Characterization of the caleosin gene family in the Triticeae

BMC Genomics

Patrick J Gulick¹  André Laroche²  Deborah Maret¹  Uyen Minh Pham¹  Sabrina C Brunetti¹  Hala Badr Khalil³ 

[1]Biology Department, Concordia University, 7141 Sherbrooke W, Montreal, QC H4B 1R6, Canada

[2]Agriculture and Agri-Food Canada, Lethbridge Research Centre, 5403, 1st Avenue South, C.P. 3000, Lethbridge, AB T1J 4B1, Canada

[3]Present address: Department of Genetics, Faculty of Agriculture, Ain-Shams University, Shoubra El-khema, Cairo, Egypt

关键词: RNA-seq;    Heterotrimeric G protein signaling;    Gα;    GAP;    Tissue-specific expression;    Phylogenetic analysis;    Calcium-binding protein;    Caleosin gene family;   

Others  :  1217603
DOI  :  10.1186/1471-2164-15-239

 received in 2013-03-28, accepted in 2014-02-22,  发布年份 2014

【 摘 要 】

Background

The caleosin genes encode proteins with a single conserved EF hand calcium-binding domain and comprise small gene families found in a wide range of plant species. Some members of the gene family have been shown to be upregulated by environmental stresses including low water availability and high salinity. Caleosin 3 from wheat has been shown to interact with the α-subunit of the heterotrimeric G proteins, and to act as a GTPase activating protein (GAP). This study characterizes the size and diversity of the gene family in wheat and related species and characterizes the differential tissue-specific expression of members of the gene family.

Results

A total of 34 gene family members that belong to eleven paralogous groups of caleosins were identified in the hexaploid bread wheat, T. aestivum. Each group was represented by three homeologous copies of the gene located on corresponding homeologous chromosomes, except the caleosin 10, which has four gene copies. Ten gene family members were identified in diploid barley, Hordeum vulgare, and in rye, Secale cereale, seven in Brachypodium distachyon, and six in rice, Oryza sativa. The analysis of gene expression was assayed in triticale and rye by RNA-Seq analysis of 454 sequence sets and members of the gene family were found to have diverse patterns of gene expression in the different tissues that were sampled in rye and in triticale, the hybrid hexaploid species derived from wheat and rye. Expression of the gene family in wheat and barley was also previously determined by microarray analysis, and changes in expression during development and in response to environmental stresses are presented.

Conclusions

The caleosin gene family had a greater degree of expansion in the Triticeae than in the other monocot species, Brachypodium and rice. The prior implication of one member of the gene family in the stress response and heterotrimeric G protein signaling, points to the potential importance of the caleosin gene family. The complexity of the family and differential expression in various tissues and under conditions of abiotic stress suggests the possibility that caleosin family members may play diverse roles in signaling and development that warrants further investigation.

