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On a Fitzhugh-Nagumo type model for the pulse-like jasmonate defense response in plants. (English) Zbl 1360.92074

Summary: A mechanistic model of the Fitzhugh-Nagumo type is proposed for the pulse-like jasmonate response in plants. The model is composed of a bistable signaling pathway coupled to a negative feedback loop. The bistable signaling pathway describes a recently discovered positive feedback loop involving jasmonate and the MYC2 transcription factor regulating promoter activity during plant defense. The negative feedback loop is assumed to reflect a second jasmonate-dependent signaling pathway that is also used for ethylene signaling. The impact of the negative feedback loop is to destroy the high-level jasmonate fixed-point of the bistable jasmonate/MYC2 module. As a result, the high-level state becomes a ghost attractor and the jasmonate defense response becomes pulse-like.

MSC:

92C80 Plant biology
92C40 Biochemistry, molecular biology
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[1] Fitzhugh, R., Impulses and physiological states in theoretical models of nerve membranes, Biophys. J., 1, 445-466 (1961)
[2] Nagumo, J.; Arimoto, S.; Yoshizawa, S., An active pulse transmission line stimulating nerve axon, Proc. IRE, 50, 2061-2070 (1962)
[3] Feng, J.; Brown, D., Integrate and fire models with nonlinear leakage, Bull. Math. Biol., 62, 467-481 (2000) · Zbl 1323.92045
[4] Rüdiger, S.; Schimansky-Geier, L., Dynamics of excitable elements with time-delay coupling, J. Theor. Biol., 259, 96-100 (2009) · Zbl 1402.92113
[5] Dahlem, M. A.; Schneider, F. M.; Schöll, E., Efficient control of transient wave forms to prevent spreading polarization, J. Theor. Biol., 251, 202-209 (2010) · Zbl 1398.92039
[6] Hartzell, S.; Bartlett, M. S.; Virgin, L.; Porporato, A., Nonlinear dynamics of the CAM circadian rhythm in response to environmental forcing, J. Theor. Biol., 368, 83-94 (2015) · Zbl 1405.92009
[7] Sukhov, V.; Nerush, V.; Orlova, L.; Vodeneev, V., Simulation of action potential propagation in plants, J. Theor. Biol., 291, 47-55 (2011) · Zbl 1397.92434
[8] Browse, J., Jasmonate passes muster: a receptor and targets for the defense hormone, Annu. Rev. Plant Biol., 60, 183-205 (2009)
[9] Chung, H. S.; Koo, A. J.K.; Gao, X.; Jayanty, S.; Thines, B.; Jones, A. D.; Howe, G. A., Regulation and function of Arabidopsis jasmonate ZIM-domain genes in response to wounding and herbivory, Plant Physiol., 146, 952-964 (2008)
[10] Suza, W. P.; Staswick, P. E., The role of JAR1 in jasmonoyl-L-isoleucine production during Arabidopsis wound response, Planta, 227, 1221-1232 (2008)
[11] McConn, M.; Creelman, R. A.; Bell, E.; Mullet, J. E.; Browse, J., Jasmonate is essential for insect defense in Arabidopsis, Proc. Natl. Acad. Sci. USA, 94, 5473-5477 (1997)
[12] Schittko, U.; Preston, C. A.; Baldwin, I. T., Eating the evidence? Mandacu sexta larvae can not disrupt specific jasmonate induction in Nicotiana attenuata by rapid consumption, Planta, 210, 343-346 (2000)
[13] Kang, J. H.; Wang, L.; Giri, A.; Baldwin, T., Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid-isoleucine-mediated defense against Manduca sexta, The Plant Cell, 18, 3303-3320 (2006)
[14] Wang, L.; Halitschke, R.; Kang; Berg, A.; Harnisch, F.; Baldwin, I. T., Independent silencing two JAR family members impairs levels of trypsin proteinase inhibitors but not nicotine, Planta, 226, 159-167 (2007)
[15] Karban, R.; Baldwin, I. T., Induced Responses to Herbivory (1997), Chicago University Press: Chicago University Press Chicago
[16] Karban, R.; Agrawal, A. A.; Mangel, M., The benefits of induced defenses against herbivores, Ecology, 78, 1351-1355 (1997)
