BMC Genomics | |
Transcriptome sequencing of two wild barley (Hordeum spontaneum L.) ecotypes differentially adapted to drought stress reveals ecotype-specific transcripts | |
Karl J Schmid2  Eyal Fridman1  Menachem Moshelion1  Eyal Bdolach1  Eyal Galkin1  Thomas Müller2  Anna Westerbergh3  Girma Bedada3  | |
[1] Institute of Plant Science and Genetics, The Hebrew University of Jerusalem, Rehovot, Israel;Institute for Plant Breeding, Seed Science and Population Genetics, University of Hohenheim, Fruwirthstrasse 21, D-70599 Stuttgart, Germany;Department of Plant Biology, Uppsala BioCenter, Linnean Centre of Plant Biology in Uppsala, Swedish University of Agricultural Sciences (SLU), Uppsala, Sweden | |
关键词: Genetic diversity; Drought tolerance; Transcriptome; Hordeum spontaneum; | |
Others : 1092198 DOI : 10.1186/1471-2164-15-995 |
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received in 2014-06-09, accepted in 2014-11-04, 发布年份 2014 | |
【 摘 要 】
Background
Wild barley is adapted to highly diverse environments throughout its geographical distribution range. Transcriptome sequencing of differentially adapted wild barley ecotypes from contrasting environments contributes to the identification of genes and genetic variation involved in abiotic stress tolerance and adaptation.
Results
Two differentially adapted wild barley ecotypes from desert (B1K2) and Mediterranean (B1K30) environments were analyzed for drought stress response under controlled conditions. The desert ecotype lost more water under both irrigation and drought, but exhibited higher relative water content (RWC) and better water use efficiency (WUE) than the coastal ecotype. We sequenced normalized cDNA libraries from drought-stressed leaves of both ecotypes with the 454 platform to identify drought-related transcripts. Over half million reads per ecotype were de novo assembled into 20,439 putative unique transcripts (PUTs) for B1K2, 21,494 for B1K30 and 28,720 for the joint assembly. Over 50% of PUTs of each ecotype were not shared with the other ecotype. Furthermore, 16% (3,245) of B1K2 and 17% (3,674) of B1K30 transcripts did not show orthologous sequence hits in the other wild barley ecotype and cultivated barley, and are candidates of ecotype-specific transcripts. Over 800 unique transcripts from each ecotype homologous to over 30 different stress-related genes were identified. We extracted 1,017 high quality SNPs that differentiated the two ecotypes. The genetic distance between the desert ecotype and cultivated barley was 1.9-fold higher than between the Mediterranean ecotype and cultivated barley. Moreover, the desert ecotype harbored a larger proportion of non-synonymous SNPs than the Mediterranean ecotype suggesting different demographic histories of these ecotypes.
Conclusions
The results indicate a strong physiological and genomic differentiation between the desert and Mediterranean wild barley ecotypes and a closer relationship of the Mediterranean to cultivated barley. A significant number of novel transcripts specific to wild barley were identified. The higher SNP density and larger proportion of SNPs with functional effects in the desert ecotype suggest different demographic histories and effects of natural selection in Mediterranean and desert wild barley. The data are a valuable genomic resource for an improved genome annotation, transcriptome studies of drought adaptation and a source of new genetic markers for future barley improvement.
【 授权许可】
2014 Bedada et al.; licensee BioMed Central Ltd.
【 预 览 】
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Figure 1. | 104KB | Image | download |
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【 参考文献 】
- [1]Langridge P, Paltridge N, Fincher G: Functional genomics of abiotic stress tolerance in cereals. Brief Funct Genomics Proteomics 2006, 4(4):343-354.
- [2]Fleury D, Jefferies S, Kuchel H, Langridge P: Genetic and genomic tools to improve drought tolerance in wheat. J Exp Bot 2010, 61(12):3211-3222.
- [3]Verslues PE, Juenger TE: Drought, metabolites, and Arabidopsis natural variation: a promising combination for understanding adaptation to water-limited environments. Curr Opin Plant Biol 2011, 14(3):240-245.
- [4]Chaves MM, Maroco JP, Pereira JS: Understanding plant responses to drought - from genes to the whole plant. Funct Plant Biol 2003, 30(3):239-264.
- [5]Barnabas B, Jager K, Feher A: The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ 2008, 31(1):11-38.
- [6]Blum A: Drought resistance and its improvement. In Plant Breeding for Water-Limited Environments. New York: Springer New York; 2011:53-152.
