Transcriptome Analysis in Sheepgrass (Leymus chinensis): A Dominant Perennial Grass of the Eurasian Steppe

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Chen, Shuangyan ^a   Huang, Xin ^a,b   Yan, Xueqing ^a,b   Liang, Ye ^a,b   Wang, Yuezhu ^c   Li, Xiaofeng ^a   Peng, Xianjun ^a   Ma, Xingyong ^a,b   Zhang, Lexin ^a,b   Cai, Yueyue ^a,b   Ma, Tian ^a   Cheng, Liqin ^a   Qi, Dongmei ^a   Zheng, Huajun ^c   Yang, Xiaohan ^d   Li, Xiaoxia ^a,b   Liu, Gongshe ^a  

^a INSTITUTE OF BOTANY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c CHINESE NATIONAL HUMAN GENOME CENTER AT SHANGHAI   (China)

^d OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME;

AMINO ACID SEQUENCE; ARTICLE; BARLEY; EVOLUTIONARY ADAPTATION; EXPRESSED SEQUENCE TAG; GENETIC DATABASE; GENETIC TRANSFORMATION; LEYMUS CHINENSIS; NONHUMAN; NUCLEOTIDE REPEAT; PERENNIAL PLANT; PHYLOGENY; PLANT BREEDING; PLANT GENOME; PYROSEQUENCING; RNA SEQUENCE; SHEEPGRASS; SIMPLE SEQUENCE REPEAT; TRANSCRIPTOMICS; WHEAT;

ASIA; DATABASES, GENETIC; EUROPE; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; HORDEUM; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR TYPING; PHYLOGENY; POACEAE; SEQUENCE ANALYSIS, DNA; TRANSCRIPTOME; TRITICUM;

HORDEUM; LEYMUS CHINENSIS; POACEAE; TRITICUM AESTIVUM;

EID: 84879810700     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067974     Document Type: Article

References (89)

