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DING Haiyan, GUO Li, LI Xiaojie, YANG Guanpin. Transcriptome analysis of kelp Saccharina japonica unveils its weird transcripts and metabolite shift of main components at different sporophyte developmental stages[J]. HaiyangYuHuZhao, 2019, 37(2): 640-650

Transcriptome analysis of kelp Saccharina japonica unveils its weird transcripts and metabolite shift of main components at different sporophyte developmental stages

DING Haiyan1, GUO Li1, LI Xiaojie2, YANG Guanpin3,4
1 College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China;
2 Shandong Oriental Ocean Sci-Tech Co., Ltd., Yantai 264003, China;
3 Key Laboratory of Marine Genetics and Breeding of Ministry of Education, Ocean University of China, Qingdao 266003, China;
4 Institutes of Evolution and Marine Biodiversity, Ocean University of China, Qingdao 266003, China
Saccharina japonica is an economically important cold water brown alga extensively cultivated in China. It is cultivated upside down under a floating rope net with its holdfast and meristematic area facing sunlight and UV irradiation and its blade tip toward dark, and other worse cultivation environmental factors also make S. japonica face more stresses. In this study, S. japonica transcriptomes corresponding to its four developmental stages were analyzed. In total, 7 800 genes predicted in the genome were transcribed. We found that 1 208 of the 7 800 expressed and 2 697 annotated were virus associating genes. Of 778 differentially expressed genes (DEGs), 372 were annotatable and 209 were virus associating. Such portion of virus associating genes indicated that the S. japonica genome contained a large portion of active virus originating genes. It was found that the transcripts abundance associated with sugar biosynthesis was about 2.13 folds of all the expressed, indicating that the biosyntheses of structural and storage sugars were very important cellular processes. The total abundance of genes involved in the biosynthesis of alginate and laminarin were similar among all developmental stages, however, that of genes involved in the biosynthesis of mannitol increased about 2-folds from mushroom and adult stages to mature and aging stages. This trend explained our observation that the content of alginate was almost constant at different development stages, while that of mannitol increased sharply. In addition, we found that a set of defense and cell recurring genes highly expressed and many of them expressed differentially among stages. On average, the sum abundance of the transcripts of these genes at four stages were 3.40-and 4.96-folds of all the annotated and all the expressed, respectively. This indicated that S. japonica sporophytes persistently respond possible pathogen and environment stresses. The findings are important for timing S. japonica harvest and amending the current cultivation mode.
Key words:    Saccharina japonica|transcriptome|developmental stage|sugar biosynthesis|defense   
Received: 2018-02-01   Revised: 2018-05-03
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Altschul S F, Madden T L, Schaffer A A, Zhang J H, Zhang Z, Miller W, Lipman D J. 1997. Gapped BLAST and PSIBLAST:A new generation of protein database search programs. Nucleic Acids Research, 25(17):3 389-3 402.
Anders S, Huber W. 2010.Differential expression analysis for sequence count data. Genome Biology, 11(10):R106.
Andreou A, Brodhun F, Feussner I. 2009. Biosynthesis of oxylipins in non-mammals. Progress in Lipid Research, 48(3-4):148-170.
Baldauf S L. 2008. An overview of the phylogeny and diversity of eukaryotes. Journal of Systematics and Evolution, 46(3):263-273.
Burton J N, Adey A, Patwardhan R P, Qiu R L, Kitzman J O, Shendure J. 2013. Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions.Nature Biotechnology, 31(12):1 119-1 125.
Cock J M, Sterck L, Rouzé P, Scornet D, Allen A E, Amoutzias G, Anthouard V, Artiguenave F, Aury J M, Badger J H, Beszteri B, Billiau K, Bonnet E, Bothwell J H, Bowler C, Boyen C, Brownlee C, Carrano C J, Charrier B, Cho G Y, Coelho S M, Collén J, Corre E, Da Silva C, Delage L, Delaroque N, Dittami S M, Doulbeau S, Elias M, Farnham G, Gachon C M, Gschloessl B, Heesch S, Jabbari K, Jubin C, Kawai H, Kimura K, Kloareg B, Küpper F C, Lang D, Le Bail A, Leblanc C, Lerouge P, Lohr M, Lopez P J, Martens C, Maumus F, Michel G, Miranda-Saavedra D, Morales J, Moreau H, Motomura T, Nagasato C, Napoli C A, Nelson D R, Nyvall-Collén P, Peters A F, Pommier C, Potin P, Poulain J, Quesneville H, Read B, Rensing S A, Ritter A, Rousvoal S, Samanta M, Samson G, Schroeder D C, Ségurens B, Strittmatter M, Tonon T, Tregear J W, Valentin K, von Dassow P, Yamagishi T, Van de Peer Y, Wincker P. 2010.The Ectocarpus genome and the independent evolution of multicellularity in brown algae.Nature, 465(7298):617-621.