【 授权许可】

   
2014 Khalil et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Khalil HB, Wang Z, Wright JA, Ralevski A, Donayo AO, Gulick PJ: Heterotrimeric Gα subunit from wheat (Triticum aestivum), GA3, interacts with the calcium-binding protein, Clo3, and the phosphoinositide-specific phospholipase C, PI-PLC1. Plant Mol Biol 2011, 77:145-158.
• [2]Takahashi S, Takeshi K, Yamaguchi-Shinozaki K, Shinozaki K: An Arabidopsis gene encoding a Ca2 + −binding protein is induced by abscisic acid during dehydration. Plant Cell Physiol 2000, 41:898-903.
• [3]Aubert Y, Vile D, Pervent M, Aldon D, Ranty B, Simonneau T, Vavasseur A, Galaud JP: RD20, a stress-inducible caleosin, participates in stomatal control, transpiration and drought tolerance in Arabidopsis thaliana. Plant Cell Physiol 2010, 51:1975-1987.
• [4]Liu H, Hedley P, Cardle L, Wright KM, Hein I, Marshall D, Waugh R: Characterisation and functional analysis of two barley caleosins expressed during barley caryopsis development. Planta 2005, 221:513-522.
• [5]Chiang CJ, Che CJ, Lin LJ, Chang C, Chao YP: Selective delivery of cargo entities to tumor cells by nanoscale artificial oil bodies. J Agric Food Chem 2010, 58:11695-702.
• [6]Huang S, Sirikhachornkit A, Su X, Faris J, Gill B, Haselkorn R, Gornicki P: Genes encoding plastid acetyl-CoA carboxylase and 3-phosphoglycerate kinase of the Triticum/Aegilops complex and the evolutionary history of polyploid wheat. Proc Natl Acad Sci U S A 2002, 99:8133-8.
• [7]Mergoum M, Singh PK, Pena RJ, Lozano-del Rio AJ, Cooper KV, Salmon DF, Gómez Macpherson H: Triticale: a 'new' crop with old challenges. In Cereals. Vol. 3. Edited by Carena MJ. New York: Springer; 2009:267-290.
• [8]Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
• [9]Huang X, Madan A: CAP3: A DNA sequence assembly program. Genome Res 1999, 9:868-77.
• [10]ExPASy Translate Tool http://web.expasy.org/translate/ webcite
• [11]International Wheat Genome Sequencing Consortium [http://www.wheatgenome.org/Tools-and-Resources webcite]
• [12]International Barley Sequencing Consortium http://webblast.ipk-gatersleben.de/barley/viroblast.php webcite
• [13]Brachypodium database http://brachypodium.org/ webcite
• [14]NCBI Batch Conserved Domain Search tool [http://www.ncbi.nlm.nih.gov/Structure/bwrpsb/bwrpsb.cgi webcite]
• [15]RCSB Protein Data Bank http://www.rcsb.org/pdb/home/home.do webcite
• [16]InterPro Scan Sequence Search. European Bioinformatics Institute, 2011 http://www.ebi.ac.uk/Tools/pfa/iprscan/ webcite
• [17]Simple Modular Architecture Research Tool (SMART) http://smart.embl-heidelberg.de/ webcite
• [18]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
• [19]Steel MA, Fu YX: Classifying and counting linear phylogenetic invariants for the Jukes-Cantor model. J Comput Biol 1995, 2:39-47.
• [20]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acid Res 2004, 32(5):1792-7.
• [21]Whelan S, Goldman N: A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 2001, 18:691-9.
• [22]Gramene database [http://www.gramene.org webcite, August 2013]
• [23]Tran F, Penniket C, Patel RV, Provart NJ, Laroche A, Rowland O, Robert LS: Developmental transcriptional profiling reveals key insights into Triticeae reproductive development. Plant J 2013, 74:971-988.
• [24]Zadoks JC, Chang TT, Konzak CF: A decimal code for the growth stages of cereals. Weed Res 1974, 14:415-421.
• [25]Gulick P, Dvorák J: Gene induction and repression by salt treatment in roots of the salinity-sensitive Chinese Spring wheat and the salinity-tolerant Chinese Spring x Elytrigia elongata amphiploid. Proc Natl Acad Sci U S A 1987, 84(1):99-103.
• [26]Comeau A, Nodichao L, Collin J, Baum M, Samsatly J, Hamidou D, Langevin F, Laroche A, Picard E: New approaches for the study of osmotic stress induced by polyethylene glycol (PEG) in cereal species. Cereal Res Commun 2010, 38:471-481.
• [27]Goecks J, Nekrutenko A, Taylor J: Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 2010, 11:R86. BioMed Central Full Text
• [28]Fu L, Niu B, Zhu Z, Wu S, Li W: CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 2012, 28:3150-2.
