Comparative analyses of phytochelatin synthase (PCS) genes in higher plants

References

• Ozturk A, Yarci C, Ozyigit II. Assessment of heavy metal pollution in Istanbul using plant (Celtis australis L.) and soil assays. Biotechnol Biotechnol Equip. 2017;31:948–954.
   Web of Science ®Google Scholar
• Osma E, Ozyigit II, Leblebici Z, et al. Determination of heavy metal concentrations in tomato (Lycopersicon esculentum Miller) grown in different station types. Rom Biotech Lett. 2012;17:6962–6974.
   Web of Science ®Google Scholar
• Dogan I, Ozyigit II, Demir G. Influence of aluminium on mineral nutrient uptake and accumulation in Urtica pilulifera L. J Plant Nutr. 2014;37:469–481.
   Web of Science ®Google Scholar
• Peterson AG, Oliver DJ. Leaf-targeted phytochelatin synthase in Arabidopsis thaliana. Plant Physiol Biochem. 2006;44:885–892.
   PubMed Web of Science ®Google Scholar
• Cobbett C, Goldsbrough P. Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol. 2002;53:159–182.
   PubMed Web of Science ®Google Scholar
• Vivares D, Arnoux P, Pignol D. A papain-like enzyme at work: native and acyl-enzyme intermediate structures in phytochelatin synthesis. Proc Natl Acad Sci USA. 2005;102:18848–18853.
   PubMed Web of Science ®Google Scholar
• Kanaujia SP. 13 understanding toxic metal–binding. In: Surajit Das, Hirak Ranjan Dash, editors. Handbook of metal-microbe interactions and bioremediation. Boca Raton, FL, USA: CRC Press, Tailor and Francis Group; 2017. p. 201.
   Google Scholar
• Inouhe M. Phytochelatins. Braz J Plant Physiol. 2005;17:65–78.
   Google Scholar
• Ha SB, Smith AP, Howden R, et al. Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell. 1999;11:1153–1164.
   PubMed Web of Science ®Google Scholar
• Tsuji N, Nishikori S, Iwabe O, et al. Comparative analysis of the two-step reaction catalyzed by prokaryotic and eukaryotic phytochelatin synthase by an ion-pair liquid chromatography assay. Planta. 2005;222:181–191.
   PubMed Web of Science ®Google Scholar
• Vatamaniuk OK, Mari S, Lang A, et al. Phytochelatin synthase, a dipeptidyltransferase that undergoes multisite acylation with γ-glutamylcysteine during catalysis. J Biol Chem. 2004;279:22449–22460.
   PubMed Web of Science ®Google Scholar
• Cobbett CS. Phytochelatins and their roles in heavy metal detoxification. Plant Physiol. 2000;123:825–832.
   PubMed Web of Science ®Google Scholar
• Maier T, Yu C, Kullertz G, et al. Localization and functional characterization of metal-binding sites in phytochelatin synthases. Planta. 2003;218:300–308.
   PubMed Web of Science ®Google Scholar
• Romanyuk ND, Rigden DJ, Vatamaniuk OK, et al. Mutagenic definition of a papain-like catalytic triad, sufficiency of the N-terminal domain for single-site core catalytic enzyme acylation, and C-terminal domain for augmentative metal activation of a eukaryotic phytochelatin synthase. Plant Physiol. 2006;141:858–869.
   PubMed Web of Science ®Google Scholar
• Wang F, Wang Z, Zhu C. Heteroexpression of the wheat phytochelatin synthase gene (TaPCS1) in rice enhances cadmium sensitivity. Acta Bioch Bioph Sin. 2012;44:886–893.
   PubMed Web of Science ®Google Scholar
• Li JC, Guo JB, Xu WZ, et al. RNA interference-mediated silencing of phytochelatin synthase gene reduce cadmium accumulation in rice seeds. J Integr Plant Biol. 2007;49:1032–1037.
