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De novo transcriptomics analysis revealed a global reprogramming towards dehydration and hyposalinity in Bangia fuscopurpurea gametophytes (Rhodophyta)

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Abstract

Bangia fuscopurpurea is a farmed species in the ancient family Bangiales. It inhabits upper intertidal zones and suffers periodical desiccation and osmotic stress. The transcriptomic regulation under dehydration and hyposalinity was investigated. The differentially expressed genes (DEGs) accounted for 18.7% of the unigenes obtained by de novo transcriptome assembly (|log2fold-change| ≥ 1, FDR ≤ 0.001). Over 72% of the DEGs were downregulated under stress. The DEGs were predominantly enriched into the KEGG pathways “metabolic pathways,” “ribosome,” “biosynthesis of secondary metabolites,” “protein processing in endoplasmic reticulum,” and “oxidative phosphorylation.” The optimum photosynthetic efficiency (Fv/Fm) and photochemical quenching (qP) dropped significantly with 89% relative water loss and recovered rapidly after being rehydrated. Most DEGs regarding “photosynthesis” and “C3 carbon fixation” were upregulated in the dehydrated thalli, which may enable the thalli to gain photosynthetic recovery once being rehydrated. Fv/Fm and qP decreased significantly with 1 h of 90% freshwater treatment and then recovered to the control level 1 day later. With 6 h hyposaline treatment, expression of plasma membrane H+-ATPase genes was strongly and predominantly induced while the mRNA abundance of vacuolar, chloroplastic, and mitochondrial H+-ATPase genes decreased or showed no significant change. Some transporter, ion channel, and transmembrane protein genes together with the gene-encoding key enzymes involving in proline and heteroside metabolism were upregulated under hyposalinity. The results indicated that transmembrane exchange of ion and osmolytes was induced under hyposalinity to balance the osmotic fluctuation, which seemed to be triggered by plasma membrane H+-ATPases. These findings will facilitate elucidating the stress acclimation mechanism of B. fuscopurpurea.

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References

  • Blouin NA, Brodie JA, Grossman AC, Xu P, Brawley SH (2011) Porphyra: a marine crop shaped by stress. Trends Plant Sci 16:29–37

    Article  CAS  Google Scholar 

  • Brawley SH, Blouin NA, Fickoblean E, Wheeler GL, Lohr M, Goodson HV, et al. (2017) Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta). Proc Natl Acad Sci 114(31):E6361–E6370

  • Broom JES, Farr TJ, Nelson WA (2004) Phylogeny of the Bangia flora of New Zealand suggests a southern origin for Porphyra and Bangia (Bangiales, Rhodophyta). Mol Phylogenet Evol 31:1197–1207

    Article  CAS  Google Scholar 

  • Butterfield NI (2000) Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26:86–404

    Article  Google Scholar 

  • Butterfield NJ (2009) Modes of pre-Ediacaran multicellularity. Precamb Res 173:201–211

    Article  CAS  Google Scholar 

  • Chan CX, Blouin NA, Zhuang Y, Zäuner S, Prochnik SE, Lindquist E, Lin S, Benning C, Lohr M, Yarish C, Gantt E, Grossman AR, Lu S, Müller K, W. Stiller J, Brawley SH, Bhattacharya D (2012) Porphyra (Bangiophyceae) transcriptomes provide insights into red algal development and metabolism. J Phycol 48:1328–1342

    Article  CAS  Google Scholar 

  • Chen CS, Wang L, Ji DH, Xie CT, Xu Y (2007) Influence of desiccation and cold preservation on the survival and growth of Porphyra haitanensis and unwanted alga. Acta Oceanol Sinica 29(2):131–136

    Google Scholar 

  • Choi S, Hwang MS, Im S, Kim N, Jeong WJ, Park EJ, Gong YG, Choi DW (2013) Transcriptome sequence and comparative analysis of the gametophyte thalli of Pyropia tenera under normal and high temperature conditions. J Appl Phycol 25:1237–1246

