Next-generation sequencing-based transcriptomic and proteomic analysis of the common reed, Phragmites australis (Poaceae), reveals genes involved in invasiveness and rhizome specificity

American Journal of Botany

Volumn 99, Issue 2, 2012, Pages 232-247

  He, Ruifeng ^a   Kim, Min Jeong ^a   Nelson, William ^b   Balbuena, Tiago S ^c   Kim, Ryan ^d   Kramer, Robin ^d   Crow, John A ^d   May, Greg D ^d   Thelen, Jay J ^c   Soderlund, Carol A ^b   Gang, David R ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c University of Missouri   (United States)

^d NATIONAL CENTER FOR GENOME RESOURCES   (United States)

Author keywords

Allelopathy; Apical dominance; De novo assembly; Invasiveness; Next generation sequencing; Phragmites australis; Proteome; Rhizome; Transcriptome; Weediness

Indexed keywords

PLANT RNA; TRANSCRIPTION FACTOR; TRANSCRIPTOME; VEGETABLE PROTEIN;

ADVANCED TECHNOLOGY; ALLELOPATHY; GENE; GEOGRAPHICAL DISTRIBUTION; INVASIVENESS; MITOCHONDRIAL DNA; PROTEIN; PROTEOMICS; REEDBED; RHIZOME; TERRITORY; WEED;

ARTICLE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC DATABASE; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTRODUCED SPECIES; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MERISTEM; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLANT GENE; POACEAE; PROTEOMICS; RHIZOME; SEQUENCE ANALYSIS; SPECIES DIFFERENCE;

BASE SEQUENCE; CHROMATOGRAPHY, LIQUID; DATABASES, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; INTRODUCED SPECIES; MASS SPECTROMETRY; MERISTEM; MOLECULAR SEQUENCE ANNOTATION; PLANT PROTEINS; POACEAE; PROTEOMICS; RHIZOME; RNA, PLANT; SEQUENCE ANALYSIS, RNA; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

MAGNOLIOPHYTA; PHRAGMITES AUSTRALIS; POACEAE;

EID: 84863338285     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1100429     Document Type: Article

References (73)