   Web of Science ®Google Scholar
• Vatamaniuk OK, Mari S, Lu YP, et al. AtPCS1, a phytochelatin synthase from Arabidopsis: isolation and in vitro reconstitution. Proc Natl Acad Sci USA. 1999;96:7110–7115.
   PubMed Web of Science ®Google Scholar
• Heiss S, Wachter A, Bogs J, et al. Phytochelatin synthase (PCS) protein is induced in Brassica juncea leaves after prolonged Cd exposure. J Exp Bot. 2003;54:1833–1839.
   PubMed Web of Science ®Google Scholar
• Meyer CL, Peisker D, Courbot M, et al. Isolation and characterization of Arabidopsis halleri and Thlaspi caerulescens phytochelatin synthases. Planta. 2011;234:83–95.
   PubMed Web of Science ®Google Scholar
• Clemens S, Kim EJ, Neumann D, et al. Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. EMBO J. 1999;18:3325–3333.
   PubMed Web of Science ®Google Scholar
• Clemens S, Schroeder JI, Degenkolb T. Caenorhabditis elegans expresses a functional phytochelatin synthase. Eur J Biochem. 2001;268:3640–3643.
   PubMedGoogle Scholar
• Lee S, Korban S. Transcriptional regulation of Arabidopsis thaliana phytochelatin synthase (AtPCS1) by cadmium during early stages of plant development. Planta. 2002;215:689–693.
   PubMed Web of Science ®Google Scholar
• Semane B, Cuypers A, Smeets K, et al. Cadmium responses in Arabidopsis thaliana: glutathione metabolism and antioxidative defence system. Physiol Plant. 2007;129:519–528.
   Web of Science ®Google Scholar
• Gasic K, Korban SS. Expression of Arabidopsis phytochelatin synthase in Indian mustard (Brassica juncea) plants enhances tolerance for Cd and Zn. Planta. 2007;225:1277–1285.
   PubMed Web of Science ®Google Scholar
• Ramos J, Clemente MR, Naya L, et al. Phytochelatin synthases of the model legume Lotus japonicus. A small multigene family with differential response to cadmium and alternatively spliced variants. Plant Physiol. 2007;143:1110–1118.
   PubMed Web of Science ®Google Scholar
• Lee BD, Hwang S. Tobacco phytochelatin synthase (NtPCS1) plays important roles in cadmium and arsenic tolerance and in early plant development in tobacco. Plant Biotechnol Rep. 2015;9:107–114.
   Web of Science ®Google Scholar
• Tennstedt P, Peisker D, Bottcher C, et al. Phytochelatin synthesis is essential for the detoxification of excess zinc and contributes significantly to the accumulation of zinc. Plant Physiol. 2008;149:938–948.
   PubMed Web of Science ®Google Scholar
• Mendoza-Cózatl DG, Springer F, et al. Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus. A role for thiol-peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant J. 2008;54:249–259.
   PubMed Web of Science ®Google Scholar
• Clemens S. Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie. 2006;88:707–1719.
   Web of Science ®Google Scholar
• Blum R, Meyer KC, Wunschmann J, et al. Cytosolic action of phytochelatin synthase. Plant Physiol. 2010;153:159–169.
   PubMed Web of Science ®Google Scholar
• Clay NK, Adio AM, Denoux C, et al. Glucosinolate metabolites required for an Arabidopsis innate immune response. Science. 2009;323:95–101.
   PubMed Web of Science ®Google Scholar
• DalCorso G. Heavy metal toxicity in plants. In: Antonella Furini, editor. Plants and heavy metals. Netherlands: Springer; 2012. p.1–25.
   Google Scholar
• UniProt Consortium. UniProt: the universal protein knowledgebase. Nucleic Acids Res. 2017;45:D158–D169. https://www.uniprot.org/help/publications
   PubMed Web of Science ®Google Scholar
• Phytozome, The Plant Comparative Genomics Portal. The Regents of the University of California; c.1997–2017 [Accessed 2018]. Available from: https://phytozome.jgi.doe.gov/pz/portal.html
   Google Scholar
• Goodstein DM, Shu S, Howson R, et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 2012;40:1178–1186.
