Chin Bull Bot

Previous Articles    

Dual Regulating Effects of Ethylene on the Formation of Plant Secondary Metabolites

Rongjun Fang1,2†, Hua Zhao1,3†, Yonghui Liao1, Chengyi Tang1, Fengyao Wu1, Yu Zhu1, Yanjun Pang1, Guihua Lu1, Xiaoming Wang1, Rongwu Yang1*, Jinliang Qi1,4*, Yonghua Yang1*   

  1. 1State Key Laboratory of Pharmaceutical Biotechnology, Institute of Plant Molecular Biology, School of Life Sciences, Nanjing University, Nanjing 210093, China;

    2Jiangsu University of Science and Technology, Zhenjiang 212003, China;

    3Nantong University, Nantong 226019, China; 4Huaian High-Tech Research Institute of Nanjing University, Huaian 223005, China
  • Received:2013-09-29 Revised:2014-01-14 Online:2014-07-02 Published:2014-09-01
  • Contact: Rongwu Yang, Jinliang Qi, Yonghua Yang E-mail:YangYH@nju.edu.cn; QiJL@nju.edu.cn; robertyang@nju.edu.cn

Abstract: Plant secondary metabolites are important natural sources for drugs and chemical raw materials. The formation of these metabolites is closely related to the normal growth and adaptation to environments by plants and could be regulated by a variety of factors. As an endogenous hormone in plants, ethylene plays important roles in regulating most plant physiological processes such as growth, development, stress resistance and secondary metabolite biosynthesis. Here, we review the signal transduction mechanism and regulatory effects of ethylene, especially its dual regulatory effects, on the formation of plant secondary metabolites, namely, how ethylene promotes the biosynthesis of secondary metabolites within a range of concentration in plants but has an inhibitory effect on the formation of secondary metabolites outside of a certain threshold of concentration. We give prospects for further research in this field.

[1]Ahsan, N, Lee, D.-G., Lee, S.-H., Lee, K.-W., Bahk, J. D., & Lee, B.-H. .A proteomic screen and identification of waterlogging-regulated proteins in tomato roots. [J].Plant and Soil, (2007). , 295

((1-2), ):37--51.
[2]Arimura, G, Kost, C., & Boland, W. .Herbivore-induced, indirect plant defences. [J].Biochim Biophys Acta,, (2005). , 1734

((2), ):91--111.
[3]Barry, CS., Llop-Tous, M. I., & Grierson, D. .The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. [J].Plant Physiol,, (2000). , 123

((3), ):979--986.
[4]Binder, BM., Mortimore, L. A., Stepanova, A. N., Ecker, J. R., & Bleecker, A. B..Short-term growth responses to ethylene in Arabidopsis seedlings are EIN3/EIL1 independent. [J].Plant Physiol,, (2004). , 136

((2), ):2921--2927.
[5]Binder, BM., Walker, J. M., Gagne, J. M., Emborg, T. J., Hemmann, G., Bleecker, A. B., et al. .The Arabidopsis EIN3 binding F-Box proteins EBF1 and EBF2 have distinct but overlapping roles in ethylene signaling. [J].Plant Cell,, (2007). , 19

((2), ):509--523.
[6]Biondi, S, Antognoni, F., Perellino, N. C., Sacchetti, G., Minghetti, A., & Poli, F. .Medium composition and methyl jasmonate influence the amount and spectrum of secondary metabolites in callus cultures of Zanthoxylum stenophyllum Hemsl. [J].Plant Biosystems,, (2004). , 138

((2), ):117--124.
[7]Broekaert, WF., Delaure, S. L., De Bolle, M. F., & Cammue, B. P. .The role of ethylene in host-pathogen interactions.[J].Annu Rev Phytopathol,, (2006). , 44,

(1):393--416.
[8]Brown, RL., Kazan, K., McGrath, K. C., Maclean, D. J., & Manners, J. M. .A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 gene of Arabidopsis.[J].Plant Physiol,, (2003). , 132

((2), ):1020--1032.
[9]Buer, CS., Sukumar, P., & Muday, G. K. .Ethylene modulates flavonoid accumulation and gravitropic responses in roots of Arabidopsis.[J].Plant Physiol,, (2006). , 140