1. ADAMIDI, C., Y. WANG, D. GRUEN, G. MASTROBUONI, X. YOU, D. TOLLE, M. DODT, et al. 2011. title typecontributorDe novo assembly and validation of planaria transcriptome by massive parallel sequencing and shotgun proteomics/title. Genome Research 21: 1193-1200.
2. AL-DOUS, E. K., B. GEORGE, M. E. AL-MAHMOUD, M. Y. AL-JABER, H. WANG, Y. M. SALAMEH, E. K. AL-AZWANI, et al. 2011. De novo genome sequencing and comparative genomics of date palm (Phoenix dactylifera). Nature Biotechnology 29: 521-527.
3. ALTSCHUL, S. F., T. L. MADDEN, A. A. SCHAFFER, J. ZHANG, Z. ZHANG, W. MILLER, and D. J. LIPMAN. 1997. Gapped BLAST and PSIBLAST: A new generation of protein database search programs. Nucleic Acids Research 25: 3389-3402.
4. AMSBERRY, L., M. A. BAKER, P. J. EWANCHUK, and M. D. BERTNESS. 2000. Clonal integration and the expansion of Phragmites australis. Ecological Applications 10: 1110-1118.
5. APWEILER, R., M. J. MARTIN, C. O'DONOVAN, M. MAGRANE, Y. AL-AMFARUQUE, R. ANTUNES, D. BARRELL, et al. 2010. The Universal Protein Resource (UniProt) in 2010. Nucleic Acids Research 38: D142-D148.
6. APWEILER, R., M. J. MARTIN, C. O 'DONOVAN, M. MAGRANE, Y. ALAMFARUQUE, R. ANTUNES, D. BARRELL, et al. 2011. Ongoing and future developments at the Universal Protein Resource. Nucleic Acids Research 39: D214-D219.
7. ASHBURNER, M., C. A. BALL, J. A. BLAKE, D. BOTSTEIN, H. BUTLER, J. M. CHERRY, A. P. DAVIS, et al. 2000. Gene Ontology: Tool for the unification of biology. The Gene Ontology Consortium. Nature Genetics 25: 25-29.
8. BATTY, L. C., and P. L. YOUNGER. 2003. Effects of external iron concentration upon seedling growth and uptake of Fe and phosphate by the common reed, Phragmites australis (Cav.) Trin ex. Steudel. Annals of Botany 92: 801-806.
9. BERKOWITZ, O., R. JOST, S. POLLMANN, and J. MASLE. 2008. Characterization of TCTP, the translationally controlled tumor protein, from Arabidopsis thaliana. Plant Cell 20: 3430-3447.
10. BIROL, I., S. D. JACKMAN, C. B. NIELSEN, J. Q. QIAN, R. VARHOL, G. TAZYK, R. D. MORIN, et al. 2009. De novo transcriptome assembly with ABySS. Bioinformatics 25: 2872-2877.
11. BOHLMANN, H., and K. APEL. 1991. Thionins. Annual Review of Plant Physiology and Plant Molecular Biology 42: 227-240.
12. BOHLMANN, H., S. CLAUSEN, S. BEHNKE, H. GIESE, C. HILLER, U. EIMANNPHILIPP, G. SCHRADER, et al. 1988. Leaf-specific thionins of barley - A novel class of cell wall proteins toxic to plant-pathogenic fungi and possibly involved in the defence mechanism of plants. EMBO Journal 7: 1559-1565.
13. BRAUTIGAM, A., T. MULLICK, S. SCHLIESKY, and A. P. M. WEBER. 2011. Critical assessment of assembly strategies for non-model species mRNA-Seq data and application of next-generation sequencing to the comparison of C 3 and C 4 species. Journal of Experimental Botany 62: 3093-3102.
14. BRIX, H. 1999. Genetic diversity, ecophysiology and growth dynamics of reed (Phragmites australis)- Introduction. Aquatic Botany 64: 179-184.
15. CALLAWAY, R. M., and E. T. ASCHEHOUG. 2000. Invasive plants versus their new and old neighbors: A mechanism for exotic invasion. Science 290: 521-523.
16. CARNINCI, P. 2009. Is sequencing enlightenment ending the dark age of the transcriptome? Nature Methods 6: 711-713.
17. CHEVREUX, B., T. PFISTERER, B. DRESCHER, A. J. DRIESEL, W. E. MULLER, T. WETTER, and S. SUHAI. 2004. Using the mira EST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Research 14: 1147-1159.
