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Keywords:
Homology modeling, n Cicer arietinumn , n Fusarium oxysporumn , Wilt disease, Phenylalanine ammonia lyase
The sessile nature of plant makes its immune response more interesting as well as complex. The lack of mobile defender cells increases its further dependency on cellular signaling events and protein-protein interaction. Chickpea (Cicer arietinum) is an important legume crop and its production is seriously curtailed by wilt disease caused by Fusarium oxysporum f. sp. ciceris (Foc). Several attempts have been made to solve the complex metabolic signaling in this host-pathogen interplay. Reactive oxygen species and salicylic acid signaling were known to play a pivotal role in defense signaling against Foc in chickpeas. Phenylalanine ammonia lyase (PAL) is an important protein that senses the redox homoeostasis of the cell to produce salicylic acid in response to pathogenic attacks. In chickpea, although many works have been done on ROS signaling but detailed structural analysis of PAL is missing. Structural information on PAL is necessitated to gain more insight into this plant pathogen interplay. The present study focuses towards determination of physico-chemical properties, secondary organization, and tertiary structure prediction of PAL protein. The structure is validated through Ramachandran plot, Z score analysis, and energy minimization to gain the optimal structure. Finally, the interaction of PAL with other proteins was analyzed by STRING interaction map generator. Cluster analysis revealed that trans cinnamate 4 monooxygenase (C4H) is the best interactor of PAL. Further, the docking study also confirmed its interaction with PAL. This finding may be helpful for further in-depth study of these two protein entities to develop sustainable resistance in chickpeas upon Foc infection.
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Achnine L, Blancaflor EB, Rasmussen S, Dixon RA (2004) Colocalization of L-phenylalanine ammonia-lyase and cinnamate 4-hydroxylase for metabolic channeling in phenylpropanoid biosynthesis. Plant Cell 16:3098–3109
Akula R, Ravishankar GA (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav 6:1720–1731
Allwood EG, Davies DR, Gerrish C, Bolwell GP (2002) Regulation of CDPKs, including identification of PAL kinase, in biotically stressed cells of French bean. Plant Mol Biol 49:533–544
Bartwal A, Mall R, Lohani P, Guru SK, Arora S (2013) Role of secondary metabolites and brassinosteroids in plant defense against environmental stresses. J Plant Growth Regul 32:216–232
Bata Z, Madaras E, Leveles I, Hammerschmidt F, Paizs C, Poppe L, Vértessy BG (2018) Bioactive 3D structure of phenylalanine ammonia-lyase reveal key insights into ligand binding dynamics. Biophys J 114:406a
Benkert P, Tosatto SC, Schomburg D (2008) QMEAN: a comprehensive scoring function for model quality assessment. Proteins: Struct Funct Bioinf 71:261–277
Bhar A, Chatterjee M, Gupta S, Das S (2018) Salicylic acid regulates systemic defense signaling in chickpea during Fusarium oxysporum f. sp. ciceri race 1 infection. Plant Mol Biol Rep 36:162–175
Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546
Bowie JU, Lüthy R, Eisenberg D (1991) A method to identify protein sequences that fold into a known three-dimensional structure. Science 253:164–170
Calabrese JC, Jordan DB, Boodhoo A, Sariaslani S, Vannelli T (2004) Crystal structure of phenylalanine ammonia lyase: multiple helix dipoles implicated in catalysis. Biochemistry 43:11403–11416
Cass CL, Peraldi A, Dowd PF, Mottiar Y, Santoro N, Karlen SD, Bukhman YV, Foster CE, Thrower N, Bruno LC, Moskvin OV (2015) Effects of phenylalanine ammonia lyase (PAL) knockdown on cell wall composition, biomass digestibility, and biotic and abiotic stress responses in Brachypodium. J Exp Bot 66:4317–4335
