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Dynamic profile of proteome revealed multiple levels of regulation under heat stress in Saccharina japonica

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Abstract

Saccharina japonica is a typical seaweed that has been domesticated and cultivated at a large scale for a long time worldwide. Compared to the wild populations, the Saccharina cultivars have significant greater high-temperature tolerance. However, the molecular mechanisms of high temperature tolerance are still unknown. This study characterized the protein expression profile under heat stress using the iTRAQ strategy integrated with transcriptome data to identify the candidate genes involved in the heat stress tolerance. A total of 104 and 107 proteins were identified as the differential expressed proteins (DEPs) in sporophyte and gametophyte, respectively. Only 14 DEPs identified both in sporophyte and gametophyte indicated that the two generations have different protein expression in response to the heat stress. The correlation between proteome and transcriptome profile under heat stress was very low, with only six genes were identified both on the transcription and protein levels. However, 23 pathways, including multiple cellular processes such as nitrogen and carbon metabolism, transcription, translation, posttranslational modification, antioxidant system etc., were identified. This study is the first exploration into the molecular mechanism of Saccharina heat tolerance on both transcriptomic and proteomic levels, which provides new insight into the regulation mechanism in response to heat stress in kelp.

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References

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

  • Coelho SM, Peters AF, Charrier B, Roze D, Destombe C, Valero M, Cock JM (2007) Complex life cycles of multicellular eukaryotes: new approaches based on the use of model organisms. Gene 406:152–170

    Article  CAS  PubMed  Google Scholar 

  • Colin C, Leblanc C, Michel G, Wagner E, Wagner EL, Dorsselaer AV, Potin P (2005) Vanadium-dependent iodoperoxidases in Laminaria digitata, a novel biochemical function diverging from brown algal bromoperoxidases. J Biol Inorg Chem 10:156–166

    Article  CAS  PubMed  Google Scholar 

  • Collén J, Guisle-Marsollier I, Leger J, Boyen C (2007) Response of the transcriptome of the intertidal red seaweed Chondrus crispus to controlled and natural stresses. New Phytol 176:45–55

    Article  CAS  PubMed  Google Scholar 

  • Conesa A, Götz S, García-Gómez JM, Talón JT, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21(18):3674–3676

  • 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 Phytol 182:239–250

    Article  CAS  PubMed  Google Scholar 

  • Cox J, Mann M (2007) Is proteomics the new genomics? Cell 130:395–398

    Article  CAS  PubMed  Google Scholar 

  • Deng YY, Yao JT, Wang XL, Guo H, Duan DL (2012) Transcriptome sequencing and comparative analysis of Saccharina japonica (Laminariales, Phaeophyceae) under blue light induction. PLoS One 7:e39704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dring ML (2005) Stress resistance and disease resistance in seaweeds, the role of reactive oxygen metabolism. Adv Bot Res 43:175–207

    Article  CAS  Google Scholar 

  • Fang ZX, Wu CY, Li JJ (1962) Increased adaptability to high temperature of gametophytes and sporelings of the Haiqing No. 1 breed of Laminaria japonica Aresch. Oceanol Limnol Sinica 4:29–37

    Google Scholar 

  • Fields P, Graham J, Rosenblat H, Somero G (1993) Effects of expected global climate change on marine faunas. Trends Ecol Evol 8:361–367

    Article  CAS  PubMed  Google Scholar 

  • Gerard VA (2008) The role of nitrogen nutrition in high-temperature tolerance of the kelp, Laminaria saccharina (Chromophyta). J Phycol 33:800–810

    Article  Google Scholar 

  • Gomez I, Wiencke C (1996) Photosynthesis, dark respiration and pigment contents of gametophytes and sporophytes of the Antarctic brown alga Desmarestia menziesii. Bot Mar 39:149–157

  • Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talón M, Dopaza J, Conesa A (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36:3420–3435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ideker T, Thorsson V, Ranish JA, Christmas R, Buhler J, Eng JK, Bumgarner R, Goodlett DR, Aebersold R, Hood L (2001) Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 292:929–934

    Article  CAS  PubMed  Google Scholar 

  • Kosová K, Vítámvás P, Prášil IT, Renaut J (2011) Plant proteome changes under abiotic stress—contribution of proteomics studies to understanding plant stress response. J Proteome 74:1301–1322

    Article  CAS  Google Scholar 

  • Leblanc C, Colin C, Cosse A, Delage L, Brre SL, Morin P, Potin P (2006) Iodine transfers in the coastal marine environment, the key role of brown algae and of their vanadium-dependent haloperoxidases. Biochimie 88:1773–1785

