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Transcriptome Profiling in the Marine Red Alga Neopyropia yezoensis Under Light/Dark Cycle

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Abstract

Many organisms are subjected to a daily cycle of light and darkness, which significantly influences metabolic and physiological processes. In the present study, Neopyropia yezoensis, one of the major cultivated seaweeds used in “nori,” was harvested in the morning and evening during light/dark treatments to investigate daily changes in gene expression using RNA-sequencing. A high abundance of transcripts in the morning includes the genes associated with carbon–nitrogen assimilations, polyunsaturated fatty acid, and starch synthesis. In contrast, the upregulation of a subset of the genes associated with the pentose phosphate pathway, cell cycle, and DNA replication at evening is necessary for the tight control of light-sensitive processes, such as DNA replication. Additionally, a high abundance of transcripts at dusk encoding asparaginase and glutamate dehydrogenase imply that regulation of asparagine catabolism and tricarboxylic acid cycle possibly contributes to supply nitrogen and carbon, respectively, for growth during the dark. In addition, genes encoding cryptochrome/photolyase family and histone modification proteins were identified as potential key players for regulating diurnal rhythmic genes.

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Data Availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  • Alia SPP, Mohanty P (1997) Involvement of proline in protecting thylakoid membranes against free radical-induced photodamage. J Photochem Photobiol B Biol 38:253–257

    Article  CAS  Google Scholar 

  • Amsler CD, Neushul M (1989) Diel periodicity of spore release from the kelp Nereocystis luetkeana (Mertens) Postels et Ruprecht. J Exp Mar Biol Ecol 134:117–127

    Article  Google Scholar 

  • Antosch M, Schubert V, Holzinger P, Houben A, Grasser KD (2015) Mitotic lifecycle of chromosomal 3xHMG-box proteins and the role of their N-terminal domain in the association with rDNA loci and proteolysis. New Phytol 208:1067–1077

    Article  CAS  PubMed  Google Scholar 

  • Barinaga M (1998) Circadian rhythms - clock photoreceptor shared by plants and animals. Science 282:1628–1630

    Article  CAS  PubMed  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boros LG, Lee PW, Brandes JL, Cascante M, Muscarella P, Schirmer WJ, Melvin WS, Ellison EC (1998) Nonoxidative pentose phosphate pathways and their direct role in ribose synthesis in tumors: is cancer a disease of cellular glucose metabolism? Med Hypotheses 50:55–59

    Article  CAS  PubMed  Google Scholar 

  • Boros LG, Puigjaner J, Cascante M, Lee W-NP, Brandes JL, Bassilian S, Yusuf FI, Williams RD, Muscarella P, Melvin WS, Schirmer WJ (1997) Oxythiamine and dehydroepiandrosterone inhibit the nonoxidative synthesis of ribose and tumor cell proliferation. Cancer Res 57:4242–4248

    CAS  PubMed  Google Scholar 

  • Breeman AM (1993) Photoperiodic history affects the critical daylength of the short day-plant Acrosymphyton purpuriferum (Rhodophyta). Eur J Phycol 28:157–160

    Article  Google Scholar 

  • Cánovas FM, Avila C, Cantón FR, Cañas RA, De La Torre F (2007) Ammonium assimilation and amino acid metabolism in conifers. J Exp Bot 58:2307–2318

    Article  CAS  PubMed  Google Scholar 

  • Cao M, Wang D, Mao Y, Kong F, Bi G, Xing Q, Weng Z (2017) Integrating transcriptomics and metabolomics to characterize the regulation of EPA biosynthesis in response to cold stress in seaweed Bangia fuscopurpurea. PLoS One 12:e0186986

  • Cashmore AR (2003) Cryptochromes: enabling plants and animals to determine circadian time. Cell 114:537–543

    Article  CAS  PubMed  Google Scholar 

  • Chaves I, Pokorny R, Byrdin M, Hoang N, Ritz T, Brettel K, Essen LO, van der Horst GTJ, Batschauer A, Ahmad M (2011) The cryptochromes: blue light photoreceptors in plants and animals. Annu Rev Plant Biol 62:335–364

