In collaboration with Payame Noor University and Iranian Biotechnology Society

Document Type : Research Paper

Authors

1 Ph.D student, Department of Agricultural Biotechnology, Faculty of Agricultural Sciences, University of Guilan, Rasht, Iran

2 Assistant Professor, Department of Agricultural Biotechnology, Faculty of Agricultural Sciences, University of Guilan, Rasht, Iran

3 Associate Professor, Department of Agricultural Biotechnology, Faculty of Agricultural Sciences, University of Guilan, Rasht, Iran

Abstract

Strictosidine synthase is a key enzyme in the monoterpenoid indole alkaloids biosynthesis pathway. Proteins with Str_synth domain have been identified in plants, bacteria, insects and even mammalians and called Strictosidine synthase-like due to unknown functional roles. With the Arabidopsis and rice genome sequence completed, SSL genes were also identified in these plants. However, little is known about evolutionary path, gene structure, expansion and function of SSL family in rice. In this study, through bioinformatic analysis, a total of 23 SSL genes were identified in rice genome. A phylogenetic analysis of the SSL genes in rice and Arabidopsis clarified that these genes could be divided into four different groups and the evolutionary paths are different in rice and Arabidopsis. The OsSSL genes contained zero to five introns and were distributed across 10 out of 12 chromosomes at different densities and tandem duplication was a major cause in expanding this family. Promoter analysis showed the presence of several cis-regulatory elements related to stress and hormone response in regulatory region, indicating probable their role in stress response. Microarray-based expression analysis of OsSSL genes indicated that a few number of these genes were widely expressed in various tissues and also in response to some abiotic stresses. This study is the first report about SSL gene family in rice and provides a framework for further analysis of the biological functions of SSL genes in either rice or other crops.