    Article  CAS  PubMed  Google Scholar 

  • Li DP, Zhou ZG, Liu HH, Wu CY (1999) A new method of Laminaria japonica strain selection and sporeling raising by the use of gametophyte clones. Hydrobiologia 398/399:473–476

    Article  Google Scholar 

  • Liu F, Pang SJ (2010) Performances of growth, photochemical efficiency, and stress tolerance of young sporophytes from seven populations of Saccharina japonica (Phaeophyta) under short-term heat stress. J Appl Phycol 22:221–229

    Article  CAS  Google Scholar 

  • Liu FL, Wang WJ, Sun XT, Liang ZR, Wang FJ (2014) RNA-seq revealed complex response to heat stress on transcriptomic level in Saccharina japonica (Laminariales, Phaeophyta). J Appl Phycol 26:1585–1596

    Article  CAS  Google Scholar 

  • Liu FL, Wang WJ, Sun XT, Liang ZR, Wang FJ (2015) Conserved and novel heat stress-responsive microRNAs were identified by deep sequencing in Saccharina japonica (Laminariales, Phaeophyta). Plant Cell Environ 38:1357–1367

    Article  CAS  PubMed  Google Scholar 

  • Mable BK, Otto SP (1998) The evolution of life cycles with haploid and diploid phases. BioEssays 20:453–462

    Article  Google Scholar 

  • Martínez EA (1999) Latitudinal differences in thermal tolerance among microscopic sporophytes of the kelp Lessonia nigrescens (Phaeophyta, Laminariales). Pac Sci 53:74–81

    Google Scholar 

  • Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KEEG, an automatic genome annotation and pathway reconstruction server. Nucleic Acid Res 35:W182–W185

    Article  PubMed  PubMed Central  Google Scholar 

  • Nagai K, Yotsukura N, Ikegami H, Kimura H, Morimoto K (2008) Protein extraction for two-dimensional electrophoresis from the lamina of Ecklonia kurome (Laminariales), a recalcitrant tissue containing high levels of viscous polysaccharides. Electrophoresis 29:672–681

    Article  CAS  PubMed  Google Scholar 

  • Pang SJ, Jin ZH, Sun JZ, Gao SQ (2007) Temperature tolerance of young sporophytes from two populations of Laminaria japonica revealed by chlorophyll fluorescence measurements and short-term growth and survival performances in tank culture. Aquaculture 262:493–503

    Article  Google Scholar 

  • Roeder V, Collén J, Rousvoal S, Corre E, Leblanc C, Boyen C (2005) Identification of stress gene transcripts in Laminaria digitata (Phaeophyceae) protoplast cultures by expressed sequence tag analysis. J Phycol 41:1227–1235

    Article  CAS  Google Scholar 

  • Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes JA, Tegner MJ (2002) Kelp forest ecosystems, biodiversity, stability, resilience and future. Environ Conserv 29:436–459

    Article  Google Scholar 

  • Suzuki S, Furuya K, Kawai T, Takeuchi I (2008) Effect of seawater temperature on the productivity of Laminaria japonica in the Uwa Sea, southern Japan. J Appl Phycol 20:833–844

    Article  Google Scholar 

  • Thomas DN, Kirst GO (1991) Differences in osmoacclimation between sporophytes and gametophytes of the brown alga Ectocarpus siliculosus. Physiol Plantarum 83:281–289

    Article  CAS  Google Scholar 

  • Tse WKF, Sun J, Zhang HM, Law AYS, Yeung BHY, Chow SC, Qiu JW, Won CKC (2013) Transcriptomic and iTRAQ proteomic approaches reveal novel short-term hyperosmotic stress responsive proteins in the gill of the Japanese eel (Anguilla japonica). J Proteome 89:81–94

    Article  CAS  Google Scholar 

  • Tseng CK, Chang CF (1960) An analysis of the nature of marine algal flora. Oceanol Limnol Sinica 3:177–187

    Google Scholar 

  • Van den Hoek C, Breeman AM, Stam WT (1990) The geographic distribution of seaweed species in relation to temperature, present and past. In: Beukema JJ, Wolff WJ, Brouns JJWM (eds) Expected effects of climatic change on marine coastal ecosystems. Springer, Dordrecht, pp 55–67

    Chapter  Google Scholar 

  • Wang Y, Tang XX (2005) Relationships between antioxidant activities and heat-resistant features of two Laminaria japonica strains. Chin J Appl Ecol 16:1507–1512

    CAS  Google Scholar 

  • Wang Y, Yu QY, Tang XX, Wang L (2009) Calcium pretreatment increases thermotolerance of Laminaria japonica sporophytes. Prog Nature Sci 19:435–442

