期刊论文详细信息
BMC Genomics
Building the sugarcane genome for biotechnology and identifying evolutionary trends
Marie-Anne Van Sluys9  João Paulo Kitajima1,11  Michel Vincentz3  Glaucia Mendes Souza7  Anete Pereira de Souza3  Angélique D’Hont1,12  Hélène Bergès1  Andrew H Paterson4  Changsoo Kim4  Monalisa Sampaio Carneiro5  Antônio Augusto Franco Garcia1,10  Katia Castanho Scortecci6  Claudio Benicio Cardoso-Silva3  Milton Yutaka Nishiyama7  Rodrigo Fandino de Andrade7  Paloma Mieko Sato7  Carolina Gimiliani Lembke7  Mariane de Mendonça Vilela3  Adilson Silva da Trindade6  Sonia Vautrin1  Alessandro de Mello Varani1,10  Carlos Takeshi Hotta7  Tatiana Caroline Silveira Corrêa9  Edgar Andrés Ochoa Cruz9  Andreia Prata Vieira9  Paula Cristina Gasperazzo Turrini9  Sideny Lima Nunes7  Roberta Alvares Campos7  Fábio Tebaldi Silveira Nogueira2  Renato Vicentini3  Luiz Eduardo Del Bem3  Guilherme Marcelo Queiroga Cruz9  Cushla Jane Metcalfe9  Cláudia Barros Monteiro-Vitorello1,10  Nathalia de Setta8 
[1] INRA – CNRGV, 24 Chemin de Borde Rouge, Auzeville, CS 52627, 31326 Castanet Tolosan Cedex, France;Departamento de Genética, Instituto de Biociências, Universidade Estadual Paulista, campus de Botucatu, Distrito de Rubião Jr., s/n, 18618-000, Botucatu, Brazil;Centro de Biologia Molecular e Engenharia Genética, Universidade Estadual de Campinas, Av. Cândido Rondon, 400, 13083-875 Campinas, Brazil;Departments of Plant Biology, Crop and Soil Science, and Genetics, University of Georgia, 111 Riverbend Rd, Athens, GA 30602, USA;Centro de Ciências Agrárias, Universidade Federal de São Carlos, Araras, SP, Brazil;Departamento de Biologia Celular e Genética – UFRN, Campus Universitário s/n, Natal, RN 59072-970, Brazil;Departamento de Bioquímica, Instituto de Química, Av. Prof. Lineu Prestes, 748, São Paulo 05508-900, SP, Brazil;Universidade Federal do ABC, Rua Santa Adélia, 166, Santo André, 09210-170, Brazil;Departamento de Botânica – Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, São Paulo 05508-090, SP, Brazil;Escola Superior de Agricultura Luiz de Queiroz, Departamento de Genética, Universidade de São Paulo, Av. Padua Dias, 11, Agronomia 13418-900, Piracicaba, SP, Brasil;Mendelics Genomic Analysis, Rua Cubatão 86, São Paulo, SP, Brazil;CIRAD, UMR1096, TA40/03 Avenue Agropolis, 34398, Montpellier Cedex 5, France
关键词: Grasses;    Genetics;    Genome;    Polyploidy;    Bacterial artificial chromosome sequencing;    Saccharum;   
Others  :  1216544
DOI  :  10.1186/1471-2164-15-540
 received in 2013-12-17, accepted in 2014-06-19,  发布年份 2014
PDF
【 摘 要 】

Background

Sugarcane is the source of sugar in all tropical and subtropical countries and is becoming increasingly important for bio-based fuels. However, its large (10 Gb), polyploid, complex genome has hindered genome based breeding efforts. Here we release the largest and most diverse set of sugarcane genome sequences to date, as part of an on-going initiative to provide a sugarcane genomic information resource, with the ultimate goal of producing a gold standard genome.