Cosse A, Potin P, Leblanc C. 2009. Patterns of gene expression induced by oligoguluronates reveal conserved and environment-specific molecular defense responses in the brown alga Laminaria digitata. New Phytologist, 182(1):239-250.
Delaroque N, Boland W. 2008. The genome of the brown alga Ectocarpus siliculosus contains a series of viral DNA pieces, suggesting an ancient association with large dsDNA viruses. BMC Evolutionary Biology, 8:110.
Eid J, Fehr A, Gray J, Luong K, Lyle J, Otto G, Peluso P, Rank D, Baybayan P, Bettman B, Bibillo A, Bjornson K, Chaudhuri B, Christians F, Cicero R, Clark S, Dalal R, de Winter A, Dixon J, Foquet M, Gaertner A, Hardenbol P, Heiner C, Hester K, Holden D, Kearns G, Kong X, Kuse R, Lacroix Y, Lin S, Lundquist P, Ma C, Marks P, Maxham M, Murphy D, Park I, Pham T, Phillips M, Roy J, Sebra R, Shen G, Sorenson J, Tomaney A, Travers K, Trulson M, Vieceli J, Wegener J, Wu D, Yang A, Zaccarin D, Zhao P, Zhong F, Korlach J, Turner S. 2009. Real-time DNA sequencing from single polymerase molecules. Science, 323(5910):133-138.
Enquist-Newman M, Faust A M E, Bravo D D, Santos C N S, Raisner R M, Hane A, Sarvabhowman P, Le C, Regitsky D D, Cooper S R, Peereboom L, Clark A, Martinez Y, Goldsmith J, Cho M Y, Donohoue P D, Luo L, Lamberson B, Tamrakar P, Kim E J, Villari J L, Gill A, Tripathi S A, Karamchedu P, Paredes C J, Rajgarhia V, Kotlar H K, Bailey R B, Miller D J, Ohler N L, Swimmer C, Yoshikuni Y. 2014. Efficient ethanol production from brown macroalgae sugars by a synthetic yeast platform. Nature, 505(7482):239-243.
Grabherr M G, Haas B J, Yassour M, Levin J Z, Thompson D A, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q D, Chen Z H, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren B W, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A. 2011. Full-length transcriptome assembly from RNA-seq data without a reference genome.Nature Biotechnology, 29(7):644-652.
Ji M. 2004. Algal Chemistry. Science Press, Beijing. 812p. (in Chinese)
Keeling P J, Burger G, Durnford D G, Lang B F, Lee R W, Pearlman R E, Roger A J, Gray M W. 2005. The tree of eukaryotes. Trends in Ecology and Evolution, 20(12):670-676.
Kiseleva A A, Tarachovskaya E A, Shishova M F. 2012. Biosynthesis of phytohormones in algae. Russian Journal of Plant Physiology, 59(5):595-610.
Kraan S. 2013. Mass-cultivation of carbohydrate rich macroalgae, a possible solution for sustainable biofuel production, Mitigation and Adaptation Strategies for Global Change, 18(1):27-46.
Küpper F C, Schweigert N, Gall E A, Legendre J M, Vilter H, Kloareg B. 1998. Iodine uptake in Laminariales involves extracellular, haloperoxidase-mediated oxidation of iodide. Planta, 207(2):163-171.
Lane C E, Archibald J M. 2008. The eukaryotic tree of life:endosymbiosis takes its TOL. Trends in Ecology and Evolution, 23(5):268-275.
Le Bail A, Billoud B, Kowalczyk N, Kowalczyk M, Gicquel M, Le Panse S, Stewart S, Scornet D, Cock J M, Ljung K, Charrier B. 2010.Auxin metabolism and function in the multicellular brown alga Ectocarpus siliculosus. Plant Physiology, 153(1):128-144.
Li X J, Zhang Z Z, Qu S C, Liang G J, Sun J, Zhao N, Cui C J, Cao Z M, Li Y, Pan J H, Yu S H, Wang Q Y, Li X, Luo S J, Song S F, Guo L, Yang G P. 2016. Improving seedless kelp (Saccharina japonica) during its domestication by hybridizing gametophytes and seedling-raising from sporophytes. Scientific Reports, 6:21 255.
Lieberman-Aiden E, van Berkum N L, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie B R, Sabo P J, Dorschner M O, Sandstrom R, Bernstein B, Bender M A, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny L A, Lander E S, Dekker J. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science, 326(5950):289-293.
Mao X, Cai T, Olyarchuk J G, Wei L. 2005. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary.Bioinformatics, 21(19):3 787-3 793.
Miao Y Y, Zhu Z B, Guo Q S, Zhu Y H, Yang X H, Sun Y. 2016. Transcriptome analysis of differentially expressed genes provides insight into stolon formation in Tulipa edulis. Frontiers in Plant Science, 7:409.