    Article  CAS  Google Scholar 

  • Wang WJ, Wang FJ, Sun XT, Liu FL, Liang ZR (2013) Comparison of transcriptome under red and blue light culture of Saccharina japonica (Phaeophyceae). Planta 237:123–1133

    Google Scholar 

  • Wang YT, Xu D, Fan X, Zhang XW, Ye NH, Wang WQ, Mao YZ, Mou SL, Cao S N (2013) Variation of photosynthetic performance, nutrient uptake, and elemental composition of different generations and different thallus parts of Saccharina japonica. J Appl Phycol 25:631–637

  • Wiese S, Reidegeld KA, Meyer HE, Warscheid B (2007) Protein labeling by iTRAQ: a new tool for quantitative mass spectrometry in proteome research. Proteomics 7:340–350

    Article  PubMed  Google Scholar 

  • Xiong Q, Feng J, Li ST, Zhang GY, Qiao ZX, Chen Z, Wu Y, Lin Y, Li T, Ge F, Zhao JD (2015) Integrated transcriptomic and proteomic analysis of the global response of Synechococcus to high light stress. Mol Cell Proteomics 14:1038–1053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Qiang X, Owsiany K, Zhang S, Thannhauser TW, Li L (2011) Evaluation of different multidimensional LC-MS/MS pipelines for isobaric tags for relative and absolute quantitation (iTRAQ)-based proteomic analysis of potato tubers in response to cold storage. J Proteome Res 10:4647–4660

    Article  CAS  PubMed  Google Scholar 

  • Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang ZJ, Wang J, Li ST, Li RQ, Bolund L, Wang J (2006) WEGO, a web tool for plotting GO annotations. Nucleic Acid Res 34:W293–W297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yotsukura N, Nagai K, Kimura H, Morimoto K (2010) Seasonal changes in proteomic profiles of Japanese kelp, Saccharina japonica (Laminariales, Phaeophyceae). J Appl Phycol 22:443–451

    Article  CAS  Google Scholar 

  • Yotsukura N, Nagai K, Tanaka T, Kimura H, Morimoto K (2012) Temperature stress-induced changes in the proteomic profiles of Ecklonia cava (Laminariales, Phaeophyceae). J Appl Phycol 24:163–171

    Article  CAS  Google Scholar 

  • Zhang LN, Cui CJ, Li XJ, Zhang ZZ, Luo SJ, Liang GJ, Liu YL, Yang GP (2013) Effect of temperature on the development of Saccharina japonica gametophytes. J Appl Phycol 25:261–267

    Article  Google Scholar 

  • Zheng Q, Wang XJ (2008) GOEAST, a web-based software toolkit for gene ontology enrichment analysis. Nucleic Acid Res 36:W358–W363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Key R&D Program of China (2018YFD0900305; 2018YFD0901500), China Agriculture Research System(CARS-50), Qingdao Science and Technology Project (17-3-3-65-nsh), Central Public-interest Scientific Institution Basal Research Fund, CAFS (2019GH13) and Projects of International Exchange and Cooperation in Agriculture, Ministry of Agriculture and Rural Affairs of China, Technology and Innovation Cooperation in Aquaculture with Tropical Countries along the Belt and Road. The authors are grateful to the anonymous reviewers for their constructive comments on this paper.

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Authors and Affiliations

  1. Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, China

    Fuli Liu, Pengyan Zhang, Zhourui Liang, Wenjun Wang, Xiutao Sun & Feijiu Wang

  2. Laboratory for Marine Fisheries and Aquaculture, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China

    Fuli Liu, Pengyan Zhang, Zhourui Liang, Wenjun Wang & Xiutao Sun

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  1. Fuli Liu
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  2. Pengyan Zhang
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  3. Zhourui Liang
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  5. Xiutao Sun
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  6. Feijiu Wang
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Correspondence to Fuli Liu.

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Table S1

The information for all the proteins identified by iTRAQ–LCMS/MS proteomic analysis. (XLSX 687 kb)

Table S2

The information for the differentially expressed proteins in response to the heat stress in the sporophyte and gametophyte identified by iTRAQ–LCMS/MS proteomic analysis. (XLSX 131 kb)

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Liu, F., Zhang, P., Liang, Z. et al. Dynamic profile of proteome revealed multiple levels of regulation under heat stress in Saccharina japonica. J Appl Phycol 31, 3077–3089 (2019). https://doi.org/10.1007/s10811-019-01813-w

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  • DOI: https://doi.org/10.1007/s10811-019-01813-w

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