((4), ):1384--1396.
[10]Chae, HS., Faure, F., & Kieber, J. J. .The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein.[J].Plant Cell,, (2003). , 15

((2), ):545--559.
[11]Chappell, J.The Biochemistry and Molecular Biology of Isoprenoid Metabolism.[J].Plant Physiol,, (1995). , 107

((1), ):1--6.
[12]Chen, L, Wang, T., Zhao, M., & Zhang, W. . Ethylene-responsive miRNAs in roots of Medicago truncatula identified by high-throughput sequencing at whole genome level.[J].Plant Sci,, (2012)., 184,

(1):14--19.
[13]Chen, YF., Etheridge, N., & Schaller, G. E. .Ethylene signal transduction.[J].Ann Bot,, (2005). , 95

((6), ):901--915.
[14]Cheng, A-X., Lou, Y.-G., Mao, Y.-B., Lu, S., Wang, L.-J., & Chen, X.-Y. .Plant terpenoids: Biosynthesis and ecological functions. [J].Journal of Integrative Plant Biology,, (2007). , 49

((2), ):179--186.
[15]Clay, NK., Adio, A. M., Denoux, C., Jander, G., & Ausubel, F. M. .Glucosinolate metabolites required for an Arabidopsis innate immune response. [J].Science,, (2009). , 323

((5910),):95--101.
[16]Dangl, JL., & Jones, J. D. .Plant pathogens and integrated defence responses to infection. [J].Nature,, (2001)., 411

((6839),): 826--833.
[17]De Boer, K, Tilleman, S., Pauwels, L., Vanden Bossche, R., De Sutter, V., Vanderhaeghen, R., et al.. APETALA2/ETHYLENE RESPONSE FACTOR and basic helix-loop-helix tobacco transcription factors cooperatively mediate jasmonate-elicited nicotine biosynthesis. [J].Plant J,, (2011). , 66

((6), ):1053--1065.
[18]De Luca, V, & St Pierre, B. .The cell and developmental biology of alkaloid biosynthesis. [J].Trends Plant Sci,, (2000). , 5

((4), ):168--173.
[19]Diezel, C, Allmann, S., & Baldwin, I. T. .Mechanisms of optimal defense patterns in Nicotiana attenuata: flowering attenuates herbivory-elicited ethylene and jasmonate signaling. [J].J Integr Plant Biol,, (2011). , 53

((12), ):971--983.
[20]Dixon, RA. .Natural products and plant disease resistance. [J].Nature,, (2001). , 411

((6839),):843--847.
[21]Dubos, C, Le Gourrierec, J., Baudry, A., Huep, G., Lanet, E., Debeaujon, I., et al. .MYBL2 is a new regulator of flavonoid biosynthesis in Arabidopsis thaliana. [J].Plant J,, (2008). , 55

((6), ):940--953.
[22]Efferth, T, Herrmann, F., Tahrani, A., & Wink, M. .Cytotoxic activity of secondary metabolites derived from Artemisia annua L. towards cancer cells in comparison to its designated active constituent artemisinin.[J].Phytomedicine,, (2011). , 18

((11), ):959--969.
[23]El-Kereamy, A, Chervin, C., Roustan, J. P., Cheynier, V., Souquet, J. M., Moutounet, M., et al. .Exogenous ethylene stimulates the long-term expression of genes related to anthocyanin biosynthesis in grape berries.[J].Physiologia Plantarum,, (2003). , 119

((2), ):175--182.
[24]Facchini, PJ. .ALKALOID BIOSYNTHESIS IN PLANTS: Biochemistry, Cell Biology, Molecular Regulation, and Metabolic Engineering Applications.[J].Annu Rev Plant Physiol Plant Mol Biol,, (2001). , 52,

(1):29--66.
[25]Fujimoto, SY., Ohta, M., Usui, A., Shinshi, H., & Ohme-Takagi, M. .Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. [J].Plant Cell,, (2000). , 12

((3), ):393--404.
[26]Gagne, JM., Smalle, J., Gingerich, D. J., Walker, J. M., Yoo, S. D., Yanagisawa, S., et al. .Arabidopsis EIN3-binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation.[J].Proc Natl Acad Sci U S A,, (2004). , 101

