Transcriptome sequencing of essential marine brown and red algal species in China and its significance in algal biology and phylogeny

Acta Oceanologica Sinica

Volumn 33, Issue 2, 2014, Pages 1-12

  Wu, Shuangxiu ^a   Sun, Jing ^a,c   Chi, Shan ^b   Wang, Liang ^a,c   Wang, Xumin ^a   Liu, Cui ^b   Li, Xingang ^a   Yin, Jinlong ^a   Liu, Tao ^b   Yu, Jun ^a  

^a China National Center for Bioinformation   (China)

^b OCEAN UNIVERSITY OF CHINA   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Brown algae; Marine macroalgae; Phaeophyceae; Red algae; Rhodophyta; Secondary generation sequencing; Transcriptome sequencing

Indexed keywords

EID: 84899033121     PISSN: 0253505X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s13131-014-0435-4     Document Type: Article

References (84)

1. Agarwal P K, Agarwal P, Jain P, et al. 2008. Constitutive overexpression of a stress-inducible small GTP-binding protein PgRab7 from Pennisetum glaucum enhances abiotic stress tolerance in transegene tabacco. Plant Cell Rep, 27: 105-115 (Pubitemid 350242822)
2. Armbrust E V, Berges J A, Bowler C, et al. 2004. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science, 306(5693): 79-86 (Pubitemid 39451941)
3. Baldauf S L. 2008. An overview of the phylogeny and diversity of eukaryotes. Journal of Systematics and Evolution, 46: 263-273
4. Bartsch I, Wiencke C, Bischof K, et al. 2008. The genus Laminaria sensu lato: recent insights and developments. Euro J of Phycol, 43: 1-86 (Pubitemid 351239664)
5. Ben Ali A, De Baere R, Van der Auwera G, et al. 2001. Phylogenetic relationships among algae based on complete large-subunit rRNA sequences. International Journal of Systematic and Evolutionary Microbiology, 51: 737-749 (Pubitemid 32499274)
6. Berteau O, Mulloy B. 2003. Sulfated fucans, fresh perspectives: Structures, functions, and biological properties of sulfated fucans and an overview of enzymes active toward this class of polysaccharide. Glycobiology, 13(6): 29R-40R (Pubitemid 36665414)
7. Blanc G, Agarkova I, Grimwood J, et al. 2012. The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biol, 13(5): R39
8. Blanc G, Duncan G, Agarkova I, et al. 2010. The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell, 22(9): 2943-2955
9. Bolte S, Schiene K, Dietz K, et al. 2000. Characterization of a small GTP-binding protein of the rab5 family in Mesembryanthemum crystallium with increased level of expression during early salt stress. Plant Mol Biol, 42: 923-936 (Pubitemid 30409653)
10. Bowler C, Allen A E, Badger J H, et al. 2008. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature, 456(7219): 239-244
11. Butler A, Carter-Franklin J N. 2004. The role of vanadium bromoperoxidase in the biosynthesis of halogenated marine natural products. Nat Prod Rep, 21(1): 180-188 (Pubitemid 38260880)
12. Cavalier-Smith T. 2010. Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree. Biol Lett, 6(3): 342-345
13. Cho G Y, Rousseau F, de Reviers B, et al. 2006. Phylogenetic relationships within the Fucales (Phaeophyceae) assessed by the photosystem I coding psaA sequences. Phycologia, 45: 512-519 (Pubitemid 44360085)
14. Cock J M, Arun A, Godfroy O, et al. 2012. Genomics of brown algae: current advances and future prospects. Genes & Genomics, 34(1): 1-5
15. Cock J M, Sterck L, Rouz P, et al. 2010. The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature, 465(7298): 617-621
16. Collén J, Porcel B, Carr W, et al. 2013. Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida. Proc Natl Acad Sci U S A, 110(13): 5247-5252
17. Curtis B A, Tanifuji G, Burki F, et al. 2012. Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature, 492: 59-65
18. Delwiche C F, Palmer J D. 1996. Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids. Mol Biol Evol, 13: 873-882 (Pubitemid 26240091)