Chatterjee M, Gupta S, Bhar A, Chakraborti D, Basu D, Das S (2014) Analysis of root proteome unravels differential molecular responses during compatible and incompatible interaction between chickpea (Cicer arietinum L.) and Fusarium oxysporum f. sp. ciceri Race1 (Foc1). BMC Genomics 15:949
Colovos C, Yeates TO (1993) Verification of protein structures: patterns of nonbonded atomic interactions. Protein Sci 2:1511–1519
Crozier A, Clifford MN (2008) In: Ashihara H (ed) Plant secondary metabolites: occurrence, structure and role in the human diet. Wiley, New Jersey
Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM (2008) Phylogeny. Fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:465–469
Duhovny D, Nussinov R, Wolfson HJ (2002) Efficient unbound docking of rigid molecules. Lect Notes Comp Sci 2452:185–200
Gasteiger E, Hoogland C, Gattiker A, Duvaud SE, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. Humana Press, Mew Jersey, pp 571–607
Gholizadeh A (2011) Effects of drought on the activity of phenylalanine ammonia lyase in the leaves and roots of maize inbreds. Aust J Basic Appl Sci 5:952–956
Goujon T, Sibout R, Eudes A, MacKay J, Jouanin L (2003) Genes involved in the biosynthesis of lignin precursors in Arabidopsis thaliana. Plant Physiol Biochem 41:677–687
Gupta S, Bhar A, Chatterjee M, Das S (2013) Fusarium oxysporum f. sp. ciceri race 1 induced redox state alterations are coupled to downstream defense signaling in root tissues of chickpea (Cicer arietinum L). PLoS ONE 8:e73163
Gupta S, Bhar A, Chatterjee M, Ghosh A, Das S (2017) Transcriptomic dissection reveals wide spread differential expression in chickpea during early time points of Fusarium oxysporum f. sp. ciceri race 1 attack. PLoS ONE 12(5):e0178164
Gupta R, Singh A, Srivastava M, Singh V, Gupta MM, Pandey R (2017) Microbial modulation of bacoside a biosynthetic pathway and systemic defense mechanism in Bacopa monnieri under meloidogyne incognita stress. Sci Rep 7:41867
Kim DS, Hwang BK (2014) An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in salicylic acid-dependent signalling of the defence response to microbial pathogens. J Exp Bot 65:2295–2306
Krieger E, Nabuurs SB, Vriend G (2003) Homology modeling. Methods Biochem Analysis 44:509–524
Liang X, Chen X, Li C, Fan J, Guo Z (2017) Metabolic and transcriptional alternations for defense by interfering OsWRKY62 and OsWRKY76 transcriptions in rice. Sci Rep 7:2474
Liu J, Liu Y, Wang Y, Zhang ZH, Zu YG, Efferth T, Tang ZH (2016) The combined effects of ethylene and MeJA on metabolic profiling of phenolic compounds in Catharanthus roseus revealed by metabolomics analysis. Front Physiol 7:217
Lovell SC, Davis IW, Arendall WB, De Bakker PI, Word JM, Prisant MG, Richardson JS, Richardson DC (2003) Structure validation by Cα geometry: ϕ, ψ and Cβ deviation. Proteins Struct Funct Bioinf 50:437–450
Murthy HN, Lee EJ, Paek KY (2014) Production of secondary metabolites from cell and organ cultures: strategies and approaches for biomass improvement and metabolite accumulation. Plant Cell Tissue Organ Cult 118:1–16
Nielsen M, Lundegaard C, Lund O, Petersen TN (2010) CPHmodels-3.0—remote homology modeling using structure-guided sequence profiles. Nucleic Acids Res 38:576–581
Phimchan P, Chanthai S, Bosland PW, Techawongstien S (2014) Enzymatic changes in phenylalanine ammonia-lyase, cinnamic-4-hydroxylase, capsaicin synthase, and peroxidase activities in capsicum under drought stress. J Agric Food Chem 62:7057–7062
Piasecka A, Jedrzejczak-Rey N, Bednarek P (2015) Secondary metabolites in plant innate immunity: conserved function of divergent chemicals. New Phytol 206:948–964
Ramachandran S, Kota P, Ding F, Dokholyan NV (2011) Automated minimization of steric clashes in protein structures. Proteins Struct Funct Bioinform 79:261–270
Rasmussen S, Dixon RA (1999) Transgene-mediated and elicitor-induced perturbation of metabolic channeling at the entry point into the phenylpropanoid pathway. Plant Cell 11:1537–1551