- [7]Harlan JR, Zohary D: Distribution of wild wheats and barley. Science 1966, 153(3740):1074-1080.
- [8]Hubner S, Gunther T, Flavell A, Fridman E, Graner A, Korol A, Schmid KJ: Islands and streams: clusters and gene flow in wild barley populations from the Levant. Mol Ecol 2012, 21(5):1115-1129.
- [9]Hubner S, Hoffken M, Oren E, Haseneyer G, Stein N, Graner A, Schmid K, Fridman E: Strong correlation of wild barley (Hordeum spontaneum) population structure with temperature and precipitation variation. Mol Ecol 2009, 18(7):1523-1536.
- [10]Bedada G, Westerbergh A, Nevo E, Korol A, Schmid KJ: DNA sequence variation of wild barley Hordeum spontaneum (L.) across environmental gradients in Israel. Heredity (Edinb) 2014, 112(6):646-655.
- [11]Nevo E: Genome evolution of wild cereal diversity and prospects for crop improvement. Plant Genetic Resour Charact Util 2006, 4:1. ISSN 1479-2621(print)1479-1263x(electronic)
- [12]Ellis RP, Forster BP, Robinson D, Handley LL, Gordon DC, Russell JR, Powell W: Wild barley: a source of genes for crop improvement in the 21st century? J Exp Bot 2000, 51(342):9-17.
- [13]Teulat B, Merah O, Sirault X, Borries C, Waugh R, This D: QTLs for grain carbon isotope discrimination in field-grown barley. Theor Appl Genet 2002, 106(1):118-126.
- [14]Teulat B, Zoumarou-Wallis N, Rotter B, Ben Salem M, Bahri H, This D: QTL for relative water content in field-grown barley and their stability across Mediterranean environments. Theor Appl Genet 2003, 108(1):181-188.
- [15]Diab AA, Teulat-Merah B, This D, Ozturk NZ, Benscher D, Sorrells ME: Identification of drought-inducible genes and differentially expressed sequence tags in barley. Theor Appl Genet 2004, 109(7):1417-1425.
- [16]Teulat B, Borries C, This D: New QTLs identified for plant water status, water-soluble carbohydrate and osmotic adjustment in a barley population grown in a growth-chamber under two water regimes. Theor Appl Genet 2001, 103(1):161-170.
- [17]Guo PG, Baum M, Varshney RK, Graner A, Grando S, Ceccarelli S: QTLs for chlorophyll and chlorophyll fluorescence parameters in barley under post-flowering drought. Euphytica 2008, 163(2):203-214.
- [18]Volis S, Mendlinger S, Ward D: Differentiation in populations of Hordeum spontaneum Koch along a gradient of environmental productivity and predictability: plasticity in response to water and nutrient stress. Biol J Linn Soc 2002, 75(3):301-312.
- [19]Volis S, Mendlinger S, Ward D: Adaptive traits of wild barley plants of Mediterranean and desert origin. Oecologia 2002, 133(2):131-138.
- [20]Hubner S, Bdolach E, Ein-Gedy S, Schmid KJ, Korol A, Fridman E: Phenotypic landscapes: phenological patterns in wild and cultivated barley. J Evol Biol 2013, 26(1):163-174.
- [21]von Korff M, Grando S, Del Greco A, This D, Baum M, Ceccarelli S: Quantitative trait loci associated with adaptation to Mediterranean dryland conditions in barley. Theor Appl Genet 2008, 117(5):653-669.
- [22]Varshney RK, Langridge P, Graner A: Application of genomics to molecular breeding of wheat and barley. Adv Genet 2007, 58:121-+.
- [23]Mayer KF, Waugh R, Brown JW, Schulman A, Langridge P, Platzer M, Fincher GB, Muehlbauer GJ, Sato K, Close TJ, Wise RP, Stein N, IBGS Consortium: A physical, genetic and functional sequence assembly of the barley genome. Nature 2012, 491(7426):711-716.
- [24]Mascher M, Richmond TA, Gerhardt DJ, Himmelbach A, Clissold L, Sampath D, Ayling S, Steuernagel B, Pfeifer M, D’Ascenzo M, Akhunov ED, Hedley PE, Gonzales AM, Morrell PL, Kilian B, Blattner FR, Scholz U, Mayer KF, Flavell AJ, Muehlbauer GJ, Waugh R, Jeddeloh JA, Stein N: Barley whole exome capture: a tool for genomic research in the genus Hordeum and beyond. Plant J 2013, 76(3):494-505.