    Article  CAS  PubMed  Google Scholar 

  • Chi W, He B, Mao J, Jiang J, Zhang L (2015) Plastid sigma factors: their individual functions and regulation in transcription. Biochim Biophys Acta-Bioenergetics 1847:770–778

    Article  CAS  Google Scholar 

  • Choi HG, Kim YS, Lee SJ, Park EJ, Nam KW (2005) Effects of daylength, irradiance and settlement density on the growth and reproduction of Undaria pinnatifida gametophytes. J Appl Phycol 17:423–430

    Article  Google Scholar 

  • Coate JE, Doyle JJ (2011) Divergent evolutionary fates of major photosynthetic gene networks following gene and whole genome duplications. Plant Signal Behav 6:594–597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coesel S, Mangogna M, Ishikawa T, Heijde M, Rogato A, Finazzi G, Todo T, Bowler C, Falciatore A (2009) Diatom PtCPF1 is a new cryptochrome/photolyase family member with DNA repair and transcription regulation activity. EMBO Rep 10:655–661

    Article  CAS  PubMed  PubMed Central  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  PubMed  Google Scholar 

  • Coruzzi G, Bush DR (2001) Nitrogen and carbon nutrient and metabolite signaling in plants. Plant Physiol 125:61–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4:215–223

    Article  CAS  Google Scholar 

  • Dodd AN, Salathia N, Hall A, Kévei E, Tóth R, Nagy F, Hibberd JM, Millar AJ, Webb AAR (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633

    Article  CAS  PubMed  Google Scholar 

  • Dring MJ (1967) Effects of daylength on growth and reproduction of conchocelis-phase of Porphyra tenera. J Mar Biol Ass UK 47:501–510

    Article  Google Scholar 

  • Dunlap JC (1999) Molecular bases for circadian clocks. Cell 96:271–290

    Article  CAS  PubMed  Google Scholar 

  • El-Assal SED, Alonso-Blanco C, Peeters AJM, Wagemaker C, Weller JL, Koornneef M (2003) The role of cryptochrome 2 in flowering in Arabidopsis. Plant Physiol 133:1504–1516

    Article  CAS  Google Scholar 

  • Fernandez E, Galvan A (2008) Nitrate assimilation in Chlamydomonas. Eukaryot Cell 7:555–559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fortunato AE, Annunziata R, Jaubert M, Bouly JP, Falciatore A (2015) Dealing with light: the widespread and multitasking cryptochrome/photolyase family in photosynthetic organisms. J Plant Physiol 172:42–54

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Parry M, Noctor G (2003) Markers and signals associated with nitrogen assimilation in higher plants. J Exp Bot 54:585–593

    Article  CAS  PubMed  Google Scholar 

  • Fu A, He ZY, Cho HS, Lima A, Buchanan BB, Luan S (2007) A chloroplast cyclophilin functions in the assembly and maintenance of photosystem II in Arabidopsis thaliana. Proc Natl Acad Sci USA 104:15947–15952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujimoto R, Uezono K, Ishikura S, Osabe K, Peacock WJ, Dennis ES (2018) Recent research on the mechanism of heterosis is important for crop and vegetable breeding systems. Breed Sci 68:145–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geigenberger P (2011) Regulation of starch biosynthesis in response to a fluctuating environment. Plant Physiol 155:1566–1577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goecks J, Nekrutenko A, Taylor J, Galaxy Team (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11:R86

    Article  Google Scholar 

  • Goulard F, Lüning K, Jacobsen S (2004) Circadian rhythm of photosynthesis and concurrent oscillations of transcript abundance of photosynthetic genes in the marine red alga Grateloupia turuturu . Eur J Phycol 39:431–437

  • Granbom M, Pedersen M, Kadel P, Lüning K (2001) Circadian rhythm of photosynthetic oxygen evolution in Kappaphycus alvarezii (Rhodophyta): dependence on light quantity and quality. J Phycol 37:1020–1025