[17] Bosch, M.; Berger, S.; Schaller, A.; Stintzi, A., Jasmonate-dependent induction of polyphenol oxidase activity in tomato foliage is important for defense against Spodoptera exigua but not against Manduca sexta, BMC Plant Biol., 14, 257 (2014)
[18] Dicke, M.; van Poecke, R. M.P., Signalling in plant-insect interactions: signal transduction in direct and indirect plant defense, (Scheel, D.; Wasternack, C., Plant Signal Transduction (2002), Oxford University Press: Oxford University Press New York), 289-316
[19] Schaller, F.; Weiler, E. W., Wound and mechanical signalling, (Scheel, D.; Wasternack, C., Plant Signal Transduction (2002), Oxford University Press: Oxford University Press New York), 20-44
[20] Langebartels, C.; Kangasjarvi, J.; Sandermann, H., Ethylene and jasmonate as regulators of cell death in disease resistance, Molecular Ecotoxicity of Plants, 75-109 (2004), Springer: Springer Berlin
[21] Turlings, T. C.J.; Tumlinson, J. H.; Lewis, W. J., Exploitation of herbivore- induced plant odors by host-seeking parasitic wasps, Nature, 250, 1251-1253 (1990)
[22] Carello, C.; Vaz, D.; Blau, J. J.C.; Petrusz, S., Unnerving intelligence, Ecol. Psychol., 24, 241-264 (1998)
[23] Dicke, M.; van Loon, J. J.A.; Soler, R., Jasmonic acid and herbivory differentially induce carnivore-attracting plant volatiles in lima bean plants, J. Chem. Ecol., 25, 1907-1922 (1999)
[24] Dicke, M.; van Loon, J. J.A.; Soler, R., Chemical complexity of volatiles from plants induced by multiple attack, Nat. Chem. Biol., 5, 317-324 (2009)
[25] Reymond, P.; Farmer, E. E., Jasmonate and salicylate as global signals for defense gene expression, Curr. Opin. Plant Biol., 1, 404-411 (1998)
[26] Lyons, R.; Manners, J. M.; Kazan, K., Jasmonate biosynthesis and signaling in monocots: a comparative overview, The Plant Cell Rep., 32, 815-827 (2013)
[27] Chini, S.; Fonseca, S.; Fernandez, G.; Adie, B.; Chico, J. M.; Lorenzo, O.; Gracia-Casado, G.; Lopez-Vidriero, I.; Lozano, F. M.; Ponce, M. R.; Micol, J. L.; Solano, R., The JAZ family of repressors is the missing link in jasmonate signaling, Nature, 448, 666-671 (2007)
[28] Farmer, E. E., Jasmonate perception machines, Nature, 448, 659-660 (2007)
[29] Kazan, K.; Manners, J. M., MYC2: the master in action, Mol. Plant, 6, 686-703 (2013)
[30] Kim, J. R.; Yoon, Y.; Cho, K. H., Coupled feedback loops form dynamic motifs of cellular networks, Biophys. J., 94, 359-365 (2008)
[31] Rue, P.; Garcia-Ojalvo, J., Gene circuit designs for noisy excitable dynamics, Math. Biosci., 231, 90-97 (2011) · Zbl 1214.92024
[32] Lorenz, D. R.; Cantor, C. R.; Collins, J. J., A network biology approach to aging in yeast, Proc. Natl. Acad. Sci. USA, 106, 1145-1150 (2009)
[33] Kholodenko, B. N.; Kiyatikin, A.; Bruggeman, F.; Sontag, E.; Westerhoff, H. V.; Hock, J. B., Untangling the wires: a strategy to trace functional interactions in signaling and gene networks, Proc. Natl. Acad. Sci. USA, 20, 12841-12846 (2002)
[34] Frank, T. D.; Cheong, A.; Okada-Hatakeyama, M.; Kholodenko, B. N., Catching transcriptional regulation by thermodynamical modeling, Phys. Biol., 9, 045007 (2012)
[35] Sheard, L. B.; Tan, X.; Mao, H., Jasmonate perception by inositol phosphate-potentiated COI1-JAZ co-receptor, Nature, 468, 400-405 (2010)
[36] Chini, S.; Boter, M.; Solano, R., Plant oxylipins: COI1/JAZs/MYC2 as the core jasmonic acid-signalling module, FEBS J., 276, 4682-4692 (2009)
[37] Block, D. H.S.; Hussein, R.; Liang, L. W.; Lim, H. N., Regulatory consequences of gene translocation in bacteria, Nucleic Acid Res., 40, 8979-8992 (2012)
[38] Murphy, K. F.; Balazsi, G.; Collins, J., Combinatorial promoter design for engineering noisy gene expression, Proc. Natl. Acad. Sci. USA, 104, 12726-12731 (2007)
[39] Ang, J.; Harris, E.; Hussey, B. J.; Kil, R.; McMillen, D. R., Tuning response curves for synthetic biology, ACS Synth. Biol., 2, 547-567 (2013)