19. Deng Yunyan, Yao Jianting, Wang Xiuliang, et al. 2012. Transcriptome sequencing and comparative analysis of Saccharina japonica (Laminariales, Phaeophyceae) under blue light induction. PLoS One, 7(6): e39704
20. Derelle E, Ferraz C, Lagoda P, et al. 2002. DNA libraries for sequencing the genome of Ostreococcus tauri (chlorophyta, prasinophyceae): the smallest free-living eukaryotic cell. J Phycol, 38: 1150-1156 (Pubitemid 36035659)
21. Dittami S M, Scornet D, Petit J L, et al. 2009. Global expression analysis of the brown alga Ectocarpus siliculosus (Phaeophyceae) reveals large-scale reprogramming of the transcriptome in response to abiotic stress. Genome Biol, 10(6): R66
22. Drury J L, Dennis R G, Mooney D J. 2003. The tensile properties of alginate hydrogels. Biomaterials, 25(l6): 3187-3199 (Pubitemid 38234780)
23. Dufosséa L, Galaupa P, Yaronb A. 2005. Microorganisms and microalgae as sources of pigments for food use: a scientific oddity or an industrial reality. Trends in Food Science and Technology, 16: 389-406
24. Falkowski P G, Raven J A. 1997. Aquatic Photosynthesis. Malden, MA: Blackwell Science
25. Ghangal R, Raghuvanshi S, Chand Sharma P, et al. 2009. Isolation of good quality RNA from a medicinal plant seabuckthorn, rich in secondary metabolites. Plant Physiology and Biochemistry, 47: 1113-1115
26. Glazer A N. 1997. Phycobiliproteins: A family of valuable, widely used fluorophores. Scanning, 19: 154-155 (Pubitemid 127491980)
27. Gobler C J, Berry D L, Dyhrman S T, et al. 2011. Niche of harmful alga Aureococcus anophagefferens revealed through ecogenomics. Proc Natl Acad Sci USA, 108(11): 4352-4357
28. Gould S B, Waller R F, McFadden G I. 2008. Plastid evolution. Annu Rev Plant Biol, 59: 491-517 (Pubitemid 351813040)
29. Green B. 2011. After the primary endosymbiosis: an update on the chromalveolate hypothesis and the origins of algae with Chl c. Photosynth Res, 107: 103-115
30. Grosberg R K, Strathmann R R. 2007. The evolution of multicellularity: a minor major transition? Annual Review of Ecology, Evolution, and Systematics, 38: 621-654
31. Grossman A R. 2007. In the grip of algal genomics. Adv Exp Med Biol, 616: 54-76
32. Heinrich S, Valentin K, Frickenhaus S, et al. 2012. Transcriptomic Analysis of Acclimation to Temperature and Light Stress in Saccharina latissima (Phaeophyceae). PLoS ONE, 7: e44342
33. Huovinen P, Gomez I, Lovengreen C. 2006. A five-year study of solar ultraviolet radiation in southern Chile (39 degrees S): potential impact on physiology of coastal marine algae? Photochemistry and Photobiology, 82(2): 515-522
34. Jia Shangang, Wang Xumin, Li Tianyong, et al. 2014a. Phylogenomic analysis of transcriptomic sequences of mitochondria and chloroplasts of essential brown algae (Phaeophyceae) in China. Acta Oceanologica Sinica, 33(2): 94-101
35. Jia Shangang, Wang Xumin, Qian Hao, et al. 2014b. Phylogenomic analysis of transcriptomic sequences of mitochondria and chloroplasts for marine red algae (Rhodophyta) in China. Acta Oceanologica Sinica, 33(2): 86-93
36. Johnson M T, Carpenter E J, Tian Z, et al. 2012. Evaluating methods for isolating total RNA and predicting the success of sequencing phylogenetically diverse plant transcriptomes. PLoS One, 7(11): e50226
37. Kawai H, Sasaki H, Maeba S, et al. 2005. Morphology and molecular phylogeny of Phaeostrophion irregulare (Phaeophyceae) with a proposal for Phaeostrophiaceae fam. nov., and a review of Ishigeaceae. Phycologia, 44: 169-182 (Pubitemid 40690000)
38. Küpper F C, Schweigert N, Ar Gall E, et al. 1998. Iodine uptake in Laminariales involves extracellular, haloperoxidase-mediated oxidation of iodide. Planta, 207(2): 163-171 (Pubitemid 29051679)
39. Kutschera U, Niklas K J. 2005. Endosymbiosis, cell evolution and speciation. Theory Biosci, 124: 1-24
40. Kutschera U, Niklas K J. 2008. Macroevolution via secondary endosymbiosis: a Neo-Goldschmidtian view of unicellular hopeful monsters and Darwin's primordial intermediate form. Theory Biosci, 127: 277-289