18. CONESA, A., S. GOTZ, J. M. GARCIA-GOMEZ, J. TEROL, M. TALON, and M. ROBLES. 2005. Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
19. COX, T. S., J. D. GLOVER, D. L. VAN TASSEL, C. M. COX, and L. R. DEHAAN. 2006. Prospects for developing perennial-grain crops. BioScience 56: 649-659.
20. DALLOUL, R. A., J. A. LONG, A. V. ZIMIN, L. ASLAM, K. BEAL, A. BLOMBERG LE, P. BOUFFARD, et al. 2010. Multi-platform next-generation sequencing of the domestic turkey (Meleagris gallopavo): Genome assembly and analysis. PLoS Biology 8: e1000475. doi:10.1371/journal.pbio.1000475.
21. DER, J. P., M. S. BARKER, N. J. W ICKETT, C. W. DEPAMPHILIS, and P. G. WOLF. 2011. De novo characterization of the gametophyte transcriptome in bracken fern, Pteridium aquilinum. BMC Genomics 12: 99.
22. DU LAING, G., F. M. G. TACK, and M. G. VERLOO. 2003. Performance of selected destruction methods for the determination of heavy metals in reed plants (Phragmites australis). Analytica Chimica Acta 497: 191-198.
23. FANG, Z., and X. CUI. 2011. Design and validation issues in RNA-seq experiments. Briefings in Bioinformatics 12: 280-287.
24. FU, X., S. A. GHARIB, P. S. GREEN, M. L. AITKEN, D. A. FRAZER, D. R. PARK, T. VAISAR, et al. 2008. Spectral index for assessment of differential protein expression in shotgun proteomics. Journal of Proteome Research 7: 845-854.
25. GARG, R., R. K. PATEL, S. JHANWAR, P. PRIYA, A. BHATTACHARJEE, G. YADAV, S. BHATIA, et al. 2011a. Gene discovery and tissue-specific transcriptome analysis in chickpea with massively parallel pyrosequencing and web resource development. Plant Physiology 156: 1661-1678.
26. GARG, R., R. K. PATEL, A. K. T YAGI, and M. JAIN. 2011b. De novo assembly of chickpea transcriptome using short reads for gene discovery and marker identification. DNA Research 18: 53-63.
27. GLOVER, J. D., J. P. REGANOLD, L. W. BELL, J. BOREVITZ, E. C. BRUMMER, E. S. BUCKLER, C. M. COX, et al. 2010. Increased food and ecosystem security via perennial grains. Science 328: 1638-1639.
28. GOLDBERG, R. B., G. HOSCHEK, J. C. KAMALAY, and W. E. TIMBERLAKE. 1978. Sequence complexity of nuclear and polysomal RNA in leaves of the tobacco plant. Cell 14: 123-131.
29. HOLM, L. G., D. L. PLUCKNETT, J. V. PANCHO, and J. P. HERBERGER. 1991. The world ' s worst weeds: Distribution and biology. University Press of Hawaii, Honolulu, Hawaii, USA.
30. HU, F., D. WANG, X. ZHAO, T. ZHANG, H. SUN, L. ZHU, F. ZHANG, et al. 2011. Identification of rhizome-specific genes by genome-wide differential expression analysis in Oryza longistaminata. BMC Plant Biology 11: 18.
31. HU, F. Y., D. Y. TAO, E. SACKS, B. Y. FU, P. XU, J. LI, Y. YANG, et al. 2003. Convergent evolution of perenniality in rice and sorghum. Proceedings of the National Academy of Sciences, USA 100: 4050-4054.
32. HUANG, S., R. LI, Z. ZHANG, L. LI, X. GU, W. FAN, W. J. LUCAS, et al. 2009. The genome of the cucumber, Cucumis sativus L. Nature Genetics 41: 1275-1281.
33. HUANG, X., and A. MADAN. 1999. CAP3: A DNA sequence assembly program. Genome Research 9: 868-877.
34. ISELI, C., C. V. JONGENEEL, and P. BUCHER. 1999. ESTScan: A program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. In Proceedings of the International Conference on Intelligent Systems for Molecular Biology, 138-148. American Association for the Advancement of Artificial Intelligence, Menlo Park, California, USA.
35. IWASAKI, M., and E. NITASAKA. 2006. The FEATHERED gene is requiredfor polarity establishment in lateral organs especially flowers of the Japanese morning glory (Ipomoea nil). Plant Molecular Biology 62: 913-925.
