RNA-seq analysis of the transcriptional response to blue and red light in the extremophilic red alga, Cyanidioschyzon merolae

Springer Science and Business Media LLC - Tập 16 - Trang 657-669 - 2016
Mehmet Tardu1, Ugur Meric Dikbas2, Ibrahim Baris2, Ibrahim Halil Kavakli1,2,3
1Computational Science and Engineering, Koc University, Istanbul, Turkey
2Molecular Biology and Genetics, Koc University, Istanbul, Turkey
3Chemical and Biological Engineering, Koc University, Istanbul, Turkey

Tóm tắt

Light is one of the main environmental cues that affects the physiology and behavior of many organisms. The effect of light on genome-wide transcriptional regulation has been well-studied in green algae and plants, but not in red algae. Cyanidioschyzon merolae is used as a model red algae, and is suitable for studies on transcriptomics because of its compact genome with a relatively small number of genes. In addition, complete genome sequences of the nucleus, mitochondrion, and chloroplast of this organism have been determined. Together, these attributes make C. merolae an ideal model organism to study the response to light stimuli at the transcriptional and the systems biology levels. Previous studies have shown that light significantly affects cell signaling in this organism, but there are no reports on its blue light- and red light-mediated transcriptional responses. We investigated the direct effects of blue and red light at the transcriptional level using RNA-seq. Blue and red lights were found to regulate 35 % of the total genes in C. merolae. Blue light affected the transcription of genes involved in protein synthesis while red light specifically regulated the transcription of genes involved in photosynthesis and DNA repair. Blue or red light regulated genes involved in carbon metabolism and pigment biosynthesis. Overall, our data showed that red and blue light regulate the majority of the cellular, cell division, and repair processes in C. merolae.