Results

Three hundred and seventeen chiefly euchromatic BACs were sequenced. A reference set of one thousand four hundred manually-annotated protein-coding genes was generated. A small RNA collection and a RNA-seq library were used to explore expression patterns and the sRNA landscape. In the sucrose and starch metabolism pathway, 16 non-redundant enzyme-encoding genes were identified. One of the sucrose pathway genes, sucrose-6-phosphate phosphohydrolase, is duplicated in sugarcane and sorghum, but not in rice and maize. A diversity analysis of the s6pp duplication region revealed haplotype-structured sequence composition. Examination of hom(e)ologous loci indicate both sequence structural and sRNA landscape variation. A synteny analysis shows that the sugarcane genome has expanded relative to the sorghum genome, largely due to the presence of transposable elements and uncharacterized intergenic and intronic sequences.

Conclusion

This release of sugarcane genomic sequences will advance our understanding of sugarcane genetics and contribute to the development of molecular tools for breeding purposes and gene discovery.

【 授权许可】

   
2014 de Setta et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150701043156933.pdf 1846KB PDF download
Figure 5. 81KB Image download
Figure 4. 67KB Image download
Figure 3. 36KB Image download
Figure 2. 97KB Image download
Figure 1. 80KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】
  • [1]European Commission: Agriculture and Rural Development: Sugar http://ec.europa.eu/agriculture/sugar/index_en.htm webcite
  • [2]Kellogg EA: Evolutionary history of the grasses. Plant Physiol 2001, 125:1198-1205.
  • [3]Grivet L, Arruda P: Sugarcane genomics: depicting the complex genome of an important tropical crop. Curr Opin Plant Biol 2001, 5:122-127.
  • [4]Piperidis G, Piperidis N, D’Hont A: Molecular cytogenetic investigation of chromosome composition and transmission in sugarcane. Mol Genet Genomics 2010, 284:65-73.
  • [5]D’Hont A: Unraveling the genome structure of polyploids using FISH and GISH; examples of sugarcane and banana. Cytogenet Genome Res 2005, 109:27-33.
  • [6]D’Hont A, Glaszmann JC: Sugarcane genome analysis with molecular markers: a first decade of research. Int Soc Sugar Cane Technol Proc XXIV Congr 2001, 556-559.
  • [7]Tomkins J, Yu Y, Miller-Smith H, Frisch D, Woo S, Wing R: A bacterial artificial chromosome library for sugarcane. Theor Appl Genet 1999, 99:419-424.
  • [8]Vettore L, Silva FR, Kemper EL, Souza GM, Silva AM, Ferro M, Henrique-Silva F, Giglioti ÉA, Lemos MVF, Coutinho LL, Nobrega MP, Carrer H, França SC, Bacci MJ, Goldman MHS, Gomes SL, Nunes LR, Camargo LEA, Siqueira WJ, Van Sluys M-A, Thiemann OH, Kuramae EE, Santelli RV, Marino CL, Targon MLPN, Ferro JA, Silveira HCS, Marini DC, Lemos EGM, Monteiro-Vitorello CB, et al.: Analysis and functional annotation of an expressed sequence tag collection for tropical crop sugarcane. Genome Res 2003, 13:2725-2735.
  • [9]Repbase http://www.girinst.org/repbase/ webcite
  • [10]Domingues DS, Cruz GMQ, Metcalfe CJ, Nogueira FTS, Vicentini R, Alves C de S, Van Sluys M-A: Analysis of plant LTR-retrotransposons at the fine-scale family level reveals individual molecular patterns. BMC Genomics 2012, 13:137.
  • [11]National Center for Biotechnology Information (NCBI) http://www.ncbi.nlm.nih.gov/ webcite
  • [12]Meyer F, Paarmann D, D’Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA: The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 2008, 9:386.
  • [13]Keeling PL, Myers AM: Biochemistry and genetics of starch synthesis. Annu Rev Food Sci Technol 2010, 1:271-303.
  • [14]Phytozome v9.1: Home http://www.phytozome.net/ webcite
  • [15]Dias ES, Carareto CMA: Ancestral polymorphism and recent invasion of transposable elements in Drosophila species. BMC Evol Biol 2012, 12:119.
  • [16]Posada D, Crandall K: Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 2001, 16:37-45.
  • [17]Swaminathan K, Alabady MS, Varala K, De Paoli E, Ho I, Rokhsar DS, Arumuganathan AK, Ming R, Green PJ, Meyers BC, Moose SP, Hudson ME: Genomic and small RNA sequencing of Miscanthus x giganteus shows the utility of sorghum as a reference genome sequence for Andropogoneae grasses. Genome Biol 2010, 11:R12.
