Harrison MJ, Mavandad M, Lamb CJ, Dixon RA (1991) Phenylpropanoid pathway intermediates regulate transient expression of a chalcone synthase gene promoter. Plant Cell 3:829–840
Locher R, Martin V, Grison R, Pilet PE (1994) Cell wall-bound trans- and cis-ferulic acids in growing maize roots. Physiol Plant 90:734–738
Mavandad M, Edwards R, Liang X, Lamb CJ, Dixon RA (1990) Effects of trans-cinnamic acid on expression of the bean phenylalanine ammonia-lyase gene family. Plant Physiol 94:671–680
Miyawaki K, Tarkowski P, Matsumoto-Kitano M, Kato T, Sato S, Tarkowska D, Tabata S, Sandberg G, Kakimoto T (2006) Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc Natl Acad Sci USA 103:16598–16603
Mockler TC, Yu XH, Shalitin D, Parikh D, Michael TP, Liou J, Huang J, Smith Z, Alonso JM, Ecker JR, Chory J, Lin CT (2004) Regulation of flowering time in Arabidopsis by K homology domain proteins Proc. Nat Acad Sci USA 101:12759–12764
Morita S, Hiradate S, Fujii Y, Harada J (2005) Cis-cinnamoyl glucoside as a major plant growth inhibitor contained in Spiraea prunifolia. Plant Growth Regul 46:125–131
Nam YW, Tichit L, Leperlier M, Cuerq B, Marty I, Lelievre JM (1999) Isolation and characterization of mRNAs differentially expressed during ripening of wild strawberry (Fragaria vesca L.) fruits. Plant Mol Biol 39:629–636
Nessler CL, Burnett RJ (1992) Organization of the major latex protein gene family in opium poppy. Plant Mol Biol 20:749–752
Nessler CL, Kurz WGW, Pelcher LE (1990) Isolation and analysis of the major latex protein genes of opium poppy. Plant Mol Biol 15:951–953
Ohashi H, Yamamoto E, Lewis NG, Towers GHN (1987) 5-Hydroxyferulic acid in Zea mays and Hordeum vulgare cell walls. Phytochemistry 26:1915–1916
Ohkmae KP (2004) Proteomic studies in plants. J Biochem Mol Biol 37:133–138
Ottoline Leyser HM, Lincoln CA, Timpte C, Lammer D, Turner J, Estelle M (1993) Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin activating enzyme E1. Nature 364:161–164
Phee BK, Park S, Cho JH, Jeon JS, Bhoo SH, Hahn TR (2007) Comparative proteomic analysis of blue light signaling components in the Arabidopsis cryptochrome 1 mutant. Mol Cells 23:154–160
Rasmussen S, Rudolph H (1997) Isolation, purification and characterization of UDP-glucose: cis-p-coumaric acid beta-D-glucosyltransferase from Sphagnum fallax. Phytochemistry 46:449–453
Razal RA, Ellis S, Singh S, Lewis NG, Towers GHN (1996) Nitrogen recycling in phenylpropanoid metabolism. Phytochemistry 41(1):31–35
Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JAH (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283:1541–1544
Rohde A, Morreel K, Ralph J, Goeminne G, Hostyn V, De RR, Kushnir S, Van DJ, Joseleau JP, Vuylsteke M, Van DG, Van BJ, Messens E, Boerjan W (2004) Molecular phenotyping of the pal1 and pal2 mutants of Arabidopsis thaliana reveals far-reaching consequences on phenylpropanoid, amino acid, and carbohydrate metabolism. Plant Cell 16:2749–2771
Rossignol M, Peltier J, Mock H, Matros A, Maldonado AM, Jorrin JV (2006) Plant proteome analysis: a 2004–2006 update. Proteomics 6:5529–5548
Ruperti B, Bonghi C, Ziliotto F, Pagni S, Rasori A, Varotto S, Tonutti P, Giovannoni JJ, Ramina A (2002) Characterization of a major latex protein (MLP) gene down-regulated by ethylene during peach fruitlet abscission. Plant Sci 163:265–272
Schalk M, Cabello-Hurtado F, Pierrel MA, Atanossova R, Saindrenan P, Werck-Reichhart D (1998) Piperonylic acid, a selective, mechanism-based inactivator of the trans-cinnamate 4-hydroxylase: a new tool to control the flux of metabolites in the phenylpropanoid pathway. Plant Physiol 118:209–218
Schweizer P, Buchala A, Silverman P, Seskar M, Raskin I, Metraux JP (1997) Jasmonate-inducible genes are activated in rice by pathogen attack without a concomitant increase in endogenous jasmonic acid levels. Plant Physiol 14:79–88
Shirley BW, Kubasek WL, Storz G, Bruggemann E, Koornneef M, Ausubel FM, Goodman HM (1995) Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant J 8:659–671
Smith NA, Singh SP, Wang MB, Stoutjesdijk P, Green A, Waterhouse PM (2000) Total silencing by intron-spliced hairpin RNAs. Nature 407:319–320
Srivastava LM (2002) Plant growth and development, chaps 6, 10. Academic Press, London
Staswick PE, Tiryaki I, Rowe ML (2002) Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14:1405–1415
Steiling K, Kadar AY, Bergerat A, Flanigon J, Sridhar S, Shah V, Ahmad QR, Brody JS, Lenburg ME, Steffen M, Spira A (2009) Comparison of proteomic and transcriptomic profiles in the bronchial airway epithelium of current and never smokers. Plos One 4:e5043