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Main Subjects

Artimo P, Jonnalagedda M, Arnold K, Baratin D, Csardi G, De Castro E, Duvaud S, Flegel V, Fortier A, Gasteiger E (2012) ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res. 40: W597–W603.
Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer EL (2004) The Pfam protein families database. Nucleic Acids Res. 32: D138-D141.
Bolstad B (2005) RMAExpress. RMAExpress. html. View Article PubMed/NCBI Google Scholar
Brown S, Clastre M, Courdavault V, O’Connor SE (2015) De novo production of the plant-derived alkaloid strictosidine in yeast. Proc. Natl. Acad. Sci. U. S. A. 112 (11): 3205-3210.
Cao J, Li M, Chen J, Liu P,  Li Z (2016) Effects of MeJA on Arabidopsis metabolome under endogenous JA deficiency. Sci. Rep. 6: 37674.
Chaw SM, Chang CC, Chen HL, Li WH (2003) Dating the Monocot–Dicot Divergence and the Origin of Core Eudicots Using Whole Chloroplast Genomes. J. Mol. Evol. 58(4): 424–441.
Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant. Biol. 61: 651-679.
Dobritsa AA, Nishikawa SI, Preuss D, Urbanczyk-Wochniak E, Sumner LW, Hammond A, Carlson AL, Swanson RJ (2009) LAP3, a novel plant protein required for pollen development, is essential for proper exine formation. Sex. Plant Reprod. 22 (3): 167-177.
Dong  CJ, Shang QM. (2013). Genome-wide characterization of phenylalanine ammonia-lyase gene family in watermelon (Citrullus lanatus). Planta. 238(1): 35-49.
Dutta A, Sen J, Deswal R (2013) New evidences about strictosidine synthase (Str) regulation by salinity, cold stress and nitric oxide in Catharanthus roseus. J. Plant Biochem. Biotechnol. 22(1): 124-131.
Fabbri M, Delp G, Schmidt O, Theopold U (2000) Animal and plant members of a gene family with similarity to alkaloid-synthesizing enzymes. Biochem. Biophys. Res. Commun. 271(1): 191-196.
Facchini PJ (2001) Alkaloid biosynthesis in plants: biochemistry, cell biology, molecular regulation, and metabolic engineering applications. Annu. Rev. Plant Biol. 52 (1): 29-66
Facchini PJ, Bird DA, St-Pierre B (2004) Can Arabidopsis make complex alkaloids? Trends Plant Sci. 9(3): 116-122.
Felsenstein J (1985) Confidence Limits on Phylogenies: An Approach Using the Bootstrap. Evolution. 39 (4): 783-791.
Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J (2014) Pfam: the protein families database. Nucleic Acids Res. 42: D222-230.
Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 39: W29–W37.
Fujita M, Horiuchi Y, Ueda Y, Mizuta Y, Kubo T, Yano K, Yamaki S, Tsuda K, Nagata T, Niihama M (2010) Rice expression atlas in reproductive development. Plant Cell Physiol. 51 (12): 2060-2081.
Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40: D1178-D1186.
Guo J, Wu J, Ji Q, Wang C, Luo L, Yuan Y, Wang Y, Wang J (2008) Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis. J. Genet. Genomics. 35 (2): 105-118.
Hanada K, Zou C, Lehti-Shiu MD, Shinozaki K, Shiu S-H (2008) Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiol. 148 (2): 993-1003.
Hicks MA, Barber AE, Giddings LA, Caldwell J, O'Connor SE, Babbitt PC (2011) The evolution of function in strictosidine synthase-like proteins. Proteins: Struct., Funct., Bioinf. 79 (11): 3082-3098.
Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2014) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics. 31 (8): 1296-1297.
Huang W, Xian Z, Kang X, Tang N, Li Z (2015) Genome-wide identification, phylogeny and expression analysis of GRAS gene family in tomato. BMC Plant Biol. 15 (1): 209.
Ibraheem O, Botha CE, Bradley G (2010) In silico analysis of cis-acting regulatory elements in 5′ regulatory regions of sucrose transporter gene families in rice (Oryza sativa Japonica) and Arabidopsis thaliana. Comput. Biol. Chem. 34 (5): 268-283.
Kibble NA, Sohani MM, Shirley N, Byrt C, Roessner U, Bacic A, Schmidt O, Schultz CJ (2009) Phylogenetic analysis and functional characterisation of strictosidine synthase-like genes in Arabidopsis thaliana. Funct. Plant Biol. 36 (12): 1098-1109.
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33(7): 1870-1874.
Larkin MA, Blackshields G, Brown N, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R (2007) Clustal W and Clustal X version 2.0. Bioinformatics. 23(21): 2947-2948.
Lee T-H, Tang H, Wang X, Paterson AH (2013) PGDD: a database of gene and genome duplication in plants. Nucleic Acids Res. 41: D1152-D1158.
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 30: 325-327.