((17), ):6803--6808.
[27]Gantet, P, & Memelink, J. .Transcription factors: tools to engineer the production of pharmacologically active plant metabolites. [J].Trends Pharmacol Sci,, (2002). , 23

((12), ):563--569.
[28]Gomez-Roldan, V, Fermas, S., Brewer, P. B., Puech-Pages, V., Dun, E. A., Pillot, J. P., et al. .Strigolactone inhibition of shoot branching. [J].Nature,, (2008). , 455

((7210), ):189--194.
[29]Gray, WM. .Hormonal regulation of plant growth and development.[J].PLoS Biol,, (2004). , 2

((9), ):1270-1273
[30]Guo, H, & Ecker, J. R. .The ethylene signaling pathway: new insights.[J].Curr Opin Plant Biol,, (2004). , 7

((1), ):40--49.
[31]Hanano, S, Domagalska, M. A., Nagy, F., & Davis, S. J. .Multiple phytohormones influence distinct parameters of the plant circadian clock. [J].Genes Cells,, (2006). , 11

((12), ):1381--1392.
[32]Heidstra, R, Yang, W. C., Yalcin, Y., Peck, S., Emons, A. M., van Kammen, A., et al. .Ethylene provides positional information on cortical cell division but is not involved in Nod factor-induced root hair tip growth in Rhizobium-legume interaction. [J].Development,, (1997). , 124

((9), ):1781--1787.
[33]Herzog, TJ. .Recurrent ovarian cancer: how important is it to treat to disease progression? [J].Clin Cancer Res,, (2004). , 10

((22), ):7439--7449.
[34]Homann, V, Mende, K., Arntz, C., Ilardi, V., Macino, G., Morelli, G., et al..The isoprenoid pathway: cloning and characterization of fungal FPPS genes. [J].Curr Genet,, (1996). , 30

((3),): 232--239.
[35]Hossain, MA., Kim, S., Kim, K. H., Lee, S.-J., & Lee, H. .Flavonoid Compounds Are Enriched in Lemon Balm (Melissa officinalis) Leaves by a High Level of Sucrose and Confer Increased Antioxidant Activity. [J].Hortscience,, (2009). , 44

((7), ):1907--1913.
[36]Hughes, EH., & Shanks, J. V..Metabolic engineering of plants for alkaloid production.[J].Metab Eng,, (2002). , 4

((1), ):41--48.
[37]Iriti, M, & Faoro, F. .Chemical diversity and defence metabolism: how plants cope with pathogens and ozone pollution.[J].Int J Mol Sci,, (2009). , 10

((8), ):3371--3399.
[38]Jain, M, Nijhawan, A., Arora, R., Agarwal, P., Ray, S., Sharma, P., et al. .F-box proteins in rice. Genome-wide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. [J].Plant Physiol,, (2007). , 143

((4), ):1467--1483.
[39]Jeong, CS., Chakrabarty, D., Hahn, E. J., Lee, H. L., & Paek, K. Y. .Effects of oxygen, carbon dioxide and ethylene on growth and bioactive compound production in bioreactor culture of ginseng adventitious roots. [J].Biochemical Engineering Journal,, (2006). , 27

((3), ):252--263.
[40]Jeong, SW., Das, P. K., Jeoung, S. C., Song, J. Y., Lee, H. K., Kim, Y. K., et al. . Ethylene suppression of sugar-induced anthocyanin pigmentation in Arabidopsis. [J].Plant Physiol,, (2010)., 154

((3),):1514--1531.
[41]Johnson, PR., & Ecker, J. R. .The ethylene gas signal transduction pathway: a molecular perspective. [J].Annu Rev Genet,, (1998). , 32,

(1):227--254.
[42]Kamiyoshihara, Y, Iwata, M., Fukaya, T., Tatsuki, M., & Mori, H. .Turnover of LeACS2, a wound-inducible 1-aminocyclopropane-1-carboxylic acid synthase in tomato, is regulated by phosphorylation/dephosphorylation. [J].Plant J,, (2010). , 64

((1), ):140--150.
[43]Kerchev, PI., Fenton, B., Foyer, C. H., & Hancock, R. D. .Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways. [J].Plant Cell Environ,, (2012). , 35