    Article  CAS  Google Scholar 

  • Collén J, Guisle-Marsollier I, Léger JJ, 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  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Contreras-Porcia L, López-Cristoffanini C, Lovazzano C, Flores-Molina MR, Thomas D, Núñez A, Fierro C, Guajardo E, Correa JA, Kube M, Reinhardt R (2013) Differential gene expression in Pyropia columbina (Bangiales, Rhodophyta) under natural hydration and desiccation conditions. Lat Am J Aquat Res 41:933–958

    Article  Google Scholar 

  • Davison IR, Pearson GA (1996) Stress tolerance in intertidal seaweeds. J Phycol 32:197–211

    Article  Google Scholar 

  • Dinakar C, Djilianov D, Bartels D (2012) Photosynthesis in desiccation tolerant plants: energy metabolism and antioxidative stress defense. Plant Sci 182:29–41

    Article  CAS  Google Scholar 

  • Dittami SM, Gravot A, Goulitquer S, Rousvoal S, Peters AF, Bouchereau A, Boyen C, Tonon T (2012) Towards deciphering dynamic changes and evolutionary mechanisms involved in the adaptation to low salinities in Ectocarpus (brown algae). Plant J 71:366–377

    CAS  PubMed  Google Scholar 

  • Dittami SM, Scornet D, Petit JL, Ségurens B, da Silva C, Corre E, Dondrup M, Glatting KH, König R, Sterck L, Rouzé P, van de Peer Y, Cock JM, Boyen C, Tonon T (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:R66

    Article  Google Scholar 

  • Fuglsang AT, Guo Y, Cuin TA, Qiu QS, Song CP, Kristiansen KA, Bych K, Schulz A, Shabala S, Schumaker KS (2007) Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+-ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19:1617–1634

    Article  CAS  Google Scholar 

  • Gao K, Aruga Y (1987) Preliminary studies on the photosynthesis and respiration of Porphyra yezoensis under emersed conditions. J Tokyo Univ Fish 47:51–65

    Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotech 29:644–652

    Article  CAS  Google Scholar 

  • Hanstein S, Wang X, Qian X, Friedhoff P, Fatima A, Shan Y, Feng K, Schubert S (2011) Changes in cytosolic Mg2+ levels can regulate the activity of the plasma membrane H+-ATPase in maize. Biochem J 435:93–101

    Article  CAS  Google Scholar 

  • Heinrich S, Valentin K, Frichenhaus S, John U, Wiencke C (2012) Transcriptomic analysis of acclimation to temperature and light stress in Saccharina latissima (Phaeophyceae). PLoS One 7(8):e44342

    Article  CAS  Google Scholar 

  • Holzinger A, Kaplan F, Blaas K, Zechmann B, Komsic-Buchmann K, Becker B (2014) Transcriptomics of desiccation tolerance in the streptophyte green alga Klebsormidium reveal a land plant-like defense reaction. PLoS One 9(10):e110630

    Article  Google Scholar 

  • Im S, Choi S, Hwang MS, Park E, Jeong W, Choi D (2015) De novo assembly of transcriptome from the gametophyte of the marine red algae Pyropia seriata and identification of abiotic stress response genes. J Appl Phycol 27:1343–1353

    Article  CAS  Google Scholar 

  • Iseli C, Jongeneel CV, Bucher P (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc Int Conf Intell Syst Mol Biol 1:138–148

    Google Scholar 

  • Janicka-Russak M, Kabala K (2015) The role of plasma membrane H+-ATPase in salinity stress of plants. Progr Bot 76:77–92

    CAS  Google Scholar 

  • Jia Z, Niu J, Huan L, Wu X, Wang G, Hou Z (2013) Cyclophilin participates in responding to stress situations in Porphyra haitanensis (Bangiales, Rhodophyta). J Phycol 49:194–201

    Article  CAS  Google Scholar 

  • Kanehisa M, Goto S (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28:27–30