36. JANG, C. S., T. L. KAMPS, D. N. SKINNER, S. R. SCHULZE, W. K. VENCILL, and A. H. PATERSON. 2006. Functional classification, genomic organization, putatively cis -acting regulatory elements, and relationship to quantitative trait loci, of sorghum genes with rhizome-enriched expression. Plant Physiology 142: 1148-1159.
37. KAPTEYN, J., R. HE, E. T. MCDOWELL, and D. R. GANG. 2010. Incorporation of non-natural nucleotides into template-switching oligonucleotides reduces background and improves cDNA synthesis from very small RNA samples. BMC Genomics 11: 413.
38. KELLER, A., A. I. NESVIZHSKII, E. KOLKER, and R. AEBERSOLD. 2002. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Analytical Chemistry 74: 5383-5392.
39. KIRK, H., J. PAUL, J. STRAKA, and J. R. FREELAND. 2011. Long-distance dispersal and high genetic diversity are implicated in the invasive spread of the common reed, Phragmites australis (Poaceae), in northeastern North America. American Journal of Botany 98: 1180-1190.
40. LEAGUE, M. T., E. P. COLBERT, D. M. SELISKAR, and J. L. GALLAGHER. 2006. Rhizome growth dynamics of native and exotic haplotypes of Phragmites australis (common reed). Estuaries and Coasts 29: 269-276.
41. LEE, Y., and H. KENDE. 2001. Expression of beta-expansins is correlated with internodal elongation in deepwater rice. Plant Physiology 127: 645-654.
42. LI, H., and R. DURBIN. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
43. LI, R., C. YU, Y. LI, T. W. LAM, S. M. Y IU, K. K RISTIANSEN, and J. WANG. 2009. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25: 1966-1967.
44. LI, R. Q., W. FAN, G. TIAN, H. M. ZHU, L. HE, J. CAI, Q. F. HUANG, et al. 2010. The sequence and de novo assembly of the giant panda genome. Nature 463: 311-317.
45. LI, W., and A. GODZIK. 2006. Cd-hit: A fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659.
46. LI, Z. S., and T. L. THOMAS. 1998. PEI1, an embryo-specific zinc finger protein gene required for heart-stage embryo formation in Arabidopsis. Plant Cell 10: 383-398.
47. MCDOWELL, E. T., and D. R. GANG. In press. A dynamic model for phytohormone control of rhizome growth and development. Recent Advances in Phytochemistry.
48. MCDOWELL, E. T., J. KAPTEYN, A. SCHMIDT, C. LI, J. H. KANG, A. DESCOUR, F. SHI, et al. 2011. Comparative functional genomic analysis of Solanum glandular trichome types. Plant Physiology 155: 524-539.
49. MCSTEEN, P. 2009. Hormonal regulation of branching in grasses. Plant Physiology 149: 46-55.
50. PARCHMAN, T. L., K. S. GEIST, J. A. GRAHNEN, C. W. BENKMAN, and C. A. BUERKLE. 2010. Transcriptome sequencing in an ecologically important tree species: Assembly, annotation, and marker discovery. BMC Genomics 11: 180.
51. PATERSON, A. H., K. F. SCHERTZ, Y. R. LIN, S. C. LIU, and Y. L. CHANG. 1995. The weediness of wild plants - Molecular analysis of genes influencing dispersal and persistence of johnsongrass, Sorghum halepense (L) Pers. Proceedings of the National Academy of Sciences, USA 92: 6127-6131.
52. RENSING, S. A., D. LANG, A. D. ZIMMER, A. TERRY, A. SALAMOV, H. SHAPIRO, T. NISHIYAMA, et al. 2008. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319: 64-69.
53. RIZHSKY, L. 2002. The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiology 130: 1143-1151.
54. SAGE-ONO, K., M. ONO, H. HARADA, and H. K AMADA. 1998. Dark-induced accumulation of mRNA for a homolog of translationally controlled tumor protein (TCTP) in Pharbitis. Plant & Cell Physiology 39: 357-360.