Tài liệu tham khảo

Asimgil H, Kavakli IH (2012) Purification and characterization of five members of photolyase/cryptochrome family from Cyanidioschyzon merolae. Plant Sci 185–186:190–198 Beel B, Prager K, Spexard M, Sasso S, Weiss D, Muller N, Heinnickel M, Dewez D, Ikoma D, Grossman AR, Kottke T, Mittag M (2012) A flavin binding cryptochrome photoreceptor responds to both blue and red light in Chlamydomonas reinhardtii. Plant Cell 24:2992–3008 Berrocal-Tito G, Sametz-Baron L, Eichenberg K, Horwitz BA, Herrera-Estrella A (1999) Rapid blue light regulation of a Trichoderma harzianum photolyase gene. J Biol Chem 274:14288–14294 Burgos A, Szymanski J, Seiwert B, Degenkolbe T, Hannah MA, Giavalisco P, Willmitzer L (2011) Analysis of short-term changes in the Arabidopsis thaliana glycerolipidome in response to temperature and light. Plant J 66:656–668 Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139:5-17 Danon A, Coll NS, Apel K (2006) Cryptochrome-1-dependent execution of programmed cell death induced by singlet oxygen in Arabidopsis thaliana. Proc Natl Acad Sci U S A 103:17036–17041 Delwiche CF, Cooper ED (2015) The evolutionary origin of a terrestrial flora. Curr Biol 25:R899–R910 Figueroa FL, Aguilera J, Jimenez C, Vergara JJ, Robles MD, Niell FX (1995) Growth, pigment synthesis and nitrogen assimilation in the red alga Porphyra sp (Bangiales, Rhodophyta) under blue and red light. Sci Mar 59:9–20 Forbes-Stovall J, Howton J, Young M, Davis G, Chandler T, Kessler B, Rinehart CA, Jacobshagen S (2014) Chlamydomonas reinhardtii strain CC-124 is highly sensitive to blue light in addition to green and red light in resetting its circadiari clock, with the blue-light photoreceptor plant cryptochrome likely acting as negative modulator. Plant Physiol Bioch 75:14–23 Fortunato AE, Annunziata R, Jaubert M, Bouly JP, Falciatore A (2015) Dealing with light: the widespread and multitasking cryptochrome/photolyase family in photosynthetic organisms. Plant Physiol 172:42–54 Gadjev I, Vanderauwera S, Gechev TS, Laloi C, Minkov IN, Shulaev V, Apel K, Inze D, Mittler R, Van Breusegem F (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol 141:436–445 Garcia-Alcalde F, Okonechnikov K, Carbonell J, Cruz LM, Gotz S, Tarazona S, Dopazo J, Meyer TF, Conesa A (2012) Qualimap: evaluating next-generation sequencing alignment data. Bioinformatics 28:2678–2679 Gomes A, Fernandes E, Lima JLFC (2005) Fluorescence probes used for detection of reactive oxygen species. J Biochem Bioph Meth 65:45–80 Guan LM, Scandalios JG (2000) Hydrogen-peroxide-mediated catalase gene expression in response to wounding. Free Radic Biol Med 28:1182–1190 Hader DP, Kumar HD, Smith RC, Worrest RC (1998) Effects of UV radiation on aquatic ecosystems and interactions with climate change. J Photoch Photobio B 46:53–68 Hegemann P (2008) Algal sensory photoreceptors. Annu Rev Plant Biol 59:167–189 Heinrich S, Valentin K, Frickenhaus S, John U, Wiencke C (2012) Transcriptomic analysis of acclimation to temperature and light stress in Saccharina latissima (Phaeophyceae). PLoS One 7:e44342 Hubschmann T, Yamamoto H, Gieler T, Murata N, Borner T (2005) Red and far-red light alter the transcript profile in the cyanobacterium Synechocystis sp. PCC 6803: impact of cyanobacterial phytochromes. FEBS Lett 579:1613–1618 Jiao Y, Yang H, Ma L, Sun N, Yu H, Liu T, Gao Y, Gu H, Chen Z, Wada M, Gerstein M, Zhao H, Qu LJ, Deng XW (2003) A genome-wide analysis of blue-light regulation of Arabidopsis transcription factor gene expression during seedling development. Plant Physiol 133:1480–1493 Kanesaki Y, Imamura S, Minoda A, Tanaka K (2012) External light conditions and internal cell cycle phases coordinate accumulation of chloroplast and mitochondrial transcripts in the red alga Cyanidioschyzon merolae. DNA Res 19:289–303 Kianianmomeni A, Hallmann A (2014) Algal photoreceptors: in vivo functions and potential applications. Planta 239:1–26 Kleine T, Leister D (2016) Retrograde signaling: organelles go networking. Biochim Biophys Acta 1857:1313–1325 Kolowrat C, Partensky F, Mella-Flores D, Le Corguille G, Boutte C, Blot N, Ratin M, Ferreol M, Lecomte X, Gourvil P, Lennon JF, Kehoe DM, Garczarek L (2010) Ultraviolet stress delays chromosome replication in light/dark synchronized cells of the marine cyanobacterium Prochlorococcus marinus PCC9511. BMC Microbiol 10:204 Korbee N, Figueroa FL, Aguilera J (2005) Effect of light quality on the accumulation of photosynthetic pigments, proteins and mycosporine-like amino acids in the red alga Porphyra leucosticta (Bangiales, Rhodophyta). J Photoch Photobio B 80:71–78 Lepisto A, Toivola J, Nikkanen L, Rintamaki E (2012) Retrograde signaling from functionally heterogeneous plastids. Front Plant Sci 3:286 Li X, Kim YB, Uddin MR, Lee S, Kim SJ, Park SU (2013) Influence of light on the free amino acid content and gamma-aminobutyric acid synthesis in Brassica juncea