  • [18]Zanca AS, Vicentini R, Ortiz-Morea FA, Del Bem LE, da Silva MJ, Vincentz M, Nogueira FT: Identification and expression analysis of microRNAs and targets in the biofuel crop sugarcane. BMC Plant Biol 2010, 10:260.
  • [19]Piriyapongsa J, Jordan IK: A family of human microRNA genes from miniature inverted-repeat transposable elements. PLoS ONE 2007, 2:e203.
  • [20]Barrera-Figueroa BE, Gao L, Wu Z, Zhou X, Zhu J, Jin H, Liu R, Zhu J-K: High throughput sequencing reveals novel and abiotic stress-regulated microRNAs in the inflorescences of rice. BMC Plant Biol 2012, 12:132.
  • [21]Nagaki K, Tsujimoto H, Sasakuma T: A novel repetitive sequence of sugar cane, SCEN family, locating on centromeric regions. Chromosom Res 1998, 6:295-302.
  • [22]Nagaki K, Neumann P, Zhang D, Ouyang S, Buell CR, Cheng Z, Jiang J: Structure, divergence, and distribution of the CRR centromeric retrotransposon family in rice. Mol Biol Evol 2005, 22:845-855.
  • [23]Vicentini R, Del Bem LE, Van Sluys M-A, Nogueira F, Vincentz M: Gene content analysis of sugarcane public ESTs reveals thousands of missing coding-genes and an unexpected pool of grasses conserved ncRNAs. Trop Plant Biol 2012, 5:199-205.
  • [24]Kim C, Lee T-H, Compton RO, Robertson JS, Pierce GJ, Paterson AH: A genome-wide BAC end-sequence survey of sugarcane elucidates genome composition, and identifies BACs covering much of the euchromatin. Plant Mol Biol 2013, 81:139-147.
  • [25]Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, et al.: The Sorghum bicolor genome and the diversification of grasses. Nature 2009, 457:551-556.
  • [26]Chang Y, Gong L, Yuan W, Li X, Chen G, Li X, Zhang Q, Wu C: Replication protein A (RPA1a) is required for meiotic and somatic DNA repair but is dispensable for DNA replication and homologous recombination in rice. Plant Physiol 2009, 151:2162-2173.
  • [27]Feschotte C: Transposable elements and the evolution of regulatory networks. Nat Rev Genet 2008, 9:397-405.
  • [28]Wang J, Roe B, Macmil S, Yu Q, Murray JE, Tang H, Chen C, Najar F, Wiley G, Bowers J, Van Sluys M-A, Rokhsar DS, Hudson ME, Moose SP, Paterson AH, Ming R: Microcollinearity between autopolyploid sugarcane and diploid sorghum genomes. BMC Genomics 2010, 11:261.
  • [29]Garsmeur O, Charron C, Bocs S, Jouffe V, Samain S, Couloux A, Droc G, Zini C, Glaszmann J-C, Van Sluys M-A, D’Hont A: High homologous gene conservation despite extreme autopolyploid redundancy in sugarcane. New Phytol 2011, 189:629-642.
  • [30]Jannoo N, Grivet L, Chantret N, Garsmeur O, Glaszmann JC, Arruda P, D’Hont A: Orthologous comparison in a gene-rich region among grasses reveals stability in the sugarcane polyploid genome. Plant J 2007, 50:574-585.
  • [31]Figueira TRES, Okura V, da Silva FR, da Silva MJ, Kudrna D, Ammiraju JSS, Talag J, Wing R, Arruda P: A BAC library of the SP80–3280 sugarcane variety (saccharum sp.) and its inferred microsynteny with the sorghum genome. BMC Res Notes 2012, 5:185.
  • [32]Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, et al.: The B73 maize genome: complexity, diversity, and dynamics. Science 2009, 326:1112-1115.
  • [33]Tenaillon MI, Hufford MB, Gaut BS, Ross-Ibarra J: Genome size and transposable element content as determined by high-throughput sequencing in maize and Zea luxurians. Genome Biol Evol 2011, 3:219-229.