   PubMed Web of Science ®Google Scholar
• El-Gebali S, Mistry J, Bateman A, et al. The Pfam protein families database in 2019. Nucleic Acids Res. Forthcoming 2019:gky995. DOI:10.1093/nar/gky995, https://pfam.xfam.org/
   Google Scholar
• Punta M, Coggill PC, Eberhardt RY, et al. The Pfam protein families database. Nucleic Acids Res. 2012;44:D279–D285.
   Google Scholar
• Gasteiger E, Hoogland C, Gattiker A, et al. Protein identification and analysis tools on the ExPASy server. In: Walker JM, editor. The proteomics protocols handbook. Louisville, KY (USA): Humana; 2005. p. 571–607.
   Google Scholar
• Yu CS, Chen YC, Lu CH, et al. Prediction of protein subcellular localization. Proteins. 2006; 64:643–651.
   PubMed Web of Science ®Google Scholar
• Motif-based analysis of DNA, RNA and protein sequences. 2018. Available from: http://meme-suite.org/tools/meme
   Google Scholar
• Timothy L, Mikael B, Buske FA, et al. Meme Suite: tools for motif discovery and searching. Nucleic Acids Res. 2009;37:202–208.
   Web of Science ®Google Scholar
• Thompson JD, Higgins DG, Gibson TJ. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673–4680.
   PubMed Web of Science ®Google Scholar
• Kumar S, Stecher G, Tamura K. Mega7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;3:1870–1874.
   Google Scholar
• Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 1992;8:275–282.
   PubMedGoogle Scholar
• Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39:783–791.
   PubMed Web of Science ®Google Scholar
• PlantCARE, a database of plant cis-acting regulatory elements and a portal. 2018. Available from: http://bioinformatics.psb.ugent.be/webtools/plantcare/html/
   Google Scholar
• Lescot M, Déhais P, Thijs G, et al. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002;30:325–327.
   PubMed Web of Science ®Google Scholar
• A Plant Small RNA Target Analysis Server. 2018. Available from: https://plantgrn.noble.org/psRNATarget/
   Google Scholar
• Dai X, Zhuang Z, Zhao PX. psRNATarget: a plant small RNA target analysis server (2017 release). Nucleic Acids Res. 2018;46:W49–W54.
   PubMed Web of Science ®Google Scholar
• Gene coexpression database. 2018. Available from: http://atted.jp/
   Google Scholar
• Aoki Y, Okamura Y, Tadaka S, et al. ATTED-II in 2016: a plant coexpression database towards lineage-specific coexpression. Plant Cell Physiol. 2016;57:e5.
   PubMed Web of Science ®Google Scholar
• Obayashi T, Okamura Y, Ito S, et al. ATTED-II in 2014: evaluation of gene co-expression in agriculturally important plants. Plant Cell Physiol. 2014;55:e6. [7. [cited 2018 Sep 19] p.] DOI: 10.1093/pcp/pct178
   Google Scholar
• Structural Bioinformatics Group - Imperial College London.2018. Protein Homology/analogY Recognition Engine V 2.0. Available from: http://www.sbg.bio.ic.ac.uk/phyre2/html/page.cgi?id+index
   Google Scholar
• Kelley LA, Mezulis S, Yates CM, et al. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc. 2015;10:845.
   PubMed Web of Science ®Google Scholar
• Ramachandran Plot Analysis. 2018. Available from: http://mordred.bioc.cam.ac.uk/∼rapper/rampage.php
   Google Scholar
• Single (or Multiple) Model Protein Structure Analysis - Volume, Area, Dihedral Angle Reporter. 2018. Available from: http://vadar.wishartlab.com/
   Google Scholar
• Willard L, Ranjan A, Zhang H, et al. Vadar: a web server for quantitative evaluation of protein structure quality. Nucleic Acids Res. 2003;31:3316–3319.