    Article  CAS  Google Scholar 

  • Kong F, Yang J, Li N, Zhao H, Mao Y (2017) Identification and characterization of PyAQPs from Pyropia yezoensis, which are involved in tolerance to abiotic stress. J Appl Phycol 29:1695–1706

    Article  CAS  Google Scholar 

  • Kreps JA, Wu YJ, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141

    Article  CAS  Google Scholar 

  • Li R, Yu C, Li Y, Lam T, Yiu S, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25:1966–1967

    Article  CAS  Google Scholar 

  • Li SJ, Ma JH, Ji HH, Li EY (2003) Evaluation of nutrient components of Bangia sp. Acta Oceanol Sinica 22:89–95

    Google Scholar 

  • Lin AP, Wang GC, Yang F, Pan GH (2009) Photosynthetic parameters of sexually different parts of Porphyra katadai var. hemiphylla (Bangiales, Rhodophyta) during dehydration and rehydration. Planta 229:803–810

    Article  CAS  Google Scholar 

  • Martz F, Sutinen ML, Kiviniemi S, Palta JP (2006) Changes in freezing tolerance, plasma membrane H+-ATPase activity and fatty acid composition in Pinus resinosa needles during cold acclimation and de-acclimation. Tree Physiol 26:783–790

    Article  CAS  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, SchaeVer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Meth 5:621–628

    Article  CAS  Google Scholar 

  • Nakamura Y, Sasaki N, Kobayashi M, Ojima N, Yasuike M, Shigenobu Y, Satomi M, Fukuma Y, Shiwaku K, Tsujimoto A, Kobayashi T, Nakayama I, Ito F, Nakajima K, Sano M, Wada T, Kuhara S, Inouye K, Gojobori T, Ikeo K (2013) The first symbiont-free genome sequence of marine red alga, Susabi-nori (Pyropia yezoensis). PLoS One 8:e57122

    Article  CAS  Google Scholar 

  • Narusaka Y, Narusaka M, Seki M, Umezawa T, Ishida J, Nakajima M, Enju A, Shinozaki K (2004) Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant Mol Biol 55:327–342

    Article  CAS  Google Scholar 

  • Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S (2003) TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19:651–652

    Article  CAS  Google Scholar 

  • Piette AS, Derua R, Waelkens E, Boutry M, Duby G (2011) A phosphorylation in the C-terminal auto-inhibitory domain of the plant plasma membrane H+-ATPase activates the enzyme with no requirement for regulatory 14-3-3 proteins. J Biol Chem 286:18474–18482

    Article  CAS  Google Scholar 

  • Sampath-Wiley P, Neefus CD, Jahnke LS (2008) Seasonal effects of sun exposure and emersion on intertidal seaweed physiology: fluctuations in antioxidant contents, photosynthetic pigments and photosynthetic efficiency in the red alga Porphyra umbilicalis Kützing (Rhodophyta, Bangiales). J Exp Mar Biol Ecol 361:83–91

    Article  CAS  Google Scholar 

  • Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292

    Article  CAS  Google Scholar 

  • Sheath RG, Cole KM (1980) Distribution and salinity adaptations of Bangia atropurpurea (Rhodophyta), a putative migrant into the Laurentian Great Lakes. J Phycol 16:412–420

    Article  CAS  Google Scholar 

  • Smith CM, Satoh K, Fork DC (1986) The effects of osmotic tissue dehydration and air drying on morphology and energy transfer in two species of Porphyra. Plant Physiol 80:843–847

    Article  CAS  Google Scholar 

  • Sun P, Mao Y, Li G, Cao M, Kong F, Wang L, Bi G (2015) Comparative transcriptome profiling of Pyropia yezoensis (Ueda) M.S.Hwang & H.G. Choi in response to temperature stresses. BMC Genomics 16:463