[40] Alon, U., An Introduction to Systems Biology: Design Principles of Biological Circuits (2007), Chapman and Hall: Chapman and Hall London
[41] James, E. G., Metastable postural coordination dynamics, Neurosci. Lett., 548, 176-180 (2013)
[42] Deca, G.; Jirsa, V. K., Ongoing cortical activity at rest: criticality, multistability, and ghost attractors, J. Neurosci., 32, 3366-3375 (2012)
[43] Patanarapeelert, K.; Frank, T. D.; Beek, P. J.; Friedrich, R.; Tang, I. M., Theoretical analysis of destabilization resonances in time-delayed stochastic second order dynamical systems and some implications for human motor control, Phys. Rev. E, 73, 021901 (2006)
[44] Devoto, A.; Turner, J. G., Regulation of jasmonate-mediated plant responses in Arabidopsis, Ann. Bot., 92, 329-337 (2003)
[45] Penninckx, I. A.M. A.; Eggermont, K.; Terras, F. R.G.; Thomma, B. P.H. J.; De Samblanx, G. W.; Buchala, A.; Metraux, J. P.; Manners, J. M.; Broekaert, W. F., Pathogen-induced systemic activation of a plant defiensin gene in Arabidopsis follows a salicylic acid-independent pathway, The Plant Cell, 8, 2309-2323 (1996)
[46] Lorenzo, O.; Piqueras, R.; Sanchez-Serrano, J. J.; Solano, R., Ethylene response factor 1 integrates signals from ethylene and jasmonate pathways in plant defense, The Plant Cell, 15, 165-178 (2003)
[47] Yang, D. L.; Yao, J.; Mei, C. S.; Tong, X. H.; Zeng, L. J.; Li, Q.; Xiao, L. T.; Sun, T. P.; Li, J.; Deng, X. W.; Lee, C. M.; Thomashow, M. F.; He, Z.; He, S. Y., Plant hormone jasmonate prioritizes defense over growth by interfering with the gibberellin signaling cascade, Proc. Natl. Acad. Sci. USA, 109, E1192-E1200 (2012)
[48] Heinrich, M.; Hettenhausen, C.; Lange, T.; Wunsche, H.; Fang, J.; Baldwin, I. T.; Wu, J., High levels of jasmonic acid antagonized the biosynthesis of gibberellins and inhibit the growth of Nicotiana attenuata stems, The Plant J., 73, 591-606 (2013)
[49] Takahasi, H.; Kanayama, Y.; Zheng, M. S.; Kusano, T.; Hase, S.; Ikegami, M.; Shah, J., Antagonistic interactions between the SA and JA signaling pathway in Arabidopsis modulate expression of defense genes and gene-for-gene resistance to cucumber mosaic virus, Plant Cell Physiol., 45, 803-809 (2004)
[50] Sasaki-Sekimoto, Y.; Jikumaru, Y.; Obayashi, T.; Saito, H.; Masuda, S.; Ohta, Y. K.H.; Shirasu, K., Basic helix-loop-helix transcription factors jasmonate-associated MYC2-like1 (JAM1), JAM2, and JAM3 are negative regulators of jasmonate responses in Arabidopsis, Plant Physiol., 163, 291-304 (2013)
[51] Chao, L.; He, X.; Luo, X.; Xu, L.; Liu, L.; Min, L.; Jin, L.; Zhu, L.; Zhang, X., Cotton WRKY1 mediates the plant defense-to-development transition during infection of cotton by Verticillium dahliae by activating jasmonate zim-domain1 expression, Plant Physiol., 166, 2179-2194 (2014)
[52] Banerjee, S.; Bose, I., Transient pulse formation in jasmonate signaling pathway, J. Theor. Biol., 273, 188-196 (2011) · Zbl 1405.92091
[53] Frank, T. D., A limit cycle model for cycling mood variations of bipolar disorder patients derived from cellular biochemical reaction equations, Commun. Nonlinear Sci. Numer. Simul., 18, 2107-2119 (2013) · Zbl 1308.92028
[54] Steinfeld, J. L.; Francisco, J. S.; Hase, W. L., Chemical Kinetics and Dynamics (1989), Prentice Hall: Prentice Hall New Jersey
[55] Wilkinson, D. J., Stochastic Modeling for Systems Biology (2006), Chapman and Hall/CRC: Chapman and Hall/CRC Boca Raton
[56] Zhao, T.; Xiao, Y.; Smith, R. J., Non-smooth plant disease models with economic thresholds, Math. Biosci., 241, 34-48 (2013) · Zbl 1309.92077
[57] Feng, Z.; Qiu, Z.; Liu, R.; DeAngelis, D. L., Dynamics of a plant-herbivore-predator system with plant-toxicity, Math. Biosci., 229, 190-204 (2011) · Zbl 1208.92046
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