1. Liu ZP, Chen ZY, Pan J, Li XF, Su M, et al. (2008) Phylogenetic relationships in Leymus (Poaceae: Triticeae) revealed by the nuclear ribosomal internal transcribed spacer and chloroplast trnL-F sequences. Mol Phylogenet Evol 46: 278-289.
2. Jiang J, Friebe B, Gill BS, (1994) Recent advances in alien gene transfer in wheat. Euphytica 73: 199-212.
3. Liu X, Shi J, Zhang XY, Ma YS, Jia JZ, (2001) Screening salt tolerance germplasms and tagging the tolerance gene(s) using microsatellite (SSR) markers in wheat. Acta Bot Sinica 43: 948-954.
4. Chen PD, Liu WX, Yuan JH, Wang XE, Zhou B, et al. (2005) Development and characterization of wheat-Leymus racemosus translocation lines with resistance to Fusarium Head Blight. Theor Appl Genet 111: 941-948.
5. Qi LL, Pumphrey MO, Briebe B, Chen PD, Gill BS, (2008) Molecular cytogenetic characterization of alien introgressions with gene Fhb3 for resistance to Fusarium head blight disease of wheat. Theor Appl Genet 117: 1155-1166.
6. Subbarao GV, Tomohiro B, Masahiro K, Osamu I, Samejima H, (2007) Can biological nitrification inhibition (BNI) genes from perennial Leymus racemosus (Triticeae) combat nitrification in wheat farming? Plant Soil 299: 55-64.
7. Bai YF, Han XG, Wu JG, Chen ZZ, Li LH, (2004) Ecosystem stability and compensatory effects in the Inner Mongolia grassland. Nature 431: 181-184.
8. Bai WM, Xun F, Li Y, Zhang WH, Li LH, (2010) Rhizome severing increases root lifespan of Leymus chinensis in a typical steppe of Inner Mongolia. PLoS One 5: e12125.
9. Zhang WD, Chen SY, Liu GS, Jan CC, (2004) Seed-set and pollen-stigma compatibility in Leymus Chinensis. Grass Forage Sci 59: 180-185.
10. Ma HY, Liang ZW, (2007) Effects of different soil pH and soil extracts on the germination and seedling growth of Leymus chinensis. Chin Bull Bot 24: 181-188.
11. Wang RZ, Chen L, Bai YG, Xiao CW, (2008) Seasonal dynamics in resource partitioning to growth and storage in response to drought in a perennial rhizomatous grass, Leymus chinensis. J Plant Growth Regul 27: 39-48.
12. Wang LJ, Li XF, Chen SY, Liu GS, (2009) Enhanced drought tolerance in transgenic Leymus chinensis plants with constitutively expressed wheat TaLEA3. Biotechnol Lett 31: 313-319.
13. Niu S, Liu W, Wan S, (2008) Different growth responses of C3 and C4 grasses to seasonal water and nitrogen regimes and competition in a pot experiment. J Exp Bot 59: 1431-1439.
14. Wang YH, Zhou GS, Wang YH, (2007) Modeling responses of the meadow steppe dominated by Leymus chinensis to climate change. Climatic Change 82: 437-452.
15. Xu Z, Zhou G, Shimizu H, (2009) Are plant growth and photosynthesis limited by pre-drought following rewatering in grass? J Exp Bot 60: 3737-3749.
16. Xu ZZ, Zhou GS, (2006) Combined effects of water stress and high temperature on photosynthesis, nitrogen metabolism and lipid peroxidation of a perennial grass Leymus chinensis. Planta 224: 1080-1090.
17. Zhang L, Yang Y, Zhan X, Zhang C, Zhou S, et al. (2009) Responses of a dominant temperate grassland plant (Leymus chinensis) to elevated carbon dioxide and nitrogen addition in China. J Environ Qual 39: 251-259.
18. Jin H, Plaha P, Park JY, Hong CP, Lee IS, et al. (2006) Comparative EST profiles of leaf and root of Leymus chinensis, a xerophilous grass adapted to high pH sodic soil. Plant Sci 170: 1081-1086.
19. Peng XJ, Ma XY, Fan WH, Su M, Cheng LQ, et al. (2011) Improved drought and salt tolerance of Arabidopsis thaliana by transgenic expression of a novel DREB gene from Leymus chinensis. Plant Cell Rep 30: 1493-1502.
20. Ma P, Liu J, (2012) Isolation and characterization of a novel plasma membrane intrinsic protein gene, LcPIP1, in Leymus chinensis that enhances salt stress tolerance in Saccharomyces cerevisiae. Appl Biochem Biotechnol 166: 479-485.