    Article  Google Scholar 

  • Sutherland JE, Lindstrom SC, Nelson WA, Brodie J, Lynch MDJ, Hwang MS, Choi HG, Miyata M, Kikuchi N, Oliveira MC, Farr T, Neefus C, Mols-Mortensen A, Milstein D, Müller KM (2011) A new look at an ancient order: generic revision of the Bangiales (Rhodophyta). J Phycol 47:1131–1151

    Article  Google Scholar 

  • Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signaling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270

    Article  CAS  Google Scholar 

  • Wang WJ, Sun XT, Liu FL, Liang ZR, Zhang JH, Wang FJ (2016) Effect of abiotic stress on the gameophyte of Pyropia katadae var. hemiphylla (Bangiales, Rhodophyta). J Appl Phycol 28:469–479

    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 237:1123–1133

    Article  CAS  Google Scholar 

  • Wang WJ, Zhu JY, Xu P, Xu JR, Lin XZ, Huang CK, Song W, Peng G, Wang GC (2008) Characterization of the life history of Bangia fuscopurpurea (Bangiaceae, Rhodophyta) in connection with its artificial cultivation in China. Aquaculture 278:101–109

    Article  CAS  Google Scholar 

  • Xie C, Li B, Ji D, Chen C (2013) Characterization of the global transcriptome for Pyropia haitanensis (Bangiales, Rhodophyta) and development of cSSR markers. BMC Genomics 14:107

    Article  CAS  Google Scholar 

  • Xu Y, Gao S, Yang Y, Huang M, Cheng L, Wei Q, Fei Z, Hong B (2013) Transcriptome sequencing and whole genome expression profiling of chrysanthemum under dehydration stress. BMC Genomics 14:662

    Article  CAS  Google Scholar 

  • Yang Y, Qin Y, Xie C, Zhao F, Zhao J, Liu D, Chen S, Fuglsang AT, Palmgren MG, Schumaker KS, Deng XW, Guo Y (2010) The Arabidopsis chaperone J3 regulates the plasma membrane H+-ATPase through interaction with the PKS5 kinase. Plant Cell 22:1313–1332

  • Yang H, Mao YX, Kong FN, Yang GP, Ma F, Wang L (2011) Profiling of the transcriptome of Porphyra yezoensis with Solexa sequencing technology. Chin Sci Bull 20:2119–2130

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D (2004) A molecular timeline for the origin of photosynthetic eukaryotes. Mol Biol Evol 21:809–818

    Article  CAS  Google Scholar 

  • Yu X, Li M, Gao G, Feng HZ, Geng XQ, Peng CC, Zhu SY, Wang XJ, Shen YY, Zhang DP (2006) Abscisic acid stimulates a calcium-dependent protein kinase in grape berry. Plant Physiol 140:558–579

    Article  CAS  Google Scholar 

  • Zhou W, He L, Yang F, Lin A, Zhang B, Niu J, Wang G (2014) Pyropia yezoensis can utilize CO2 in the air during moderate dehydration. Chin J Oceanol Limnol 32:358–364

    Article  Google Scholar 

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Acknowledgements

We are grateful to the anonymous reviewers for their constructive comments and suggestions on the manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (31672630), Primary Research & Development Plan of Shandong Province (2016GSF115038), Special Scientific Research Funds for Central Non-profit Institutes, Chinese Academy of Fishery Sciences (2015A02XK01), National Science and Technology Infrastructure Project (2012), and the Open Funds of Seaweed Genetics and Germplasm Key Laboratory, Changshu Institute of Technology (2014-2016).

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  1. Zonggen Shen contributed equally to this work.

Authors and Affiliations

  1. Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China

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

  2. Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China

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

  3. Changshu Institute of Technology, Changshu, Jiangshu, 215500, China

    Zonggen Shen & Jianyi Zhu

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  1. Wenjun Wang
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Wang, W., Shen, Z., Sun, X. et al. De novo transcriptomics analysis revealed a global reprogramming towards dehydration and hyposalinity in Bangia fuscopurpurea gametophytes (Rhodophyta). J Appl Phycol 31, 637–651 (2019). https://doi.org/10.1007/s10811-018-1501-7

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