    Article  Google Scholar 

  • Grant M, Bevan MW (1994) Asparaginase gene expression is regulated in a complex spatial and temporal pattern in nitrogen sink-tissues. Plant J 5:695–704

    Article  CAS  Google Scholar 

  • Guo H, Yang H, Mockler TC, Lin C (1998) Regulations of flowering time by Arabidopsis photoreceptors. Science 279:1360–1363

    Article  CAS  PubMed  Google Scholar 

  • Harashima H, Dissmeyer N, Schnittger A (2013) Cell cycle control across the eukaryotic kingdom. Trends Cell Biol 23:345–356

    Article  CAS  PubMed  Google Scholar 

  • Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290:2110–2113

    Article  CAS  PubMed  Google Scholar 

  • Heijde M, Zabulon G, Corellou F, Ishikawa T, Brazard J, Usman A, Sanchez F, Plaza P, Martin M, Falciatore A, Todo T, Bouget FY, Bowler C (2010) Characterization of two members of the cryptochrome/photolyase family from Ostreococcus tauri provides insights into the origin and evolution of cryptochromes. Plant Cell Environ 33:1614–1626

    Article  CAS  PubMed  Google Scholar 

  • Hennig L, Bouveret R, Gruissem W (2005) MSI1-like proteins: an escort service for chromatin assembly and remodeling complexes. Trends Cell Biol 15:295–302

    Article  CAS  PubMed  Google Scholar 

  • Hu CAA, Delauney AJ, Verma DPS (1992) A bifunctional enzyme (delta 1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proc Natl Acad Sci USA 89:9354–9358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Imaizumi T (2010) Arabidopsis circadian clock and photoperiodism: time to think about location. Curr Opin Plant Biol 13:83–89

    Article  CAS  PubMed  Google Scholar 

  • Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080

    Article  CAS  PubMed  Google Scholar 

  • Johansson M, Staiger D (2015) Time to flower: interplay between photoperiod and the circadian clock. J Exp Bot 66:719–730

    Article  CAS  PubMed  Google Scholar 

  • Kageyama A, Yokohama Y, Nisizawa K (1979) Diurnal rhythm of apparent photosynthesis of a brown alga, Spatoglossum pacificum. Bot Mar 22: 199–201

  • Kanamaru K, Tanaka K (2004) Roles of chloroplast RNA polymerase sigma factors in chloroplast development and stress response in higher plants. Biosci Biotechnol Biochem 68:2215–2223

    Article  CAS  PubMed  Google Scholar 

  • Kang J, Turano FJ (2003) The putative glutamate receptor 1.1 (AtGLR1.1) functions as a regulator of carbon and nitrogen metabolism in Arabidopsis thaliana. Proc Natl Acad Sci USA 100:6872–6877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kapanidou M, Curtis NL, Bolanos-Garcia VM (2017) Cdc20: At the crossroads between chromosome segregation and mitotic exit. Trends Biochem Sci 42:193–205

    Article  CAS  PubMed  Google Scholar 

  • Kim SH, Turnbull J, Guimond S (2011) Extracellular matrix and cell signalling: the dynamic cooperation of integrin, proteoglycan and growth factor receptor. J Endocrinol 209:139–151

    Article  CAS  PubMed  Google Scholar 

  • Kiontke S, Göbel T, Brych A, Batschauer A (2020) DASH-type cryptochromes-solved and open questions. Biol Chem 401:1487–1493

    Article  CAS  PubMed  Google Scholar 

  • Kishor P, Hong Z, Miao GH, Hu C, Verma D (1995) Overexpression of [delta]-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi K, Endo K, Wada H (2017) Specific distribution of phosphatidylglycerol to photosystem complexes in the thylakoid membrane. Front Plant Sci 8:1991

    Article  PubMed  PubMed Central  Google Scholar 

  • Kowalik MA, Columbano A, Perra A (2017) Emerging role of the pentose phosphate pathway in hepatocellular carcinoma. Front Oncol 7:87

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuwano K, Sakurai R, Motozu Y, Kitade Y, Saga N (2008) Diurnal cell division regulated by gating the G1/S transition in Enteromorpha compressa (Chlorophyta). J Phycol 44:364–373