21. Mardis ER, (2008) The impact of next-generation sequencing technology on genetics. Trends Genet 24: 133-141.
22. Varshney RK, Nayak SN, May GD, Jackson SA, (2009) Next generation sequencing technologies and their implications for crop genetics and breeding. Trends Biotechnol 27: 522-530.
23. Cheung F, Haas BJ, Goldberg SMD, May GD, Xiao Y, et al. (2006) Sequencing Medicago truncatula expressed sequenced tags using 454 Life Sciences technology. BMC Genomics 7: 272.
24. Weber APM, Weber KL, Carr K, Wilkerson C, Ohlrogge JB, (2007) Sampling the Arabidopsis transcriptome with massively parallel pyrosequencing. Plant Physiol 144: 32-42.
25. Emrich SJ, Barbazuk WB, Li L, Schnable PS, (2007) Gene discovery and annotation using LCM-454 transcriptome sequencing. Genome Res 17: 69-73.
26. Steuernagel B, Taudien S, Gundlach H, Seidel M, Ariyadasa R, et al. (2009) De novo 454 sequencing of barcoded BAC pools for comprehensive gene survey and genome analysis in the complex genome of barley. BMC Genomics 10: 547.
27. Deschamps S, Rota M, Ratashak JP, Biddle P, Thureen D, et al. (2010) Rapid genome-wide single nucleotide polymorphism discovery in soybean and rice via deep resequencing of reduced representation libraries with the Illumina Genome Analyzer. Plant Genome 3: 53-68.
28. Garg R, Patel RK, Jhanwar S, Priya P, Bhattacharjee A, et al. (2011) Gene discovery and tissue-specific transcriptome analysis in chickpea with massively parallel pyrosequencing and web resource development. Plant Physiol 156: 1661-1678.
29. Hiremath PJ, Farmer A, Cannon SB, Woodward J, Kudapa H, et al. (2011) Large-scale transcriptome analysis in chickpea (Cicer arietinum L.), an orphan legume crop of the semi-arid tropics of Asia and Africa. Plant Biotechnol J 9: 922-931.
30. Troncoso-Ponce MA, Kilaru A, Cao X, Durrett TP, Fan J, et al. (2011) Comparative deep transcriptional profiling of four developing oilseeds. Plant J 68: 1014-1027.
31. Sun Y, Wang F, Wang N, Dong Y, Liu Q, et al. (2013) Transcriptome exploration in Leymus chinensis under saline-alkaline treatment using 454 pyrosequencing. PLoS One 8(1): e53632.
32. Burge SW, Daub J, Eberhardt R, Tate J, Barquist L, et al. (2013) Rfam 11.0: 10 years of RNA families. Nucleic Acids Res 41: D226-232.
33. Nawrocki EP, Kolbe DL, Eddy SR, (2009) Infernal 1.0: inference of RNA alignments. Bioinformatics 25: 1335-1337.
34. Alagna F, D'Agostino N, Torchia L, Servili M, Rao R, et al. (2009) Comparative 454 pyrosequencing of transcripts from two olive genotypes during fruit development. BMC Genomics 10: 399.
35. Barakat A, DiLoreto DS, Zhang Y, Smith C, Baier K, et al. (2009) Comparison of the transcriptomes of American chestnut (Castanea dentata) and Chinese chestnut (Castanea mollissima) in response to the chestnut blight infection. BMC Plant Biol 9: 51.
36. Wang W, Wang Y, Zhang Q, Qi Y, Guo D, (2009) Global characterization of Artemisia annua glandular trichome transcriptome using 454 pyrosequencing. BMC Genomics 10: 465.
37. Sun C, Li Y, Wu Q, Luo H, Sun Y, et al. (2010) De novo sequencing and analysis of the American ginseng root transcriptome using a GS FLX Titanium platform to discover putative genes involved in ginsenoside biosynthesis. BMC Genomics 11: 262.
38. Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkerts O, et al. (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43: 109-116.
39. Der JP, Barker MS, Wickett NJ, dePamphilis CW, Wolf PG, (2011) De novo characterization of the gametophyte transcriptome in bracken fern, Pteridium aquilinum. BMC Genomics 12: 99.
40. Palmer NA, Saathoff AJ, Kim J, Benson A, Tobias CM, et al. (2011) Next-generation sequencing of crown and rhizome transcriptome from an upland, tetraploid switchgrass. Bioenerg Res 5: 649-661.
41. Wang Y, Zeng X, Iyer NJ, Bryant DW, Mockler TC, et al. (2012) Exploring the switchgrass transcriptome using second-generation sequencing technology. PLoS One 7: e34225.