- [25]Munoz-Amatriain M, Eichten SR, Wicker T, Richmond TA, Mascher M, Steuernagel B, Scholz U, Ariyadasa R, Spannagl M, Nussbaumer T, Mayer KF, Taudien S, Platzer M, Jeddeloh JA, Springer NM, Muehlbauer GJ, Stein N: Distribution, functional impact, and origin mechanisms of copy number variation in the barley genome. Genome Biol 2013, 14(6):R58.
- [26]Morrell PL, Buckler ES, Ross-Ibarra J: Crop genomics: advances and applications. Nat Rev Genet 2011, 13(2):85-96.
- [27]Stapley J, Reger J, Feulner PG, Smadja C, Galindo J, Ekblom R, Bennison C, Ball AD, Beckerman AP, Slate J: Adaptation genomics: the next generation. Trends Ecol Evol 2010, 25(12):705-712.
- [28]Ekblom R, Galindo J: Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity 2011, 107(1):1-15.
- [29]Eppel A, Keren N, Salomon E, Volis S, Rachmilevitch S: The response of Hordeum spontaneum desert ecotype to drought and excessive light intensity is characterized by induction of O2 dependent photochemical activity and anthocyanin accumulation. Plant Sci 2013, 201–202:74-80.
- [30]Suprunova T, Krugman T, Distelfeld A, Fahima T, Nevo E, Korol A: Identification of a novel gene (Hsdr4) involved in water-stress tolerance in wild barley. Plant Mol Biol 2007, 64(1–2):17-34.
- [31]Knight CA, Vogel H, Kroymann J, Shumate A, Witsenboer H, Mitchell-Olds T: Expression profiling and local adaptation of Boechera holboellii populations for water use efficiency across a naturally occurring water stress gradient. Mol Ecol 2006, 15(5):1229-1237.
- [32]Brouillette LC, Mason CM, Shirk RY, Donovan LA: Adaptive differentiation of traits related to resource use in a desert annual along a resource gradient. New Phytol 2014, 201(4):1316-1327.
- [33]Müller T, Ensminger I, Schmid KJ: A catalogue of putative unique transcripts from Douglas-fir (Pseudotsuga menziesii) based on 454 transcriptome sequencing of genetically diverse, drought stressed seedlings. BMC Genomics 2012, 13(1):673.
- [34]Haseneyer G, Schmutzer T, Seidel M, Zhou R, Mascher M, Schon CC, Taudien S, Scholz U, Stein N, Mayer KF, Bauer E: From RNA-seq to large-scale genotyping - genomics resources for rye (Secale cereale L.). BMC Plant Biol 2011, 11:131.
- [35]Cantu D, Pearce SP, Distelfeld A, Christiansen MW, Uauy C, Akhunov E, Fahima T, Dubcovsky J: Effect of the down-regulation of the high Grain Protein Content (GPC) genes on the wheat transcriptome during monocarpic senescence. BMC Genomics 2011, 12:492.
- [36]Thiel J, Hollmann J, Rutten T, Weber H, Scholz U, Weschke W: 454 Transcriptome sequencing suggests a role for two-component signalling in cellularization and differentiation of barley endosperm transfer cells. Plos One 2012, 7(7):e41867.
- [37]Matsumoto T, Tanaka T, Sakai H, Amano N, Kanamori H, Kurita K, Kikuta A, Kamiya K, Yamamoto M, Ikawa H, Fujii N, Hori K, Itoh T, Sato K: Comprehensive sequence analysis of 24,783 barley full-length cDNAs derived from 12 clone libraries. Plant Physiol 2011, 156(1):20-28.
- [38]Sato K, Shin-I T, Seki M, Shinozaki K, Yoshida H, Takeda K, Yamazaki Y, Conte M, Kohara Y: Development of 5006 full-length CDNAs in barley: a tool for accessing cereal genomics resources. DNA Res 2009, 16(2):81-89.
- [39]Azam S, Thakur V, Ruperao P, Shah T, Balaji J, Amindala B, Farmer AD, Studholme DJ, May GD, Edwards D, Jones JD, Varshney RK: Coverage-based consensus calling (CbCC) of short sequence reads and comparison of CbCC results to identify SNPs in chickpea (Cicer arietinum; Fabaceae), a crop species without a reference genome. Am J Bot 2012, 99(2):186-192.
- [40]Li B, Ruotti V, Stewart RM, Thomson JA, Dewey CN: RNA-Seq gene expression estimation with read mapping uncertainty. Bioinformatics 2010, 26(4):493-500.