    Article  PubMed  Google Scholar 

  • Lancien M, Gadal P, Hodges M (2000) Enzyme redundancy and the importance of 2-oxoglutarate in higher plant ammonium assimilation. Plant Physiol 123:817–824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lea PJ, Sodek L, Parry MAJ, Shewry PR, Halford NG (2007) Asparagine in plants. Ann Appl Biol 150:1–26

    Article  CAS  Google Scholar 

  • Li QB, Haskell D, Zhang C, Sung DY, Guy C (2000) Diurnal regulation of Hsp70s in leaf tissue. Plant J 21:373–378

    Article  PubMed  Google Scholar 

  • Liao Y, Smyth GK, Shi W (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930

    Article  CAS  PubMed  Google Scholar 

  • Lin C, Todo T (2005) The Cryptochromes Genome Biol 6:220

    Article  CAS  PubMed  Google Scholar 

  • Lüning K (1994) Circadian growth rhythm in juvenile sporophytes of Laminariales (Phaeophyta). J Phycol 30:193–199

    Article  Google Scholar 

  • Lüning K, Titlyanov EA, Titlyanova TV (1997) Diurnal and circadian periodicity of mitosis and growth in marine macroalgae.III. The red alga Porphyra umbilicalis. Eur J Phycol 32:167–173

    Article  Google Scholar 

  • Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Makarov VN, Schoschina EV, Luning K (1995) Diurnal and circadian periodicity of mitosis and growth in marine macroalgae.I. Juvenile sporophytes of Laminariales (Phaeophyta). Eur J Phycol 30:261–266

    Article  Google Scholar 

  • Matysik J, Alia Bhalu B, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532

    CAS  Google Scholar 

  • McClung CR (2021) Circadian clock components offer targets for crop domestication and improvement. Genes 12:374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meeuse BJD, Andries M, Wood JA (1960) Floridean Starch. J Exp Bot 11:129

    Article  CAS  Google Scholar 

  • Mei QM, Dvornyk V (2015) Evolutionary history of the photolyase/cryptochrome superfamily in eukaryotes. PLoS ONE 10:9

    Google Scholar 

  • Miyashita Y, Good AG (2008) NAD(H)-dependent glutamate dehydrogenase is essential for the survival of Arabidopsis thaliana during dark-induced carbon starvation. J Exp Bot 59:667–680

    Article  CAS  PubMed  Google Scholar 

  • Mouritsen OG, Duelund L, Petersen MA, Hartmann AL, Frøst MB (2019) Umami taste, free amino acid composition, and volatile compounds of brown seaweeds. J Appl Phycol 31:1213–1232

    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

  • Ngan Y, Price IR (1983) Periodicity of spore discharge in tropical Florideophyceae (Rhodophyta). Br Phycol J 18:83–95

    Article  Google Scholar 

  • Nunes-Nesi A, Fernie AR, Stitt M (2010) Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol Plant 3:973–996

    Article  CAS  PubMed  Google Scholar 

  • Ohi R, Gould KL (1999) Regulating the onset of mitosis. Curr Opin Cell Biol 11:267–273

    Article  CAS  PubMed  Google Scholar 

  • Okada M, Inoue M, Ikeda T (1978) Circadian rhythm in photosynthesis of the green alga Bryopsis maxima. Plant Cell Physiol 19:197–202

    CAS  Google Scholar 

  • Oliveri P, Fortunato AE, Petrone L, Ishikawa-Fujiwara T, Kobayashi Y, Todo T, Antonova O, Arboleda E, Zantke J, Tessmar-Raible K, Falciatore A (2014) The cryptochrome/photolyase Family in aquatic organisms. Mar Genomics 14:23–37

    Article  PubMed  Google Scholar 

  • Oohusa T (1980) Diurnal rhythm in the rates of cell division, growth and photosynthesis of Porphyra yezoensis (Rhodophyceae) Cultured in the laboratory. Bot Mar 23:1–5