  • [34]Zhang J, Yu C, Krishnaswamy L, Peterson T: Transposable Elements as Catalysts for Chromosome Rearrangements. In Methods Mol Biol. Edited by Birchler JA. Totowa, NJ: Humana Press; 2011:315-326.
  • [35]Ma J, Wing RA, Bennetzen JL, Jackson SA: Plant centromere organization: a dynamic structure with conserved functions. Trends Genet 2007, 23:134-139.
  • [36]D’Hont A, Grivet L, Feldmann P, Rao S, Berding N, Glaszmann JC: Characterisation of the double genome structure of modern sugarcane cultivars (Saccharum spp.) by molecular cytogenetics. Mol Gen Genet 1996, 250:405-413.
  • [37]Bao Y, Wendel JF, Ge S: Multiple patterns of rDNA evolution following polyploidy in Oryza. Mol Phylogenet Evol 2010, 55:136-142.
  • [38]Lynch M: The Origins of Genome Architecture. Sunderland, Massachussetts, USA: Sinauer Associates Inc.; 2007.
  • [39]International Rice Genome Sequencing Project: The map-based sequence of the rice genome. Nature 2005, 436:793-800.
  • [40]Liu B, Xu C, Zhao N, Qi B, Kimatu JN, Pang J, Han F: Rapid genomic changes in polyploid wheat and related species: implications for genome evolution and genetic improvement. J Genet Genomics 2009, 36:519-528.
  • [41]Lisch D: How important are transposons for plant evolution? Nat Rev Genet 2012, 14:49-61.
  • [42]Udall JA, Wendel JF: Polyploidy and crop improvement. Crop Sci 2006, 46:S3-S14.
  • [43]Varshney RK, Graner A, Sorrells ME: Genomics-assisted breeding for crop improvement. Trends Plant Sci 2005, 10:621-630.
  • [44]Menossi M, Silva-Filho MC, Vincentz M, Van-Sluys M-A, Souza GM: Sugarcane functional genomics: gene discovery for agronomic trait development. Int J Plant Genomics 2008, 2008:458732. doi:10.1155/2008/458732
  • [45]Palhares AC, Rodrigues-Morais TB, Van Sluys M-A, Domingues DS, Maccheroni W, Jordão H, Souza AP, Marconi TG, Mollinari M, Gazaffi R, Garcia AAF, Vieira MLC: A novel linkage map of sugarcane with evidence for clustering of retrotransposon-based markers. BMC Genet 2012, 13:51.
  • [46]Andersen JR, Lübberstedt T: Functional markers in plants. Trends Plant Sci 2003, 8:554-560.
  • [47]Kalendar R, Flavell AJ, Ellis THN, Sjakste T, Moisy C, Schulman A: Analysis of plant diversity with retrotransposon-based molecular markers. Heredity (Edinb) 2011, 106:520-530.
  • [48]PGML BACMan On The Web: Grasses http://www.plantgenome.uga.edu/bacman/BACManwww.php webcite
  • [49]Rice Genome Annotation Project http://rice.plantbiology.msu.edu/ webcite
  • [50]Bowers JE, Arias MA, Asher R, Avise JA, Ball RT, Brewer GA, Buss RW, Chen AH, Edwards TM, Estill JC, Exum HE, Goff VH, Herrick KL, Steele CLJ, Karunakaran S, Lafayette GK, Lemke C, Marler BS, Masters SL, McMillan JM, Nelson LK, Newsome GA, Nwakanma CC, Odeh RN, Phelps CA, Rarick EA, Rogers CJ, Ryan SP, Slaughter KA, Soderlund CA, et al.: Comparative physical mapping links conservation of microsynteny to chromosome structure and recombination in grasses. Proc Natl Acad Sci U S A 2005, 102:13206-13211.
  • [51]Adam-Blondon A-F, Bernole A, Faes G, Lamoureux D, Pateyron S, Grando MS, Caboche M, Velasco R, Chalhoub B: Construction and characterization of BAC libraries from major grapevine cultivars. Theor Appl Genet 2005, 110:1363-1371.
  • [52]Manetti ME, Rossi M, Cruz GMQ, Saccaro NL, Nakabashi M, Altebarmakian V, Rodier-Goud M, Domingues D, D’Hont A, Van Sluys MA: Mutator system derivatives isolated from sugarcane genome sequence. Trop Plant Biol 2012, 5:233-243.