Liu T, Zeng J, Xia K, Fan T, Li Y, Wang Y, Xu X, Zhang M (2012) Evolutionary expansion and functional diversification of oligopeptide transporter gene family in rice. Rice. 5(1): 12.
Liu Z, Zhang M, Kong L, Lv Y, Zou M, Lu G, Cao J, Yu X (2014) Genome-Wide Identification, Phylogeny, Duplication, and Expression Analyses of Two-Component System Genes in Chinese Cabbage (Brassica rapa ssp. pekinensis). DNA Res. 21(4): 379–396.
Ma X, Panjikar S, Koepke J, Loris E, Stöckigt J (2006) The structure of Rauvolfia serpentina strictosidine synthase is a novel six-bladed β-propeller fold in plant proteins. The Plant Cell. 18 (4): 907-920.
Magadum S, Banerjee U, Murugan P, Gangapur D, Ravikesavan R (2013) Gene duplication as a major force in evolution. J. Genet. 92 (1): 155-161.
Memelink J, Gantet P (2007) Transcription factors involved in terpenoid indole alkaloid biosynthesis in Catharanthus roseus. Phytochem. Rev. 6: 353-362.
Menke FL, Champion A, Kijne JW, Memelink J (1999) A novel jasmonate-and elicitor-responsive element in the periwinkle secondary metabolite biosynthetic gene Str interacts with a jasmonate-and elicitor-inducible AP2-domain transcription factor, ORCA2. The EMBO Journal. 18(16): 4455-4463.
Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol. 140 (2): 411-432.
O'Connor SE, Maresh JJ (2006) Chemistry and biology of monoterpene indole alkaloid biosynthesis. Nat. Prod. Rep. 23(4): 532-547.
Pan Q, Mustafa NR, Tang K, Choi YH, Verpoorte R (2016) Monoterpenoid indole alkaloids biosynthesis and its regulation in Catharanthus roseus: a literature review from genes to metabolites Phytochem. Rev. 15(2): 221-250.
Pandey A, Misra P, Alok A, Kaur N, Sharma S, Lakhwani D, Asif MH, Tiwari S, Trivedi PK (2016) Genome-Wide Identification and Expression Analysis of Homeodomain Leucine Zipper Subfamily IV (HDZ IV) Gene Family from Musa accuminata. Front Plant Sci. 7: 20.
Pasquali G, Goddijn OJ, de Waal A, Verpoorte R, Schilperoort RA, Hoge JHC, Memelink J (1992) Coordinated regulation of two indole alkaloid biosynthetic genes from Catharanthus roseus by auxin and elicitors. Plant Mol. Biol. 18 (6): 1121-1131.
Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A (2009) The Sorghum bicolor genome and the diversification of grasses. Nature. 457 (7229): 551-556.
Schmidt O, Söderhäll K, Theopold U, Faye I (2010) Role of adhesion in arthropod immune recognition. Annu. Rev. Entomol. 55: 485-504.
Sharp PA (1981) Speculations on RNA splicing (minireview). Cell. 23(643): 621.
Singh AK, Kumar R, Tripathi AK, Gupta BK, Pareek A, Singla-Pareek SL (2015) Genome-wide investigation and expression analysis of Sodium/Calcium exchanger gene family in rice and Arabidopsis. Rice. 8(1): 21.
Singh AK, Sharma V, Pal AK, Acharya V, Ahuja PS (2013) Genome-wide organization and expression profiling of the NAC transcription factor family in potato (Solanum tuberosum L.). DNA Res. 20 (4): 403-423.
Sohani M, Schenk P, Schultz CJ, Schmidt O (2009) Phylogenetic and transcriptional analysis of a strictosidine synthase-like gene family in Arabidopsis thaliana reveals involvement in plant defence responses. Plant Biol. 11(1): 105-117.
Stöckigt J, Barleben L, Panjikar S, Loris EA (2008) 3D-Structure and function of strictosidine synthase–the key enzyme of monoterpenoid indole alkaloid biosynthesis. Plant Physiol. Biochem. 46 (3): 340-355.
Theopold U, Samakovlis C, Erdjument-Bromage H, Dillon N, Axelsson B, Schmidt O, Tempst P, Hultmark D (1996) Helix pomatia lectin, an inducer of Drosophila immune response, binds to hemomucin, a novel surface mucin. J. Biol. Chem. 271 (22): 12708-12715.
Wei K-F, Chen J, Chen Y-F, Wu L-J, Xie D-X (2012) Molecular phylogenetic and expression analysis of the complete WRKY transcription factor family in maize. DNA Res. 19(2):153-164.
Xu G, Guo C, Shan H, Kong H (2011) Divergence of duplicate genes in exon–intron structure. Proc. Natl. Acad. Sci. U. S. A. 109(4): 1187–1192.
Yoshida S, Ito M, Nishida I, Watanabe A (2001) Isolation and RNA gel blot analysis of genes that could serve as potential molecular markers for leaf senescence in Arabidopsis thaliana. Plant Cell Physiol. 42(2): 170-178.
Yu CS, Chen YC, Lu CH, Hwang JK (2006) Prediction of protein subcellular localization. Proteins: Struct., Funct., Bioinf.  64(3): 643-651.
Zhang Y, Gao M, Singer SD, Fei Z, Wang H, Wang X. (2012) Genome-Wide Identification and Analysis of the TIFY Gene Family in Grape. PLoS One. 7(9): e44465.