((2), ):441--453.
[44]Khan, NA. .Activity of 1-aminocyclopropane carboxylic acid synthase in two mustard (Brassica juncea L.) cultivars differing in photosynthetic capacity. [J].Photosynthetica,, (2004). , 42

((3), ):477--480.
[45]Lavola, A, Julkunen-Tiitto, R., de la Rosa, T. M., Lehto, T., & Aphalo, P. J. .Allocation of carbon to growth and secondary metabolites in birch seedlings under UV-B radiation and CO2 exposure. [J].Physiologia Plantarum,, (2000). , 109

((3),): 260--267.
[46]Lee-Parsons, CW. T. .Gas composition strategies for the successful scale-up of Catharanthus roseus cell cultures for the production of ajmalicine. [J].Phytochemistry Reviews,, (2007). , 6

((2-3), ):419--433.
[47]Legrand, S, Valot, N., Nicole, F., Moja, S., Baudino, S., Jullien, F., et al..One-step identification of conserved miRNAs, their targets, potential transcription factors and effector genes of complete secondary metabolism pathways after 454 pyrosequencing of calyx cDNAs from the Labiate Salvia sclarea L.[J].Gene,, (2010). , 450

((1-2), ):55--62.
[48]Leon-Reyes, A, Du, Y., Koornneef, A., Proietti, S., Korbes, A. P., Memelink, J., et al..Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic Acid. [J].Mol Plant Microbe Interact,, (2010). , 23

((2), ):187--197.
[49]Linden, JC., Haigh, J. R., Mirjalili, N., & Phisaphalong, M. . Gas concentration effects on secondary metabolite production by plant cell cultures. [J].Adv Biochem Eng Biotechnol,, (2001)., 72,

( 1):27--62.
[50]Liu, HH., Tian, X., Li, Y. J., Wu, C. A., & Zheng, C. C.. Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. [J].RNA,, (2008)., 14

((5), ):836--843.
[51]Liu, Q, & Chen, Y. Q. .Insights into the mechanism of plant development: interactions of miRNAs pathway with phytohormone response. [J].Biochem Biophys Res Commun,, (2009). , 384

((1), ):1--5.
[52]Lorenzo, O, Piqueras, R., Sanchez-Serrano, J. J., & Solano, R..ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. [J].Plant Cell,, (2003). , 15

((1), ):165--178.
[53]Matsui, K, Umemura, Y., & Ohme-Takagi, M. .AtMYBL2, a protein with a single MYB domain, acts as a negative regulator of anthocyanin biosynthesis in Arabidopsis. [J].Plant J,, (2008). , 55

((6), ):954--967.
[54]McClellan, CA., & Chang, C..The role of protein turnover in ethylene biosynthesis and response. [J].Plant Sci,, (2008). , 175

((1-2), ):24--31.
[55]Mirjalili, N, & Linden, J. C. .Methyl jasmonate induced production of taxol in suspension cultures of Taxus cuspidata: ethylene interaction and induction models. [J].Biotechnol Prog,, (1996). , 12

((1), ):110--118.
[56]Montiel, G, Zarei, A., Korbes, A. P., & Memelink, J..The jasmonate-responsive element from the ORCA3 promoter from Catharanthus roseus is active in Arabidopsis and is controlled by the transcription factor AtMYC2. [J].Plant Cell Physiol,, (2011). , 52

((3),): 578--587.
[57]Moxon, S, Jing, R., Szittya, G., Schwach, F., Rusholme Pilcher, R. L., Moulton, V., et al. .Deep sequencing of tomato short RNAs identifies microRNAs targeting genes involved in fruit ripening. [J].Genome Res,, (2008). , 18

((10), ):1602--1609.
[58]Nambara, E, & Marion-Poll, A.. Abscisic acid biosynthesis and catabolism. [J].Annu Rev Plant Biol,, (2005)., 56,

(1): 165--185.
[59]Nemhauser, JL., Hong, F., & Chory, J. .Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses.[J].Cell,, (2006). , 126

((3),): 467--475.
[60]Oudin, A, Mahroug, S., Courdavault, V., Hervouet, N., Zelwer, C., Rodriguez-Concepcion, M., et al. .Spatial distribution and hormonal regulation of gene products from methyl erythritol phosphate and monoterpene-secoiridoid pathways in Catharanthus roseus. [J].Plant Mol Biol,, (2007). , 65