55. SALTONSTALL, K. 2002. Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proceedings of the National Academy of Sciences, USA 99: 2445-2449.
56. SCHILMILLER, A. L., D. P. MINER, M. LARSON, E. MCDOWELL, D. R. GANG, C. WILKERSON, and R. L. LAST. 2010. Studies of a biochemical factory: Tomato trichome deep expressed sequence tag sequencing and proteomics. Plant Physiology 153: 1212-1223.
57. SHEVCHENKO, A., H. TOMAS, J. HAVLIS, J. V. OLSEN, and M. MANN. 2007. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nature Protocols 1: 2856-2860.
58. SHI, C.-Y., H. YANG, C.-L. WEI, O. YU, Z.-Z. ZHANG, C.-J. JIANG, J. SUN, et al. 2011. Deep sequencing of the Camellia sinensis transcriptome revealed candidate genes for major metabolic pathways of tea-specific compounds. BMC Genomics 12: 131.
59. SHULAEV, V., D. J. SARGENT, R. N. CROWHURST, T. C. MOCKLER, O. FOLKERTS, A. L. DELCHER, P. JAISWAL, et al. 2010. The genome of woodland strawberry (Fragaria vesca). Nature Genetics 43: 109-116.
60. SODERLUND, C., A. DESCOUR, D. KUDRNA, M. BOMHOFF, L. BOYD, J. CURRIE, A. ANGELOVA, et al. 2009a. Sequencing, mapping, and analysis of 27,455 maize full-length cDNAs. PLoS Genetics 5: e1000740. doi:10.1371/journal.pgen.1000740.
61. SODERLUND, C., E. JOHNSON, M. BOMHOFF, and A. DESCOUR. 2009b. PAVE: Program for assembling and viewing ESTs. BMC Genomics 10: 400.
62. SWINDELL, W. R., M. HUEBNER, and A. P. WEBER. 2007. Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genomics 8: 125.
63. THELEN, J. J., and S. C. PECK. 2007. Quantitative proteomics in plants: Choices in abundance. Plant Cell 19: 3339-3346.
64. VELASCO, R., A. ZHARKIKH, J. AFFOURTIT, A. DHINGRA, A. CESTARO, A. KALYANARAMAN, P. FONTANA, et al. 2010. The genome of the domesticated apple (Malus × domestica Borkh.). Nature Genetics 42: 833-839.
65. WALL, P. K., J. LEEBENS-MACK, A. S. CHANDERBALI, A. BARAKAT, E. WOLCOTT, H. LIANG, L. LANDHERR, et al. 2009. Comparison of next generation sequencing technologies for transcriptome characterization. BMC Genomics 10: 347.
66. WANG, X.-W., J.-B. LUAN, J.-M. LI, Y.-Y. BAO, C.-X. ZHANG, and S.-S. LIU. 2010. De novo characterization of a whitefly transcriptome and analysis of its gene expression during development. BMC Genomics 11: 400.
67. WANG, Z., B. FANG, J. CHEN, X. ZHANG, Z. LUO, L. HUANG, X. CHEN, et al. 2010. De novo assembly and characterization of root transcriptome using Illumina paired-end sequencing and development of cSSR markers in sweetpotato (Ipomoea batatas). BMC Genomics 11: 726.
68. WANG, Z., M. GERSTEIN, and M. SNYDER. 2009. RNA-Seq: A revolutionary tool for transcriptomics. Nature Reviews. Genetics 10: 57-63.
69. WEIS, J. S., and P. WEIS. 2003. Is the invasion of the common reed, Phragmites australis, into tidal marshes of the eastern US an ecological disaster? Marine Pollution Bulletin 46: 816-820.
70. WERNERSSON, R. 2006. Virtual Ribosome - A comprehensive DNA translation tool with support for integration of sequence feature annotation. Nucleic Acids Research 34: W385-W388.
71. XU, M., L. ZHU, H. X. SHOU, and P. WU. 2005. A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant & Cell Physiology 46: 1674-1681.
72. XU, X., S. PAN, S. CHENG, B. ZHANG, D. MU, P. NI, G. ZHANG, et al. 2011. Genome sequence and analysis of the tuber crop potato. Nature 475: 189-195.
73. ZHANG, H., J. JIN, L. TANG, Y. ZHAO, X. GU, G. GAO, and J. LUO. 2011. PlantTFDB 2.0: Update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Research 39 (supplement 1): D1114-D1117.