42. He R, Kim MJ, Nelson W, Balbuena TS, Kim R, et al. (2012) Next-generation sequencing-based transcriptomic and proteomic analysis of the common reed, Phragmites australis (Poaceae), reveals genes involved in invasiveness and rhizome specificity. Am J Bot 99: 232-247.
43. Kumar S, Blaxter ML, (2010) Comparing de novo assemblers for 454 transcriptome data. BMC Genomics 11: 571.
44. Novaes E, Drost DR, Farmerie WG, Pappas GJ Jr, Grattapaglia D, et al. (2008) High-throughput gene and SNP discovery in Eucalyptus grandis, an uncharacterized genome. BMC Genomics 9: 312.
45. Meyer E, Aglyamova GV, Wang S, Buchanan-Carter J, Abrego D, et al. (2009) Sequencing and de novo analysis of a coral larval transcriptome using 454 GS Flx. BMC Genomics 10: 219.
46. Moellering ER, Muthan B, Benning C, (2010) Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330: 226-228.
47. Reyes JC, (2006) Chromatin modifiers that control plant development. Curr Opin Plant Biol 9: 21-27.
48. Wood CC, Robertson M, Tanner G, Peacock WJ, Dennis ES, et al. (2006) The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc Natl Acad Sci USA 103: 14631-14636.
49. Zhu J, Jeong JC, Zhu Y, Sokolchik I, Miyazaki S, et al. (2008) Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance. Proc Natl Acad Sci USA 105: 4945-4950.
50. Chinnusamy V, Zhu JK, Sunkar R, (2010) Gene regulation during cold stress acclimation in plants. Methods Mol Biol 639: 39-55.
51. Novillo F, Medina J, Salinas J, (2007) Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proc Natl Acad Sci USA 104: 21002-21007.
52. Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF, (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41: 195-211.
53. Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, et al. (2004) Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J 38: 982-93.
54. Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, et al. (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17: 1043-1054.
55. Fursova OV, Pogorelko GV, Tarasov VA, (2009) Identification of ICE2, a gene involved in cold acclimation which determines freezing tolerance in Arabidopsis thaliana. Gene 429: 98-103.
56. Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H, et al. (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281: 37636-37645.
57. Zhu J, Verslues PE, Zheng X, Lee BH, Zhan X, et al. (2005) HOS10 encodes an R2R3-type MYB transcription factor essential for cold acclimation in plants. Proc Natl Acad Sci USA 102: 9966-9971.
58. Xiong L, Lee H, Ishitani M, Tanaka Y, Stevenson B, et al. (2002) Repression of stress-responsive genes by FIERY2, a novel transcriptional regulator in Arabidopsis. Proc Natl Acad Sci USA 99: 10899-10904.
59. Lee H, Guo Y, Ohta M, Xiong L, Stevenson B, et al. (2002) LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase. EMBO J 21: 2692-2702.
60. Xin Z, Mandaokar A, Chen J, Last R, Browse J, (2007) Arabidopsis ESK1 encodes a novel regulator of freezing tolerance. Plant J 49: 786-799.
61. Skinner JS, von Zitzewitz J, Szucs P, Marquez-Cedillo L, Filichkin T, et al. (2005) Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol Biol 59: 533-551.
62. Vannini C, Locatelli F, Bracale M, Magnani E, Marsoni M, et al. (2004) Overexpression of the rice Osmyb4 gene increases chilling and freezing tolerance of Arabidopsis thaliana plants. Plant J 37: 115-127.
63. Tautz D, Domazet-Lošo T, (2011) The evolutionary origin of orphan genes. Nat Rev Genet 12: 692-702.
64. Kaessmann H, (2010) Origins, evolution, and phenotypic impact of new genes. Genome Res 20: 1313-1326.
65. Long M, Betrán E, Thornton K, Wang W, (2003) The origin of new genes: glimpses from the young and old. Nature Rev Genet 4: 865-875.
66. Zhou Q, Wang W, (2008) On the origin and evolution of new genes-a genomic and experimental perspective. J Genet Genomics 35: 639-648.