((1-2), ):13--30.
[61]Pan, Q, Chen, Y., Wang, Q., Yuan, F., Xing, S., Tian, Y., et al. .Effect of plant growth regulators on the biosynthesis of vinblastine, vindoline and catharanthine in Catharanthus roseus.[J].Plant Growth Regulation,, (2010). , 60

((2),): 133--141.
[62]Pan, Z, Wang, H., & Zhong, J. .Scale-up study on suspension cultures of Taxus chinensis cells for production of taxane diterpene.[J].Enzyme Microb Technol,, (2000). , 27

((9), ):714--723.
[63]Pan, ZW., Wang, H. Q., & Zhong, J. J. .Scale-up study on suspension cultures of Taxus chinensis cells for production of taxane diterpene. [J].Enzyme and Microbial Technology,, (2000). , 27

( (9), ):714--723.
[64]Pilar Lopez-Gresa, M, Torres, C., Campos, L., Lison, P., Rodrigo, I., Maria Belles, J., et al. . Identification of defence metabolites in tomato plants infected by the bacterial pathogen Pseudomonas syringae. [J].Environmental and Experimental Botany,, (2011)., 74,

(1):216--228.
[65]Pre, M, Atallah, M., Champion, A., De Vos, M., Pieterse, C. M., & Memelink, J.. The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. [J].Plant Physiol,, (2008). , 147

((3), ):1347--1357.
[66]Pulido, A, & Laufs, P..Co-ordination of developmental processes by small RNAs during leaf development. [J].J Exp Bot,, (2010). , 61

((5), ):1277--1291.
[67]Rao, SR., & Ravishankar, G. A. .Plant cell cultures: Chemical factories of secondary metabolites. [J].Biotechnol Adv,, (2002). , 20

((2), ):101--153.
[68]Ruther, J, & Kleier, S. .Plant-plant signaling: ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)-3-hexen-1-ol. [J].J Chem Ecol,, (2005). , 31

((9),): 2217--2222.
[69]Santner, A, Calderon-Villalobos, L. I., & Estelle, M. .Plant hormones are versatile chemical regulators of plant growth. [J].Nat Chem Biol,, (2009). , 5

((5), ):301--307.
[70]Shibli, RA., Smith, M. A. L., & Kushad, M. .Headspace ethylene accumulation effects on secondary metabolite production in Vaccinium pahalae cell culture. [J].Plant Growth Regulation,, (1997). , 23

((3), ):201--205.
[71]Shoji, T, Kajikawa, M., & Hashimoto, T. . Clustered transcription factor genes regulate nicotine biosynthesis in tobacco. [J].Plant Cell,, (2010)., 22

((10), ):3390--3409.
[72]Shoji, T, Nakajima, K., & Hashimoto, T..Ethylene suppresses jasmonate-induced gene expression in nicotine biosynthesis. [J].Plant Cell Physiol,, (2000). , 41

((9), ):1072--1076.
[73]Singh, K, Foley, R. C., & Onate-Sanchez, L. .Transcription factors in plant defense and stress responses. [J].Curr Opin Plant Biol,, (2002). , 5

((5), ):430--436.
[74]Sommer, S, Kohle, A., Yazaki, K., Shimomura, K., Bechthold, A., & Heide, L. .Genetic engineering of shikonin biosynthesis hairy root cultures of Lithospermum erythrorhizon transformed with the bacterial ubiC gene. [J].Plant Mol Biol,, (1999). , 39

((4), ):683--693.
[75]Stone, SL., & Callis, J. .Ubiquitin ligases mediate growth and development by promoting protein death. [J].Curr Opin Plant Biol,, (2007). , 10

((6), ):624--632.
[76]Sudha, G, & Ravishankar, G. A..Involvement and interaction of various signaling compounds on the plant metabolic events during defense response, resistance to stress factors, formation of secondary metabolites and their molecular aspects.[J].Plant Cell Tissue and Organ Culture,, (2002). , 71