  • [53]Phrap http://www.phrap.org/ webcite
  • [54]RepeatMasker http://www.repeatmasker.org/ webcite
  • [55]Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O: Repbase update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 2005, 110:462-467.
  • [56]Han Y, Wessler SR: MITE-Hunter: a program for discovering miniature inverted-repeat transposable elements from genomic sequences. Nucleic Acids Res 2010, 38(22):e199. doi: 10.1093/nar/gkq862. Epub 2010 Sep 29
  • [57]Frickey T, Lupas A: CLANS: a Java application for visualizing protein families based on pairwise similarity. Bioinformatics 2004, 20:3702-3704.
  • [58]Han Y, Qin S, Wessler SR: Comparison of class 2 transposable elements at superfamily resolution reveals conserved and distinct features in cereal grass genomes. BMC Genomics 2013, 14:71.
  • [59]Keller O, Kollmar M, Stanke M, Waack S: A novel hybrid gene prediction method employing protein multiple sequence alignments. Bioinformatics 2011, 27:757-763.
  • [60]Majoros WH, Pertea M, Salzberg SL: TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 2004, 20:2878-2879.
  • [61]Haas BJ, Delcher AL, Mount SM, Wortman JR, Smith RK, Hannick LI, Maiti R, Ronning CM, Rusch DB, Town CD, Salzberg SL, White O: Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res 2003, 31:5654-5666.
  • [62]Haas BJ, Salzberg SL, Zhu W, Pertea M, Allen JE, Orvis J, White O, Buell CR, Wortman JR: Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to assemble spliced alignments. Genome Biol 2008, 9:R7.
  • [63]Petersen TN, Brunak S, von Heijne G, Nielsen H: SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 2011, 8:785-786.
  • [64]TMHMM Server v. 2.0 http://www.cbs.dtu.dk/services/TMHMM-2.0/ webcite
  • [65]Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B: Artemis: sequence visualization and annotation. Bioinformatics 2000, 16:944-945.
  • [66]UniProt http://www.uniprot.org/ webcite
  • [67]InterPro: Protein sequence analysis and classification http://www.ebi.ac.uk/interpro/ webcite
  • [68]Conesa A, Götz S: Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008, 2008:1-12.
  • [69]SUCEST-FUN Project http://sucest-fun.org/ webcite
  • [70]MG-RAST: metagenomics analysis server http://metagenomics.anl.gov/ webcite
  • [71]KAAS - KEGG automatic annotation server http://www.genome.jp/kegg/kaas/ webcite
  • [72]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.
  • [73]Lyons E, Freeling M: How to usefully compare homologous plant genes and chromosomes as DNA sequences. Plant J 2008, 53:661-673.
  • [74]Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1999, 41:95-98.
  • [75]Geneious - Homepage http://www.geneious.com/ webcite
  • [76]Heslop-Harrison P, Schwarzacher T: Practical In Situ Hybridization. Oxford, UK: BIOS Scientific Publishers Ltd; 2000.
  • [77]Aljanabi S, Forget L, Dookun A: An improved and rapid protocol for the isolation of polysaccharide-and polyphenol-free sugarcane DNA. Plant Mol Biol Report 1999, 17:1-8.
  • [78]Maq: Mapping and assembly with qualities http://maq.sourceforge.net/ webcite
  • [79]SeqMonk http://www.bioinformatics.babraham.ac.uk/projects/seqmonk/ webcite
  • [80]Gasic K, Hernandez A, Korban SS: RNA extraction from different apple tissues rich in polyphenols and polysaccharides for cDNA. Plant Mol Biol Report 2004, 22(December):437a-437g.
  • [81]Li H, Durbin R: Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
  • [82]Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R: The sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25:2078-2079.
  • [83]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.
  • [84]Bandelt HJ, Forster P, Röhl A: Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1999, 16:37-48.
  • [85]Paterson AH, Freeling M, Tang H, Wang X: Insights from the comparison of plant genome sequences. Annu Rev Plant Biol 2010, 61:349-372.
  文献评价指标  
  下载次数:76次 浏览次数:18次