- [41]Costa V, Angelini C, De Feis I, Ciccodicola A: Uncovering the complexity of transcriptomes with RNA-Seq. J Biomed Biotechnol 2010, 2010:853916.
- [42]Ekblom R, Slate J, Horsburgh GJ, Birkhead T, Burke T: Comparison between Normalised and Unnormalised 454-Sequencing Libraries for Small-Scale RNA-Seq Studies. Comp Funct Genomics 2012, 2012:8.
- [43]Ferreira De Carvalho J, Poulain J, Da Silva C, Wincker P, Michon-Coudouel S, Dheilly A, Naquin D, Boutte J, Salmon A, Ainouche M: Transcriptome de novo assembly from next-generation sequencing and comparative analyses in the hexaploid salt marsh species Spartina maritima and Spartina alterniflora (Poaceae). Hered (Edinb) 2013, 110(2):181-193.
- [44]Blaxter M: Revealing the dark matter of the genome. Science 2010, 330(6012):1758-1759.
- [45]Close TJ, Wanamaker SI, Caldo RA, Turner SM, Ashlock DA, Dickerson JA, Wing RA, Muehlbauer GJ, Kleinhofs A, Wise RP: A new resource for cereal genomics: 22 K barley GeneChip comes of age. Plant Physiol 2004, 134(3):960-968.
- [46]Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A: Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet 2005, 37(9):997-1002.
- [47]Wang Q, Dooner HK: Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus. Proc Natl Acad Sci U S A 2006, 103(47):17644-17649.
- [48]Morgante M, De Paoli E, Radovic S: Transposable elements and the plant pan-genomes. Curr Opin Plant Biol 2007, 10(2):149-155.
- [49]Bartels D, Sunkar R: Drought and Salt Tolerance in Plants. Crit Rev Plant Sci 2005, 24(1):23-58.
- [50]Chen GX, Komatsuda T, Ma JF, Nawrath C, Pourkheirandish M, Tagiri A, Hu YG, Sameri M, Li XR, Zhao X, Liu YB, Li C, Ma XY, Wang AD, Nair S, Wang N, Miyao A, Sakuma S, Yamaji N, Zheng XT, Nevo E: An ATP-binding cassette subfamily G full transporter is essential for the retention of leaf water in both wild barley and rice. Proc Natl Acad Sci U S A 2011, 108(30):12354-12359.
- [51]Schutze K, Harter K, Chaban C: Post-translational regulation of plant bZIP factors. Trends Plant Sci 2008, 13(5):247-255.
- [52]Feller A, Machemer K, Braun EL, Grotewold E: Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 2011, 66(1):94-116.
- [53]de Mezer M, Turska-Taraska A, Kaczmarek Z, Glowacka K, Swarcewicz B, Rorat T: Differential physiological and molecular response of barley genotypes to water deficit. Plant Physiol Biochem PPB / Soc Francaise Physiol Vegetale 2014, 80C:234-248.
- [54]Nielsen R, Paul JS, Albrechtsen A, Song YS: Genotype and SNP calling from next-generation sequencing data. Nat Rev Genet 2011, 12(6):443-451.
- [55]Quinn EM, Cormican P, Kenny EM, Hill M, Anney R, Gill M, Corvin AP, Morris DW: Development of strategies for SNP detection in RNA-Seq data: application to lymphoblastoid cell lines and evaluation using 1000 genomes data. Plos One 2013, 8(3):e58815.
- [56]Duran C, Appleby N, Vardy M, Imelfort M, Edwards D, Batley J: Single nucleotide polymorphism discovery in barley using autoSNPdb. Plant Biotechnol J 2009, 7(4):326-333.
- [57]Zhu YY, Machleder EM, Chenchik A, Li R, Siebert PD: Reverse transcriptase template switching: A SMART (TM) approach for full-length cDNA library construction. Biotechniques 2001, 30(4):892-897.
- [58]Barnes WM: PCR amplification of up to 35-kb DNA with high fidelity and high yield from lambda bacteriophage templates. Proc Natl Acad Sci U S A 1994, 91(6):2216-2220.
- [59]Zhulidov PA, Bogdanova EA, Shcheglov AS, Vagner LL, Khaspekov GL, Kozhemyako VB, Matz MV, Meleshkevitch E, Moroz LL, Lukyanov SA, Shagin DA: Simple cDNA normalization using kamchatka crab duplex‒specific nuclease. Nucleic Acids Res 2004, 32(3):e37.