   PubMed Web of Science ®Google Scholar
• Topology Independent Comparison of Biomolecular 3D Structures. 2018. Available from: http://mspc.bii.a-star.edu.sg/minhn/pairwise.html
   Google Scholar
• Nguyen MN, Tan KP, Madhusudhan MS. CLICK - Topology-independent comparison of biomolecular 3D structures. Nucleic Acids Res. 2011;39:W24–W28.
   PubMed Web of Science ®Google Scholar
• Xu L, Zhu L, Tu L, et al. Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. J Exp Bot. 2011;62:5607–5621.
   PubMed Web of Science ®Google Scholar
• Lorkovic ZJ, Wieczorek KDA, Lambermon MHL, et al. Pre-mRNA splicing in higher plants. Trends Plant Sci. 2000;5:160–167.
   PubMed Web of Science ®Google Scholar
• Das N, Bhattacharya S, Bhattacharyya S, et al. Identification of alternatively spliced transcripts of rice phytochelatin synthase 2 gene OsPCS2 involved in mitigation of cadmium and arsenic stresses. Plant Mol Biol. 2017;94:167–183.
   PubMed Web of Science ®Google Scholar
• Uraguchi S, Tanaka N, Hofmann C, et al. Phytochelatin synthase has contrasting effects on cadmium and arsenic accumulation in rice grains. Plant Cell Physiol. 2017;58:1730–1742.
   PubMed Web of Science ®Google Scholar
• Ashburner M, Ball CA, Blake JA, et al. Gene ontology: tool for the unification of biology. Nat Genet. 2000;25:25–29.
   PubMed Web of Science ®Google Scholar
• Kuhnlenz T, Westphal L, Schmidt H, et al. Expression of Caenorhabditis elegans PCS in the AtPCS1-deficient Arabidopsis thaliana cad1-3 mutant separates the metal tolerance and non-host resistance functions of phytochelatin synthases. Plant Cell Environ. 2015;38:2239–2247.
   PubMed Web of Science ®Google Scholar
• De Benedictis M, Brunetti C, Brauer EK, et al. The Arabidopsis thaliana knockout mutant for phytochelatin synthase1 (cad1-3) is defective in callose deposition, bacterial pathogen defense and auxin content. Front Plant Sci. 2018;9:19.
   PubMed Web of Science ®Google Scholar
• Zheng H, Bassham DC, da Silva Conceição A, et al. The syntaxin family of proteins in Arabidopsis: a new syntaxin homologue shows polymorphism between two ecotypes. J Exp Bot. 1999;50:915–924.
   Web of Science ®Google Scholar
• Eisenach C, Chen ZH, Grefen C, et al. The trafficking protein SYP121 of Arabidopsis connects programmed stomatal closure and K+ channel activity with vegetative growth. Plant J. 2012;69:241–251.
   PubMed Web of Science ®Google Scholar
• Joshi CP, Chiang VL. Conserved sequence motifs in plant S-adenosyl-L-methionine-dependent methyltransferases. Plant Mol Biol. 1998;37:663–674.
   PubMed Web of Science ®Google Scholar
• Lewis JD, Wu R, Guttman DS, et al. Allele-specific virulence attenuation of the Pseudomonas syringae HopZ1a type III effector via the Arabidopsis ZAR1 resistance protein. PLoS Genet. 2010;6:e1000894.
   PubMed Web of Science ®Google Scholar
• Devoto A, Hartmann HA, Piffanelli P, et al. Molecular phylogeny and evolution of the plant-specific seven-transmembrane MLO family. J Mol Evol. 2003;56:77–88.
   PubMed Web of Science ®Google Scholar
• Miao LX, Jiang M, Zhang YC, et al. Genomic identification, phylogeny, and expression analysis of MLO genes involved in susceptibility to powdery mildew in Fragaria vesca. Genet Mol Res. 2016;15:1–12.