  • Oohusa T, Araki S, Sakurai T, Saitoh M (1977a) Physiological studies on diurnal biological rhythms of Porphyra. I. Cell-size, physiological-activity and content of photosynthetic pigments in thallus cultured in laboratory. Bull Jpn Soc Sci Fish 43:245–249

    Article  CAS  Google Scholar 

  • Oohusa T, Araki S, Sakurai T, Saitoh M (1977b) Physiological studies on diurnal biological rhythms of Porphyra. II. Growth and contents of free and total nitrogen and carbohydrate in thallus cultured in laboratory. Bull Jpn Soc Sci Fish 43:251–254

    Article  CAS  Google Scholar 

  • Pang SJ, Lüning K (2004) Photoperiodic long-day control of sporophyll and hair formation in the brown alga Undaria pinnatifida. J Appl Phycol 16:83–92

    Article  Google Scholar 

  • Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL (2016) Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc 11:1650–1667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfluger J, Wagner D (2007) Histone modifications and dynamic regulation of genome accessibility in plants. Curr Opin Plant Biol 10:645–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polat IH, Tarrado-Castellarnau M, Bharat R, Perarnau J, Benito A, Cortés R, Sabatier P, Cascante M (2021) Oxidative pentose phosphate pathway enzyme 6-phosphogluconate dehydrogenase plays a key role in breast cancer metabolism. Biology 10:85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Watanabe A, Hattori A (eds) Culture and collections of algae, Proc U S-Japan Conf, Hakone, September 1966. Jpn Soc Plant Physiol Tokyo 63–75

  • Qu J, Xu S, Zhang Z, Chen G, Zhong Y, Liu L, Zhang R, Xue J, Guo D (2018) Evolutionary, structural and expression analysis of core genes involved in starch synthesis. Sci Rep 8:12736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rea S, Eisenhaber F, O’Carroll D, Strahl BD, Sun ZW, Schmid M, Opravil S, Mechtler K, Ponting CP, Allis CD, Jenuwein T (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406:593–599

    Article  CAS  PubMed  Google Scholar 

  • Sancar A (2008) Structure and function of photolyase and in vivo enzymology: 50th anniversary. J Biol Chem 283:32153–32157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanz-Luque E, Chamizo-Ampudia A, Llamas A, Galvan A, Fernandez E (2015) Understanding nitrate assimilation and its regulation in microalgae. Front Plant Sci 6:899

    Article  PubMed  PubMed Central  Google Scholar 

  • Schaffer R, Landgraf J, Accerbi M, Simon V, Larson M, Wisman E (2001) Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell 13:113–123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmid R, Dring MJ (1992) Circadian rhythm and fast responses to blue light of photosynthesis in Ectocarpus (Phaeophyta, Ectocarpales).I. Characterization of the rhythm and the blue light response. Planta 187:53–59

    Article  CAS  PubMed  Google Scholar 

  • Schroda M, Vallon O, Wollman FA, Beck CF (1999) A chloroplast-targeted heat shock protein 70 (HSP70) contributes to the photoprotection and repair of photosystem II during and after photoinhibition. Plant Cell 11:1165–1178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schubert H, Gerbersdorf S, Titlyanov E, Titlyanova T, Granbom M, Pape C, Lüning K (2004) Circadian rhythm of photosynthesis in Kappaphycus alvarezii (Rhodophyta): independence of the cell cycle and possible photosynthetic clock targets. Eur J Phycol 39:423–430

    Article  CAS  Google Scholar 

  • Sieciechowicz KA, Joy KW, Ireland RJ (1988) The metabolism of asparagine in plants. Phytochemistry 27:663–671

    Article  CAS  Google Scholar 

  • Sirpio S, Khrouchtchova A, Allahverdiyeva Y, Hansson M, Fristedt R, Vener AV, Scheller HV, Jensen PE, Haldrup A, Aro EM (2008) AtCYP38 ensures early biogenesis, correct assembly and sustenance of photosystem II. Plant J 55:639–651