((3), ):181--212.
[77]Thain, SC., Vandenbussche, F., Laarhoven, L. J., Dowson-Day, M. J., Wang, Z. Y., Tobin, E. M., et al. .Circadian rhythms of ethylene emission in Arabidopsis. [J].Plant Physiol,, (2004). , 136

((3), ):3751--3761.
[78]Tsuchisaka, A, & Theologis, A..Heterodimeric interactions among the 1-amino-cyclopropane-1-carboxylate synthase polypeptides encoded by the Arabidopsis gene family. [J].Proc Natl Acad Sci U S A,, (2004a). , 101

((8), ):2275--2280.
[79]Tsuchisaka, A, & Theologis, A. .Unique and overlapping expression patterns among the arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. [J].Plant Physiology,, (2004b). , 136

((2), ):2982--3000.
[80]Vaishnav, P, & Demain, A. L.. Unexpected applications of secondary metabolites.[J].Biotechnol Adv,, (2011)., 29

((2), ):223--229.
[81]van der Fits, L, & Memelink, J..ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism. [J].Science,, (2000). , 289

((5477), ):295--297.
[82]van der Fits, L, & Memelink, J..The jasmonate-inducible AP2/ERF-domain transcription factor ORCA3 activates gene expression via interaction with a jasmonate-responsive promoter element. [J].Plant J,, (2001). , 25

((1), ):43--53.
[83]Vanhala, L, Eeva, M., Lapinjoki, S., Hiltunen, R., & Oksman-Caldentey, K. M. . Effect of growth regulators on transformed root cultures of Hyoscyamus muticus. [J].Journal of Plant Physiology,, (1998)., 153

((3-4), ):475--481.
[84]Verpoorte, R, Contin, A., & Memelink, J..Biotechnology for the production of plant secondary metabolites. [J].Phytochemistry Reviews,, (2002). , 1

((1), ):13--25.
[85]Vining, LC. . Functions of secondary metabolites.[J].Annu Rev Microbiol,, (1990)., 44,

(1):395--427.
[86]Vom Endt, D, Kijne, J. W., & Memelink, J..Transcription factors controlling plant secondary metabolism: what regulates the regulators? [J].Phytochemistry,, (2002). , 61

((2), ):107--114.
[87]von Dahl, CC., Winz, R. A., Halitschke, R., Kuhnemann, F., Gase, K., & Baldwin, I. T. .Tuning the herbivore-induced ethylene burst: the role of transcript accumulation and ethylene perception in Nicotiana attenuata. [J].Plant J,, (2007). , 51

((2), ):293--307.
[88]Wang, KL., Li, H., & Ecker, J. R..Ethylene biosynthesis and signaling networks.[J].Plant Cell,, (2002). , 14

(Suppl, ):131--151.
[89]Woeste, KE., & Kieber, J. J. .A strong loss-of-function mutation in RAN1 results in constitutive activation of the ethylene response pathway as well as a rosette-lethal phenotype. [J].Plant Cell,, (2000a). , 12

((3), ):443--455.
[90]Woeste, KE., & Kieber, J. J. .A strong loss-of-function mutation in RAN1 results in constitutive activation of the ethylene response pathway as well as a rosette-lethal phenotype. [J].Plant Cell,, (2000b). , 12

((3),): 443--455.
[91]Wu, J, Hettenhausen, C., Schuman, M. C., & Baldwin, I. T. .A comparison of two Nicotiana attenuata accessions reveals large differences in signaling induced by oral secretions of the specialist herbivore Manduca sexta.[J].Plant Physiol,, (2008). , 146

((3), ):927--939.
[92]Xie, F, Frazier, T. P., & Zhang, B.. Identification and characterization of microRNAs and their targets in the bioenergy plant switchgrass (Panicum virgatum). [J].Planta,, (2010)., 232

((2), ):417--434.
[93]Yanagisawa, S, Yoo, S. D., & Sheen, J. .Differential regulation of EIN3 stability by glucose and ethylene signalling in plants. [J].Nature,, (2003). , 425

((6957),): 521--525.
[94]Zhang, W, Zou, A., Miao, J., Yin, Y., Tian, R., Pang, Y., et al..LeERF-1, a novel AP2/ERF family gene within the B3 subcluster, is down-regulated by light signals in Lithospermum erythrorhizon. [J].Plant Biol (Stuttg),, (2011). , 13