41. Lane C E, Mayes C, Druehl L D, et al. 2006. A multi-gene molecular investigation of the kelp (Laminariales, Phaeophyceae) supports substantial taxonomic re-organization. Journal of Phycology, 42: 493-512
42. Li Tianyong, Ren Lei, Zhou Guan, et al. 2012. A suitable method for extracting total RNA from red algae. Transactions of Oceanology and Limnology (in Chinese), 4: 64-71
43. Li Ruiqiang, Zhu Hongmei, Ruan Jue, et al. 2010. De novo assembly of human genomes with massively parallel short read sequencing. Genome Research, 20: 265-272
44. Liang Chengwei, Zhang Xiaowen, Zou Jian, et al. 2010. Identification of miRNA from Porphyra yezoensis by high-throughput sequencing and bioinformatics analysis. PLoS One, 5(5): e10698
45. Lommer M, Specht M, Roy A S, et al. 2012. Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation. Genome Biol, 13(7): R66
46. Matsubara K. 2004. Recent advances in marine algal anticoagulants. Curr Med Chem Cardiovasc Hematol Agents, 2(1): 13-19 (Pubitemid 38854965)
47. Matsuzaki M, Misumi O, Shin-I T, et al. 2004. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature, 428(6983): 653-657 (Pubitemid 38524807)
48. Merchant S S, Prochnik S E, Vallon O, et al. 2007. The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science, 318: 245-250
49. Misumi O, Yoshida Y, Nishida K, et al. 2008. Genome analysis and its significance in four unicellular algae, Cyanidioschyzon [corrected] merolae, Ostreococcus tauri, Chlamydomonas reinhardtii, and Thalassiosira pseudonana. J Plant Res, 121(1): 3-17
50. Moreau H, Verhelst B, Couloux A, et al. 2012. Gene functionalities and genome structure in Bathycoccus prasinos reflect cellular specializations at the base of the green lineage. Genome Biology, 13: R74
51. Moriya Y, Itoh M, Okuda S, et al. 2007. KAAS: an automatic genome annotation and pathway reconstruction server. Nuleic Acids Res, 35: W182-W185
52. Nakamura Y, Sasaki N, Kobayashi M, et al. 2013. The First Symbiont-Free Genome Sequence of Marine Red Alga, Susabi-nori (Pyropia yezoensis). PLoS ONE 8(3): e57122, doi:10.1371/journal.pone.0057122
53. Nyvall P, Corre E, Boisset C, et al. 2003. Characterization of mannuronan C-5-epimerase genes from the brown alga Laminaria digitata. Plant Physiol, 133(2): 726-735. (Pubitemid 37325682)
54. Palenik B, Grimwood J, Aerts A, et al. 2007. The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc Natl Acad Sci USA, 104(18): 7705-7710 (Pubitemid 47185970)
55. Pan Kehou, Qin Junjie, Li Si, et al. 2011. Nuclear monoploidy and asexual propagation of Nannochloropsis oceanica (Eustigmatophyceae) as revealed by its genome sequence. J Phycol, 47(6): 1425-1432
56. Parker M S, Mock T, Armbrust E V. 2008. Genomic insights into marine microalgae. Annu Rev Genet, 42: 619-645
57. Price D C, Chan C X, Yoon H S, et al. 2012. Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science, 335(6070): 843-847
58. Prochnik S E, Umen J, Nedelcu A M, et al. 2010. Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science, 329(5988): 223-226
59. Qu Jieqiong, Wang Xumin, Chi Shan, et al. 2014. Transcriptome characterization of Ishige okamurae (Phaeophyceae) shows strong environmental acclimation. Acta Oceanologica Sinica, 33(2): 20-26
60. Radakovits R, Jinkerson R E, Fuerstenberg S I, et al. 2012. Draft genome sequence and genetic transformation of the oleaginous alga Nannochloropis gaditana. Nat Commun, 3: 686-695
61. Raj N K, Sharma C P. 2003. Oral insulin - a perspective. J Biomater Appl, 17(3): 183-196
62. Read B A, Kegel J, Klute M J, et al. 2013. Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature, 499(7457): 209-213
63. Reyes-Prieto A, Weber A P, Bhattacharya D. 2007. The origin and establishment of the plastid in algae and plants. Annual Review of Genetics, 41: 147-168