Tam YY, Epstein E, Normanly J (2000) Characterization of auxin conjugates in Arabidopsis. Low steady-state levels of indole-3-acetyl-asparte, indole-3-acetyl-glutamate, and indole-3-acetyl-glucose. Plant Physiol 123:589–595
Trauger SA, Kalisak E, Kalisak J, Morita H, Weinberg MV, Menon AL, Poole FL II, Adams MWW, Siuzdak G (2008) Correlating the transcriptome, proteome, and metabolome in the environmental adaption of a hyperthermophile. J Proteome Research 7:1027–1035
Tsuchisaka A, Yu GX, Jin HL, Alonso JM, Ecker JR, Zhang XM, Gao S, Theologis A (2009) A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana. Genetics 183:979–1003
Tun NN, Livaja M, Kieber JJ, Scherer GF (2008) Zeatin-induced nitric oxide (NO) biosynthesis in Arabidopsis thaliana mutants of NO biosynthesis and of two-component signaling genes. New Phytol 178:515–531
Turner LB, Mueller-Harvey I, Mcallan AB (1992) light-induced isomerization and dimerization of cinnamic acid derivatives in cell walls. Phytochem 33:791–796
Van Der Straeten D, Zhou ZY, Prinsen E, Van Onckelen HA, Van Montagu MC (2001) A comparative molecular-physiological study of submergence response in lowland and deepwater rice. Plant Physiol 125:955–968
Van Overbeek J, Blondeau R, Horne V (1951) Trans-cinnamic acid as an anti-auxin. Am J Bot 38:589–595
Ververidis F, Trantas E, Douglas C, Vollmer G, Kretzschmar G, Panopoulos N (2007) Biotechnology of flavonoids and other phenylpropanoid-derived natural products. Part I: chemical diversity, impacts on plant biology and human health. Biotechnology 2:1214–1234
Vestal ML, Campbell JM (2005) Tandem time-of-flight mass spectrometry. Meth Enzymol 402:79–108
Visser EJW, Cohen JD, Barendse GWM, Blom CWPM, Voesenek LACJ (1996) An ethylene-mediated increase in sensitivity to auxin induces adventitious root formation in flooded Rumex palustris Sm. Plant Physiol 2:1687–1692
Vissers JPC, Langridge JI, Aerts JMFG (2007) Analysis and quantification of diagnostic serum markers and protein signatures for Gaucher disease. Mol Cell Proteomics 6:755–766
Vogel JP, Schuerman P, Woeste K, Brandstatter I, Kieber JJ (1998) Isolation and characterization of Arabidopsis mutants defective in the induction of ethylene biosynthesis by cytokinin. Genetics 149:417–427
Walcazk HA, Dean JV (1999) Vascular transport of the glutathione conjugate of trans-cinnaic acid. Phytochemistry 53:441–446
Wang W, Zhou H, Lin H, Roy S, Shaler TA, Hill LR, Norton S, Kumar P, Anderle M, Becker CH (2003) Quantification of proteins and metabolites by mass spectrometry without isotopic labeling or spiked standards. Anal Chem 75:4818–4826
Wang NN, Shih MC, Li N (2005) The GUS reporter-aided analysis of the promoter activities of Arabidopsis ACC synthase genes AtACS4, AtACS5, and AtACS7 induced by hormones and stresses. J Exp Bot 56:909–920
Went FW, Thimann KV (1937) Phytohormones. The macmillan company, New York, pp 137–140
Wong WS, Guo D, Wang XL, Yin ZQ, Xia B, Li N (2005) Study of cis-cinnamic acid in Arabidopsis thaliana. Plant Physiol Biochem 43:929–937
Wu H, Haig T, Pratley J, Lemerle D, An M (2001) Allelochemicals in wheat (Triticum aestivum L.): variation of phenolic acids in shoot tissues. J Chem Ecol 27:125–135
Wu FZ, Lu TC, Shen Z, Wang BC, Wang HX (2008) N-terminal acetylation of two major latex proteins from Arabidopsis thaliana using electrospray ionization tandem mass spectrometry. Plant Mol Biol Reporter 26:88–97
Yang XX, Choi HW, Yang SF, Li N (1999) A UV-light activated cinnamic acid isomer regulates plant growth and gravitropism via an ethylene receptor independent pathway. Aust J Plant Physiol 26:325–335
Yin ZQ, Wong WS, Ye WC, Li N (2003) Biologically active cis-cinnamic acid occurs naturally in Brassica parachinensis. Chin Sci Bull 48:555–558
Zimmerman PW, Hitchcock AE (1939) Activation of cinnamic acid by ultraviolet light and the physiological activity of its emanation. Contrib Boyce Thompson Inst Plant Res 10:197–200
Acknowledgments
The research was supported by the grants: HKUST6276/03M, 661207, 661408, HKUST6413/06M, N_HKUST627/06, DAG98/99.SC10, DAG04/05.SC08, DAG93/94.SC06 and HKUST6105/00M, HKUST6105/01M, RPC07/08.SC16, SBI08/09.SC08 and GMGS08/09.SC04, which were awarded to Ning LI by the Research Grant Council of Hong Kong and HKUST R&D.
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Guo, D., Wong, W.S., Xu, W.Z. et al. Cis-cinnamic acid-enhanced 1 gene plays a role in regulation of Arabidopsis bolting. Plant Mol Biol 75, 481–495 (2011). https://doi.org/10.1007/s11103-011-9746-4
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DOI: https://doi.org/10.1007/s11103-011-9746-4