((2), ):343--348.
[95]Zhao, J, Zheng, S. H., Fujita, K., & Sakai, K. .Jasmonate and ethylene signalling and their interaction are integral parts of the elicitor signalling pathway leading to beta-thujaplicin biosynthesis in Cupressus lusitanica cell cultures. [J].J Exp Bot,, (2004). , 55

((399), ):1003--1012.
[96]Zhong, JJ.. Plant cell culture for production of paclitaxel and other taxanes. [J].J Biosci Bioeng,, (2002)., 94

((6), ):591--599.
[97]Zhong, S, Zhao, M., Shi, T., Shi, H., An, F., Zhao, Q., et al. .EIN3/EIL1 cooperate with PIF1 to prevent photo-oxidation and to promote greening of Arabidopsis seedlings. [J].Proc Natl Acad Sci U S A,, (2009). , 106

((50), ):21431--21436.
[98]Zhou, M-L., Hou, H.-L., Zhu, X.-M., Shao, J.-R., Wu, Y.-M., & Tang, Y.-X. .Molecular regulation of terpenoid indole alkaloids pathway in the medicinal plant, Catharanthus roseus. [J].Journal of Medicinal Plants Research,, (2010). , 4

((25), ):2760--2772.
[99]Zhu, Z, An, F., Feng, Y., Li, P., Xue, L., A, M., et al..Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. [J].Proc Natl Acad Sci U S A,, (2011). , 108

((30),): 12539--12544.
No related articles found!
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] . [J]. Chin Bull Bot, 2002, 19(01): 121 -124 .
[2] ZHANG Shi-Gong;GAO Ji-Yin and SONG Jing-Zhi. Effects of Betaine on Activities of Membrane Protective Enzymes in Wheat (Triticum aestivum L.) Seedlings Under NaCl Stress[J]. Chin Bull Bot, 1999, 16(04): 429 -432 .
[3] HE Wei-Ming and ZHONG Zhang-Cheng. Effects of Soil Fertility on Gynostemma pentaphyllum Makino Population Behavior[J]. Chin Bull Bot, 1999, 16(04): 425 -428 .
[4] SHE Chao-WenSONG Yun-Chun LIU Li-Hua. Analysis on the G_banded Karyotypes and Its Fluctuation at Different Mitotic Phases and Stages in Triticum tauschii (Aegilops squarrosa)[J]. Chin Bull Bot, 2001, 18(06): 727 -734 .
[5] Guijun Yang, Wenjiang Huang, Jihua Wang, Zhurong Xing. Inversion of Forest Leaf Area Index Calculated from Multi-source and Multi-angle Remote Sensing Data[J]. Chin Bull Bot, 2010, 45(05): 566 -578 .
[6] Man Chen, YishengTu, Linan Ye, Biyun Yang. Effect of Amino Acids on Thallus Growth and Huperzine-A Accumulation in Huperzia serrata[J]. Chin Bull Bot, 2017, 52(2): 218 -224 .
[7] Yefei Shang, Ming Li, Bo Ding, Hao Niu, Zhenning Yang, Xiaoqiang Chen, Gaoyi Cao, Xiaodong Xie. Advances in Auxin Regulation of Plant Stomatal Development[J]. Chin Bull Bot, 2017, 52(2): 235 -240 .
[8] CUI Xiao-Yong, Du Zhan-Chi, Wang Yan-Fen. Photosynthetic Characteristics of a Semi-arid Sandy Grassland Community in Inner Mongolia[J]. Chin J Plan Ecolo, 2000, 24(5): 541 -546 .
[9] LI Wei, ZHANG Ya-Li, HU Yuan-Yuan, YANG Mei-Sen, WU Jie, and ZHANG Wang-Feng. Research on the photoprotection and photosynthesis characteristics of young cotton leaves under field conditions[J]. Chin J Plan Ecolo, 2012, 36(7): 662 -670 .
[10] HU Bao-Zhong, LIU Di, HU Guo-Fu, ZHANG A-Ying, JIANG Shu-Jun. Random Amplified Polymorphic DNA Study of Local Breeds in Chinese lfalfa[J]. Chin J Plan Ecolo, 2000, 24(6): 697 -701 .