• [29]Schreiber AW, Sutton T, Caldo RA, Kalashyan E, Lovell B, Mayo G, Muehlbauer GJ, Druka A, Waugh R, Wise RP, Langridge P, Baumann U: Comparative transcriptomics in the Triticeae. BMC Genomics 2009, 10:285. BioMed Central Full Text
• [30]Druka A, Muehlbauer G, Druka I, Caldo R, Bauman U, Rostoks N, Schreiber A, Wise R, Close T, Kleninhofs A, Graner A, Schulman A, Langridge P, Sato K, Hayes P, McNicol J, Marshall D, Waugh R: An atlas of gene expression from seed to seed through barley development. Funct Integr Genomics 2006, 6:202-211.
• [31]PLEXdb database [http://www.plexdb.org webcite]
• [32]Monroy AF, Dryanova A, Malette B, Oren DH, Ridha Farajalla M, Liu W, Danyluk J, Ubayasena LW, Kane K, Scoles GJ, Sarhan F, Gulick PJ: Regulatory gene candidates and gene expression analysis of cold acclimation in winter and spring wheat. Plant Mol Biol 2007, 64(4):409-23.
• [33]Aprile A, Mastrangelo AM, De Leonardis AM, Galiba G, Roncaglia E, Ferrari F, De Bellis L, Turchi L, Giuliano G, Cattivelli L: Transcriptional profiling in response to terminal drought stress reveals differential responses along the wheat genome. BMC Genomics 2009, 10:279. BioMed Central Full Text
• [34]ClustalW2- Multiple Sequence Alignment [www.ebi.ac.uk/Tools/msa/clustalw2/ webcite]
• [35]Farajalla R, Gulick PJ: The alpha-tubulin gene family in wheat (Triticum aestivum L.) and differential gene expression during cold acclimation. Genome 2007, 50(5):502-10.
• [36]Miftahudin RK, Ma XF, Mahmoud AA, Layton J, Milla MA, Chikmawati T, Ramalingam J, Feril O, Pathan MS, Momirovic GS, Kim S, Chema K, Fang P, Haule L, Struxness H, Birkes J, Yaghoubian C, Skinner R, McAllister J, Nguyen V, Qi LL, Echalier B, Gill BS, Linkiewicz AM, Dubcovsky J, Akhunov ED, Dvorák J, Dilbirligi M, Gill KS, Peng JH, et al.: Analysis of expressed sequence tag loci on wheat chromosome group 4. Genetics 2004, 168:651-663.
• [37]Riaño-Pachón DM, Nagel A, Neigenfind J, Wagner R, Basekow R, Weber E, Mueller-Roeber B, Diehl S, Kersten B: GabiPD: the GABI primary database – a plant integrative ‘omics‘ database. Nucleic Acids Res 2009, 37(Database issue):D954-9.
• [38]The Arabidopsis Information Resource (TAIR) [http://www.arabidopsis.org/ webcite]
• [39]Brenchley R, Spannagl M, Pfeifer M, Barker GL, D’Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser D, Kay S, Waite D, Trick M, Bancroft I, Gu Y, Huo N, Luo MC, Sehgal S, Gill B, Kianian S, Anderson O, Kersey P, Dvorak J, McCombie WR, Hall A, Mayer KF, Edwards KJ, Bevan MW, Hall N: Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 2012, 491(7426):705-10.
• [40]Arabidopsis Genome Initiative: Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 2000, 408:796-815.
• [41]Kim MC, Chung WS, Yun DJ, Cho MJ: Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2009, 2:13-21.
• [42]Liu J, Miller SS, Graham M, Bucciarelli B, Catalano CM, Sherrier DJ, Samac DA, Ivashuta S, Fedorova M, Matsumoto P, Gantt JS, Vance CP: Recruitment of novel calcium-binding proteins for root nodule symbiosis in Medicago truncatula. Plant Physiol 2006, 141:167-177.
• [43]Reddy AS, Narasimhulu SB, Safadi F, Golovkin M: A plant kinesin heavy chain-like protein is a calmodulin-binding protein. Plant J 1996, 10:9-21.
• [44]Boyko EV, Badaev NS, Maximov NG, Zelenin AV: Regularities of genome formation and organization in cereals: I. DNA quantitative changes in the process of allopolyploidization. Genetika 1988, 24:89-97.
• [45]Bennett MD, Leitch IJ: Nuclear DNA amounts in angiosperms: targets, trends and tomorrow. Annal Bot 2011, 107:467-590.
• [46]Ma X-F, Pang P, JP Gustafson JP: Polyploidization-induced genome variation in triticale. Genome 2004, 47:839-848.
• [47]Ma X-F, Gustafson JP: Timing and rate of genome variation in triticale following allopolyploidization. Genome 2006, 49:950-958.
• [48]Buggs RJA, Doust AN, Tate JA, Koh J, Soltis K, Feltus FA, Paterson AH, Soltis PS, Soltis DE: Gene loss and silencing in Tragopogon miscellus (Asteraceae): comparison of natural and synthetic allotetraploids. Heredity 2009, 103:73-81.
• [49]Adams KL, Cronn R, Percifield R, Wendel JF: Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc Natl Acad Sci U S A 2003, 100:4649-4654.