67. Cho YG, Ishii T, Temnykh S, Chen X, Lipovich L, et al. (2000) Diversity of microsatellites derived from genomic libraries and GenBank sequences in rice (Oryza sativa L.). Theor Appl Genet 100: 713-722.
68. Gupta PK, Rustgi S, Sharma S, Singh R, Kumar N, et al. (2003) Transferable EST-SSRs markers for the study of polymorphism and genetic diversity in bread wheat. Mol Gen Genet 270: 315-323.
69. Thiel T, Michalek W, Varshney RK, Graner A, (2003) Exploiting EST databases for the development and characterization of genederived SSR markers in barley (Hordeum vulgare L.). Theor Appl Genet 106: 411-422.
70. Cordeiro GM, Casu R, McIntyr CL, Manners JM, Henry RJ, (2001) Microsatellite markers from sugarcane (Saccharum spp.) ESTs cross transferable to erianthus and sorghum. Plant Sci 160: 1115-1123.
71. Bushman BS, Larson SR, Mott IW, Cliften PF, Wang RR, et al. (2008) Development and annotation of perennial Triticeae ESTs and SSR markers. Genome 51: 779-88.
72. Victoria FC, da Maia LC, de Oliveira AC, (2011) In silico comparative analysis of SSR markers in plants. BMC Plant Biol 11: 15.
73. La Rota M, Kantety RV, Yu JK, Sorrells ME, (2005) Nonrandom distribution and frequencies of genomic and EST-derived microsatellite markers in rice, wheat, and barley. BMC Genomics 6: 23.
74. Maia LC, Souza VQ, Kopp MM, Carvalho FIF, Oliveira AC, (2009) Tandem repeat distribution of gene transcripts in three plant families. Genet Mol Biol 32: 1-12.
75. Young ET, Sloan JS, Van Riper K, (2000) Trinucleotide repeats are clustered in regulatory genes in Saccharomyces cerevisiae. Genetics 154: 1053-1068.
76. Li YC, Korol AB, Fahima T, Nevo E, (2004) Microsatellites within genes: structure, function, and evolution. Mol Biol Evol 21: 991-1007.
77. Wang RR-C, Jensen KB, (1994) Absence of the J genome in Leymus species (Poaceae: Triticeae): evidence from DNA hybridization and meiotic pairing. Genome 37: 231-235.
78. Sha LN, Yang RW, Fan X, Wang XL, Zhou YH, (2008) Phylogenetic analysis of Leymus (Poaceae: Triticeae) inferred from nuclear rDNA ITS sequences. Biochem Genet 46: 605-619.
79. Zhang HB, Dvorak J, (1991) The genome origin of tetraploid species of Leymus (Poaceae: Triticeae) inferred from variation in repeated nucleotide sequences. Am J Bot 78: 871-884.
80. Fan X, Sha LN, Yang RW, Zhang HQ, Kang HY, et al. (2009) Phylogeny and evolutionary history of Leymus (Triticeae; Poaceae) based on a single-copy nuclear gene encoding plastid acetyl-CoA carboxylase. BMC Evol Biol 9: 247.
81. Bossolini E, Wicker T, Knobel PA, Keller B, (2007) Comparison of orthologous loci from small grass genomes Brachypodium and rice: Implications for wheat genomics and grass genome annotation. Plant J 49: 704-717.
82. International Brachypodium Initiative, (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463: 763-768.
83. Chalupska D, Lee HY, Faris JD, Evrard A, Chalhoub B, et al. (2008) Acc homoeoloci and the evolution of wheat genomes. Proc Natl Acad Sci USA 105: 9691-9696.
84. Rice P, Longden I, Bleasby A, (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16: 276-277.
85. Chen ZZ, Xue CH, Zhu S, Zhou FF, Xenfeng BL, et al. (2005) GoPipe: streamlined gene ontology annotation for batch anonymous sequences with statistics. Prog Biochem Biophys 32: 187-190.
86. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M, (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35: W182-W185.
87. Mao X, Cai T, Olyarchuk JG, Wei L, (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21: 3787-3793.
88. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628.
89. Vogel JP, Gu YQ, Twigg P, Lazo GR, Laudencia-Chingcuanco D, et al. (2006) EST sequencing and phylogenetic analysis of the model grass Brachypodium distachyon. Theor Appl Genet 113: 186-195.