- [60]Shagin DA, Rebrikov DV, Kozhemyako VB, Altshuler IM, Shcheglov AS, Zhulidov PA, Bogdanova EA, Staroverov DB, Rasskazov VA, Lukyanov S: A novel method for SNP detection using a New duplex-specific nuclease from crab hepatopancreas. Genome Res 2002, 12(12):1935-1942.
- [61]Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen ZT, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer MLI, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, et al.: Genome sequencing in microfabricated high-density picolitre reactors. Nature 2005, 437(7057):376-380.
- [62]SeqClean ftp://occams.dfci.harvard.edu/pub/bio/tgi/software/ webcite
- [63]The UniVec database ftp://ftp.ncbi.nih.gov/pub/UniVec/ webcite
- [64]Li WZ, Godzik A: Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006, 22(13):1658-1659.
- [65]Langmead B, Salzberg SL: Fast gapped-read alignment with Bowtie 2. Nat Methods 2012, 9(4):357-359.
- [66]454 Life Science: Genome Sequencer FLX System Software Manual, Version 2.3. 2009.
- [67]Edgar RC: Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 26(19):2460-2461.
- [68]Li H, Durbin R: Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 2010, 26(5):589-595.
- [69]Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Proc GPD: The sequence alignment/Map format and SAMtools. Bioinformatics 2009, 25(16):2078-2079.
- [70]Cingolani P, Platts A, le Wang L, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM: A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 2012, 6(2):80-92.
- [71]Auton A, McVean G: Recombination rate estimation in the presence of hotspots. Genome Res 2007, 17(8):1219-1227.
- [72]PERL scripts for RBH analysis http://sysbio.harvard.edu/csb/resources/computational/scriptome/unix/Protocols/Sequences.html webcite
- [73]Vogel JP, Garvin DF, Mockler TC, Schmutz J, Rokhsar D, Bevan MW, Barry K, Lucas S, Harmon-Smith M, Lail K, Tice H, Grimwood J, McKenzie N, Huo NX, Gu YQ, Lazo GR, Anderson OD, You FM, Luo MC, Dvorak J, Wright J, Febrer M, Idziak D, Hasterok R, Lindquist E, Wang M, Fox SE, Priest HD, Filichkin SA, Givan SA, et al.: Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 2010, 463(7282):763-768.
- [74]Matsumoto T, Wu JZ, Kanamori H, Katayose Y, Fujisawa M, Namiki N, Mizuno H, Yamamoto K, Antonio BA, Baba T, Sakata K, Nagamura Y, Aoki H, Arikawa K, Arita K, Bito T, Chiden Y, Fujitsuka N, Fukunaka R, Hamada M, Harada C, Hayashi A, Hijishita S, Honda M, Hosokawa S, Ichikawa Y, Idonuma A, Iijima M, Ikeda M, Ikeno M, et al.: The map-based sequence of the rice genome. Nature 2005, 436(7052):793-800.
- [75]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 HB, Wang XY, 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 LF, Carpita NC, et al.: The Sorghum bicolor genome and the diversification of grasses. Nature 2009, 457(7229):551-556.
- [76]Lawrence CJ, Schaeffer ML, Seigfried TE, Campbell DA, Harper LC: MaizeGDB’s new data types, resources and activities. Nucleic Acids Res 2007, 35:D895-D900.
- [77]Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, Li D, Meyer T, Muller R, Ploetz L, Radenbaugh A, Singh S, Swing V, Tissier C, Zhang P, Huala E: The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Res 2008, 36:D1009-D1014.
- [78]Kurata N, Nonomura KI, Harushima Y: Rice genome organization: The centromere and genome interactions. Ann Bot 2002, 90(4):427-435.
- [79]Zhang H, Jin JP, Tang LA, Zhao Y, Gu XC, Gao G, Luo JC: PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Res 2011, 39:D1114-D1117.
- [80]Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M: Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21(18):3674-3676.
- [81]Myhre S, Tveit H, Mollestad T, Laegreid A: Additional Gene Ontology structure for improved biological reasoning. Bioinformatics 2006, 22(16):2020-2027.
- [82]Camon E, Magrane M, Barrell DVL, Dimmer E, Maslen J, Binns D, Harte N, Lopez R, Apweiler R: The gene ontology annotation (GOA) database: sharing knowledge in uniprot with gene ontology. Nucleic Acids Res 2004, 32:D262-D266.
- [83]Min XJ, Butler G, Storms R, Tsang A: OrfPredictor: predicting protein-coding regions in EST-derived sequences. Nucleic Acids Res 2005, 33(Web Server issue):W677-W680.