64. Rousvoal S, Groisillier A, Dittami S M, et al. 2011. Mannitol-1-phosphate dehydrogenase activity in Ectocarpus siliculosus, a key role for mannitol synthesis in brown algae. Planta, 233: 261-273
65. Rudolph B. 2000. Seaweed products: red algae of economic significance. In: Martin R E, Carter E P, Davis L M, et al., eds. Marine and Freshwater Products Handbook. Lancarster, UK: Technomic Publishing Co, 515-529
66. Schönknecht G, Chen W H, Temes C M, et al. 2013. Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science, 339: 1207-1210
67. Shih C M, Cheng S N, Wong C S, et al. 2009. Antiinflammatory and antihyperalgesic activity of C-phycocyanin. Anesthesia and Analgesia, 108(4): 1303-1310
68. Silberfeld T, Leigh J W, Verbruggen H, et al. 2010. A multi-locus time-calibrated phylogeny of the brown algae (Heterokonta, Ochrophyta, Phaeophyceae): Investigating the evolutionary nature of the "brown algal crown radiation. Molecular Phylogenetics and Evolution, 56: 659-674
69. Simon N, Cras A L, Foulon E, et al. 2009. Diversity and evolution of marine phytoplankton. C R Biol, 332: 159-170
70. Song Lipu, Wu Shuangxiu, Sun Jing, et al., 2014. De novo sequencing and comparative analysis of three red algal species of Family Solieriaceae to discover putative genes associated with carrageenan biosysthesis. Acta Oceanologica Sinica, 33(2): 45-53
71. Sun Jing, Wang Liang, Wu Shuangxiu, et al. 2014. Transcriptome-wide evolutionary analysis on essential brown algae (Phaeophyceae) in China. Acta Oceanologica Sinica, 33(2): 13-19
72. Tatusov R L, Fedorova N D, Jackson J D, et al. 2003. The COG database: an updated version includes eukaryotes. BMC Bioinformatics, 4: 41
73. Tenhaken R, Voglas E, Cock J M, et al. 2011. Characterization of GDPmannose dehydrogenase from the brown alga Ectocarpus siliculosus providing the precursor for the alginate polymer. J Biol Chem, 286(19): 16707-16715
74. Tirichine L, Bowler C. 2011. Decoding algal genomes: tracing back the history of photosynthetic life on Earth. Plant J, 66(1): 45-57
75. Wang Hongwei, Kawaguchi S, Horiguchi T, et al. 2001. A morphological and molecular assessment of the genus Prionitis J. Agardh (Halymeniaceae, Rhodophyta). Phycological Research, 49(3): 251-261
76. Wang Ren, Wang Xumin, Zhang Yalan, et al. 2014. Origin and evolution of alginate-c5-mannuronan-epimerase gene based on transcriptomic analysis of brown algae. Acta Oceanologica Sinica, 33(2): 73-85
77. Wang Liang, Wu Shuangxiu, Liu Tao, et al. 2014 Endogenous Viral Elements in Algal Genomes. Acta Oceanologica Sinica, 33(2): 102-107
78. Weber A P M, Oesterhelt C, Gross W, et al. 2004. EST-analysis of the thermo-acidophilic red microalga Galdieria sulphuraria reveals potential for lipid A biosynthesis and unveils the pathway of carbon export from rhodoplasts. Plant Mol Biol, 55: 17-32
79. Worden A Z, Lee J H, Mock T, et al. 2009. Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science, 324(5924): 268-272
80. Xu Jia, Aileni M, Abbagani S, et al. 2010. A reliable and efficient method for total RNA isolation from various members of spurge family (Euphorbiaceae). Phytochemical Analysis, 21: 395-398
81. Xu Jiayue, Sun Jing, Yin Jinlong, et al. 2014. Comparative analysis of four essential Gracilariaceae species in China based on whole transcriptomic sequencing. Acta Oceanologica Sinica, 33(2): 54-62
82. Yao Jianting, Fu Wandong, Wang Xiuliang. 2009. Improved RNA isolation from Laminaria japonica Aresch (Laminariaceae, Phaeophyta). Appl Phycol, 21: 233-238
83. Zdobnov E M, Apweiler R. 2001. InterProScan - an integration platform for the signature-recognition methods in InterPro. Bioinformatics, 17(9): 847-848 (Pubitemid 32970486)
84. Zhang Junfu, Xia Bangmei. 1992. Studies on two new Gracilaria from South China and a summary of Gracilaria species in China. Taxonomy of Economic Seaweeds, 3: 195-206