Rook F (2016) Metabolic engineering of chemical defense pathways in plant disease control. In: Collinge DB (ed) Plant pathogen resistance biotechnology. Wiley, Haboken, New Jersey, pp 71–90
Sadeghi M, Dehghan S, Fischer R, Wenzel U, Vilcinskas A, Kavousi HR, Rahnamaeian M (2013) Isolation and characterization of isochorismate synthase and cinnamate 4-hydroxylase during salinity stress, wounding, and salicylic acid treatment in Carthamus tinctorius. Plant Signal Behav 8:e27335
Schneidman-Duhovny D, Inbar Y, Nussinov R, Wolfson HJ (2005) PatchDock and SymmDock: servers for rigid and symmetric docking. Nucleic Acids Res 33:363–367
Shi J, Ma C, Qi D, Lv H, Yang T, Peng Q, Chen Z, Lin Z (2015) Transcriptional responses and flavor volatiles biosynthesis in methyl jasmonate-treated tea leaves. BMC Plant Biol 15:233
Singh K, Kumar S, Rani A, Gulati A, Ahuja PS (2009) Phenylalanine ammonia-lyase (PAL) and cinnamate 4-hydroxylase (C4H) and catechins (flavan-3-ols) accumulation in tea. Funct Integr Genomics 9:125
Sun P, Schuurink RC, Caissard JC, Hugueney P, Baudino S (2016) My way: noncanonical biosynthesis pathways for plant volatiles. Trends Plant Sci 21:884–894
Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M (2014) STRING v10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43:447–452
Szklarczyk D, Morris JH, Cook H, Kuhn M, Wyder S, Simonovic M, Santos A, Doncheva NT, Roth A, Bork P, Jensen LJ (2017) The STRING database in 2017: quality-controlled protein–protein association networks, made broadly accessible. Nucleic Acids Res 45:362–368
Tonnessen BW, Manosalva P, Lang JM, Baraoidan M, Bordeos A, Mauleon R, Oard J, Hulbert S, Leung H, Leach JE (2015) Rice phenylalanine ammonia-lyase gene OsPAL4 is associated with broad spectrum disease resistance. Plant Mol Biol 87:273–286
Tovar MJ, Romero MP, Girona J, Motilva MJ (2002) L-Phenylalanine ammonia‐lyase activity and concentration of phenolics in developing olive (Olea europaea L. Cv Arbequina) fruit grown under different irrigation regimes. J Sci Food Agric 82:892–898
Wang H, Arakawa O, Motomura Y (2000) Influence of maturity and bagging on the relationship between anthocyanin accumulation and phenylalanine ammonia-lyase (PAL) activity in ‘Jonathan’apples. Postharvest Biol Technol 19:123–128
Wang L, Gamez A, Archer H, Abola EE, Sarkissian CN, Fitzpatrick P, Wendt D, Zhang Y, Vellard M, Bliesath J, Bell S, Lemont J, Scriver CR, Stevens RC (2008) Structural and biochemical characterization of the therapeutic Anabaena variabilis phenylalanine ammonia lyase. J Mol Biol 380:623–635
Wanner LA, Li G, Ware D, Somssich IE, Davis KR (1995) The phenylalanine ammonia-lyase gene family in Arabidopsis thaliana. Plant Mol Biol 27:327–338
Weng JK, Chapple C (2010) The origin and evolution of lignin biosynthesis. New Phytol 187:273–285
Yao LM, Wang B, Cheng LJ, Wu TL (2013) Identification of key drought stress-related genes in the hyacinth bean. PLoS ONE 8:e58108
Zhang X, Gou M, Liu CJ (2013) Arabidopsis Kelch repeat F-box proteins regulate phenylpropanoid biosynthesis via controlling the turnover of phenylalanine ammonia-lyase. Plant Cell 25:4994–5010
Zhang X, Liu CJ (2015) Multifaceted regulations of gateway enzyme phenylalanine ammonia-lyase in the biosynthesis of phenylpropanoids. Mol Plant 8:17–27
Zhang C, Wang X, Zhang F, Dong L, Wu J, Cheng Q, Qi D, Yan X, Jiang L, Fan S, Li N, Li D, Xu P, Zhang S (2017) Phenylalanine ammonia-lyase2. 1 contributes to the soybean response towards Phytophthora sojae infection. Sci Rep 7:7242
Zhao Q, Dixon RA (2011) Transcriptional networks for lignin biosynthesis: more complex than we thought? Trends Plant Sci 16:227–233
Zhong R, Ye ZH (2009) Transcriptional regulation of lignin biosynthesis. Plant Signal Behav 4:1028–1034
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. The author is sincerely thankful to the institutions and organizations for developing and providing access to the bioinformatics facilities to conduct the study.