    Article  CAS  PubMed  Google Scholar 

  • Steed G, Ramirez DC, Hannah MA, Webb AAR (2021) Chronoculture, harnessing the circadian clock to improve crop yield and sustainability. Science 372:eabc9141

  • Sun N, Ma LG, Pan DY, Zhao HY, Deng XW (2003) Evaluation of light regulatory potential of Calvin cycle steps based on large-scale gene expression profiling data. Plant Mol Biol 53:467–478

    Article  CAS  PubMed  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

  • Szal B, Podgórska A (2012) The role of mitochondria in leaf nitrogen metabolism. Plant Cell Environ 35:1756–1768

    Article  CAS  PubMed  Google Scholar 

  • Takada Y, Ye X, Simon S (2007) The integrins. Genome Biol 8:215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Titlyanov EA, Titlyanova TV, Lüning K (1996) Diurnal and circadian periodicity of mitosis and growth in marine macroalgae.II. The green alga Ulva pseudocurvata. Eur J Phycol 31:181–188

    Article  Google Scholar 

  • Uji T, Endo H, Mizuta H (2020) Sexual reproduction via a 1-aminocyclopropane-1-carboxylic acid-dependent pathway through redox modulation in the marine red alga Pyropia yezoensis (Rhodophyta). Front Plant Sci 11:60

    Article  PubMed  PubMed Central  Google Scholar 

  • Uji T, Matsuda R, Takechi K, Takano H, Mizuta H, Takio S (2016) Ethylene regulation of sexual reproduction in the marine red alga Pyropia yezoensis (Rhodophyta). J Appl Phycol 28:3501–3509

    Article  CAS  Google Scholar 

  • Uji T, Gondaira Y, Fukuda S, Mizuta H, Saga N (2019) Characterization and expression profiles of small heat shock proteins in the marine red alga Pyropia yezoensis. Cell Stress Chaperones 24:223–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uji T, Monma R, Mizuta H, Saga N (2012) Molecular characterization and expression analysis of two Na+/H+ antiporter genes in the marine red alga Porphyra yezoensis. Fisheries Sci 78:985–991

    Article  CAS  Google Scholar 

  • Uji T, Ueda S, Mizuta H (2022) Identification, characterization, and expression analysis of spondin-like and fasciclin-like genes in Neopyropia yezoensis, a marine red alga. Phycology 2:45–59

    Article  Google Scholar 

  • Viola R, Nyvall P, Pedersén M (2001) The unique features of starch metabolism in red algae. Proc Royal Soc B 268:1417–1422

    Article  CAS  Google Scholar 

  • Wingett SW, Andrews S (2018) FastQ Screen: a tool for multi-genome mapping and quality control. F1000Research 7:1338

  • Yanagisawa R, Sekine N, Mizuta H, Uji T (2019) Transcriptomic analysis under ethylene precursor treatment uncovers the regulation of gene expression linked to sexual reproduction in the dioecious red alga Pyropia pseudolinearis. J Appl Phycol 31:3317–3329

    Article  CAS  Google Scholar 

  • Yu S, Blennow A, Bojko M, Madsen F, Olsen CE, Engelsen SB (2002) Physico-chemical characterization of floridean starch of red algae. Starch 54:66–74

    Article  CAS  Google Scholar 

  • Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61:209–234

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We wish to thank Drs. Katsutoshi Arai and Takafumi Fujimoto (Hokkaido University, Japan) for kindly providing the LightCycler 480 system.

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This work was supported by the Grant-in-Aid for Young Scientists [grant number19K15907 to TU] from the Japan Society for the Promotion of Science.

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TU was responsible for the design of the experiments and interpretation of the data. SK and TU performed the experiments. SK, TU, and HM wrote the manuscript. All authors have read and approved the final version of the manuscript.

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Correspondence to Toshiki Uji.

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Kominami, S., Mizuta, H. & Uji, T. Transcriptome Profiling in the Marine Red Alga Neopyropia yezoensis Under Light/Dark Cycle. Mar Biotechnol 24, 393–407 (2022). https://doi.org/10.1007/s10126-022-10121-3

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