Michel G, Tonon T, Scornet D, Cock J M, Kloareg B. 2010a.Central and storage carbon metabolism of the brown alga Ectocarpus siliculosus:Insights into the origin and evolution of storage carbohydrates in Eukaryotes. New Phytologist, 188(1):67-81.
Michel G, Tonon T, Scornet D, Cock J M, Kloareg B. 2010b.The cell wall polysaccharide metabolism of the brown alga Ectocarpus siliculosus:Insights into the evolution of extracellular matrix polysaccharides in Eukaryotes. New Phytologist, 188(1):82-97.
Nyvall P, Corre E, Boisset C, Barbeyron T, Rousvoal S, Scornet D, Kloareg B, Boyen C. 2003. Characterization of mannuronan C-5-epimerase genes from the brown alga Laminaria digitata. Plant Physiology, 133(2):726-735.
Ritter A, Dittami S M, Goulitquer S, Correa J A, Boyen C, Potin P, Tonon T. 2014. Transcriptomic and metabolomic analysis of copper stress acclimation in Ectocarpus siliculosus highlights signaling and tolerance mechanisms in brown algae. BMC Plant Biology, 14:116.
Shang D R, Ning J S, Zhao Y F, Zhai Y X, Shu B S, Sheng X F, Guo Y Y. 2011. Establishment of the determination on kelp alginate. Food Science and Technology, 36(8):252-254. (in Chinese with English abstract)
Takeda H, Yoneyama F, Kawai S, Hashimoto W, Murata K. 2011. Bioethanol production from marine biomass alginate by metabolically engineered bacteria. Energy & Environmental Science, 4(7):2 575-2 581.
Thomas F, Cosse A, Le Panse S, Kloareg B, Potin P, Leblanc C. 2014. Kelps feature systemic defense responses:Insights into the evolution of innate immunity in multicellular eukaryotes. New Phytologist, 204(3):567-576.
Tonon T, Eveillard D, Prigent S, Bourdon J, Potin P, Boyen C, Siegel A. 2011. Toward systems biology in brown algae to explore acclimation and adaptation to the shore environment. Omics, 15(12):883-892.
Tonon T, Li Y, McQueen-Mason M. 2017. Mannitol biosynthesis in algae:More widespread and diverse than previously thought. New Phytologist, 213(4):1 573-1 579.
Trapnell C, Williams B A, Pertea G, Mortazavi A, Kwan G, van Baren M J, Salzberg S L, Wold B J, Pachter L. 2010.Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology, 28(5):511-515.
Tsuda K, Somssich I E. 2015. Transcriptional networks in plant immunity. New Phytologist, 206(3):932-947.
Vanburen R, Bryant D, Edger P P, Tang H B, Burgess D, Challabathula D, Spittle K, Hall R, Gu J, Lyons E, Freeling M, Bartels D, Ten Hallers B, Hastie A, Michael T P, Mockler T C. 2015. Single-molecule sequencing of the desiccation-tolerant grass Oropetium thomaeum. Nature, 527(7579):508-511.
Wargacki A J, Leonard J F, Win M N, Regitsky D D, Santos C N S, Kim P B, Cooper S R, Raisner R M, Herman A, Sivitz A B, Lakshmanaswamy A, Kashiyama Y, Baker D, Yoshikuni Y. 2012. An Engineered microbial platform for direct biofuel production from brown macroalgae.Science, 335(6066):308-313.
Wu H Y, Wang X Y, Zhu A C. 2015. Analysis of component changes of Saccharina japonica at mushroom-adult stage.Marine Sciences, 39(8):35-38. (in Chinese with English abstract)
Yang G P, Li F F. 2014. Fermenting brown algal carbohydrates into ethanol with engineered microorganisms:a new horizon for bioethanol production. Marine Sciences, 38(4):88-95. (in Chinese with English abstract)
Ye J, Fang L, Zheng H K, Zhang Y, Chen J, Zhang Z J, Wang J, Li S T, Li R Q, Bolund L, Wang J. 2006. WEGO:a web tool for plotting GO annotations. Nucleic Acids Research, 34(S2):W293-W297.
Ye N H, Zhang X W, Miao M, Fan X, Zheng Y, Xu D, Wang J F, Zhou L, Wang D S, Gao Y, Wang Y T, Shi W Y, Ji P F, Li D M, Guan Z, Shao C W, Zhuang Z M, Gao Z Q, Qi J, Zhao F Q. 2015. Saccharina genomes provide novel insight into kelp biology. Nature Communications, 6:6986.
Young M D, Wakefield M J, Smyth G K, Oshlack A. 2010.Gene ontology analysis for RNA-seq:Accounting for selection bias. Genome Biology, 11(2):R14.
Zhang Y H, Li W J, Dou Y J, Zhang J X, Jiang G H, Miao L X, Han G F, Liu Y X, Li H, Zhang Z H. 2015. Transcript quantification by RNA-seq reveals differentially expressed genes in the red and yellow fruits of Fragaria vesca. PLoS One, 10(12):e0144356.