   Web of Science ®Google Scholar
• Valmonte GR, Arthur K, Higgins CM, et al. Calcium-dependent protein kinases in plants: evolution, expression and function. Plant Cell Physiol. 2014;55:551–569.
   PubMed Web of Science ®Google Scholar
• AlbertŠ, WE, Gallwitz D. Identification of the catalytic domains and their functionally critical arginine residues of two yeast GTPase-activating proteins specific for Ypt/Rab transport GTPases. EMBO J. 1999;18:5216–5225.
   PubMed Web of Science ®Google Scholar
• Lee JH, Jung JH, Park CM. Light inhibits COP1-mediated degradation of ICE transcription factors to induce stomatal development in Arabidopsis. Plant Cell. 2017;29:2817–2830.
   PubMed Web of Science ®Google Scholar
• McAtee P, Karim S, Schaffer RJ, et al. A dynamic interplay between phytohormones is required for fruit development, maturation, and ripening. Front Plant Sci. 2013;4:79.
   PubMed Web of Science ®Google Scholar
• Yadav SK. Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot. 2010;76:167–179.
   Web of Science ®Google Scholar
• Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116:281–297.
   PubMed Web of Science ®Google Scholar
• Lv S, Nie X, Wang L, et al. Identification and characterization of MicroRNAs from barley (Hordeum vulgare L.) by high-throughput sequencing. Int J Mol Sci. 2012;13:2973–2984.
   PubMed Web of Science ®Google Scholar
• Ding Y, Chen Z, Zhu C. Microarray-based analysis of cadmium responsive microRNAs in rice (Oryza sativa). J Exp Bot. 2011;62:3563–3573.
   PubMed Web of Science ®Google Scholar
• Zhang LW, Song JB, Shu XX, et al. miR395 is involved in detoxification of cadmium in Brassica napus. J Hazard Mater. 2013;250:204–211.
   PubMed Web of Science ®Google Scholar
• Zhou ZS, Song JB, Yang ZM. Genome-wide identification of Brassica napus microRNAs and their targets in response to cadmium. J Exp Bot. 2012;63:4597–4613.
   PubMed Web of Science ®Google Scholar
• Xu L, Wang Y, Zhai L, et al. Genome-wide identification and characterization of cadmium-responsive microRNAs and their target genes in radish (Raphanus sativus L.) roots. J Exp Bot. 2013; 64:4271–4287.
   PubMed Web of Science ®Google Scholar
• Fang X, Zhao Y, Ma Q, et al. Identification and comparative analysis of cadmium tolerance-associated miRNAs and their targets in two soybean genotypes. PLoS One. 2013;8:e81471.
   PubMed Web of Science ®Google Scholar
• Huang SQ, Xiang AL, Che LL, et al. A set of miRNAs from Brassica napus in response to sulfate deficiency and cadmium stress. Plant Biotechnol J. 2010;8:887–899.
   PubMed Web of Science ®Google Scholar
• Zhou ZS, Zeng HQ, Liu ZP, et al. Genome-wide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal. Plant Cell Environ. 2012;35:86–99.
   PubMed Web of Science ®Google Scholar
• Yang ZM, Chen J. A potential role of microRNAs in plant response to metal toxicity. Metallomics. 2013;5:1184–1190.
   PubMed Web of Science ®Google Scholar
• Thorne JL, Goldman N, Jones DT. Combining protein evolution and secondary structure. Mol Biol Evol. 1996;13:666–673.
   PubMed Web of Science ®Google Scholar
• Goldman N, Thorne JL, Jones DT. Assessing the impact of secondary structure and solvent accessibility on protein evolution. Mol Biol Evol. 1999;149:445–458.
   Google Scholar
• Lio P, Goldman N. Using protein structural information in evolutionary inference: transmembrane proteins. Mol Biol Evol. 1999;16:1696–1710.
   PubMed Web of Science ®Google Scholar