seedlings. J Agr Food Chem 61:8624–8631 Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25:402–408 Lopez L, Carbone F, Bianco L, Giuliano G, Facella P, Perrotta G (2012) Tomato plants overexpressing cryptochrome 2 reveal altered expression of energy and stress-related gene products in response to diurnal cues. Plant Cell Environ 35:994–1012 Lucas-Lledo JI, Lynch M (2009) Evolution of mutation rates: phylogenomic analysis of the photolyase/cryptochrome family. Mol Biol Evol 26:1143–1153 Ma L, Li J, Qu L, Hager J, Chen Z, Zhao H, Deng XW (2001) Light control of arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell 13:2589–2607 Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks. Bioinformatics 21:3448–3449 Marchler-Bauer A, Zheng C, Chitsaz F, Derbyshire MK, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Lu S, Marchler GH, Song JS, Thanki N, Yamashita RA, Zhang D, Bryant SH (2013) CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res 41:D348–D352 Matsuzaki M, Misumi O, Shin IT, Maruyama S, Takahara M, Miyagishima SY, Mori T, Nishida K, Yagisawa F, Nishida K, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, Minoda A, Sano M, Nomoto H, Oishi K, Hayashi H, Ohta F, Nishizaka S, Haga S, Miura S, Morishita T, Kabeya Y, Terasawa K, Suzuki Y, Ishii Y, Asakawa S, Takano H, Ohta N, Kuroiwa H, Tanaka K, Shimizu N, Sugano S, Sato N, Nozaki H, Ogasawara N, Kohara Y, Kuroiwa T (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657 Mi HY, Muruganujan A, Casagrande JT, Thomas PD (2013) Large-scale gene function analysis with the PANTHER classification system. Nat Protoc 8:1551–1566 Minoda A, Nagasawa K, Hanaoka M, Horiuchi M, Takahashi H, Tanaka K (2005) Microarray profiling of plastid gene expression in a unicellular red alga, Cyanidioschyzon merolae. Plant Mol Biol 59:375–385 Minoda A, Sakagami R, Yagisawa F, Kuroiwa T, Tanaka K (2004) Improvement of culture conditions and evidence for nuclear transformation by homologous recombination in a red alga, Cyanidioschyzon merolae 10D. Plant Cell Physiol 45:667–671 Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498 Monnier A, Liverani S, Bouvet R, Jesson B, Smith JQ, Mosser J, Corellou F, Bouget FY (2010) Orchestrated transcription of biological processes in the marine picoeukaryote Ostreococcus exposed to light/dark cycles. BMC Genomics 11:192 Musacchia F, Basu S, Petrosino G, Salvemini M, Sanges R (2015) Annocript: a flexible pipeline for the annotation of transcriptomes able to identify putative long noncoding RNAs. Bioinformatics 31:2199–2201 Nishida K, Yagisawa F, Kuroiwa H, Nagata T, Kuroiwa T (2005) Cell cycle-regulated, microtubule-independent organelle division in Cyanidioschyzon merolae. Mol Biol Cell 16:2493–2502 Nozaki H, Takano H, Misumi O, Terasawa K, Matsuzaki M, Maruyama S, Nishida K, Yagisawa F, Yoshida Y, Fujiwara T, Takio S, Tamura K, Chung SJ, Nakamura S, Kuroiwa H, Tanaka K, Sato N, Kuroiwa T (2007) A 100%-complete sequence reveals unusually simple genomic features in the hot-spring red alga Cyanidioschyzon merolae. BMC Biol 5:28 Pandhal J, Wright PC, Biggs CA (2007) A quantitative proteomic analysis of light adaptation in a globally significant marine cyanobacterium Prochlorococcus marinus MED4. J Proteome Res 6:996–1005 Partch CL, Sancar A (2005) Photochemistry and photobiology of cryptochrome blue-light photopigments: the search for a photocycle. J Photochem Photobiol 81:1291–1304 Perez-Rodriguez P, Riano-Pachon DM, Correa LG, Rensing SA, Kersten B, Mueller-Roeber B (2010) PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res 38:D822–D827 Pireyre M, Burow M (2015) Regulation of MYB and bHLH transcription factors: a glance at the protein level. Mol Plant 8:378–388 Reisdorph NA, Small GD (2004) The CPH1 gene of Chlamydomonas reinhardtii encodes two forms of cryptochrome whose levels are controlled by light-induced proteolysis. Plant Physiol 134:1546–1554 Roh MH, Shingles R, Cleveland MJ, McCarty RE (1998) Direct measurement of calcium transport across chloroplast inner-envelope vesicles. Plant Physiol 118:1447–1454 Sai JQ, Johnson CH (2002) Dark-stimulated calcium ion fluxes in the chloroplast stroma and cytosol. Plant Cell 14:1279–1291 Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504 Stark MR, Dunn EA, Dunn WS, Grisdale CJ, Daniele AR, Halstead MR, Fast NM, Rader SD (2015) Dramatically reduced spliceosome in Cyanidioschyzon merolae. Proc Natl Acad Sci U S A 112:1191–1200 Suter B, Wellinger RE, Thoma F (2000) DNA repair in a yeast origin of replication: contributions of photolyase and nucleotide excision repair. Nucleic Acids Res 28:2060–2068 Suzek BE, Huang H, McGarvey P, Mazumder R, Wu CH (2007) UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics 23:1282–1288 Szymanski J, Brotman Y, Willmitzer L, Cuadros-Inostroza A (2014) Linking gene expression and membrane lipid composition of Arabidopsis. Plant Cell 26:915–928 Talarico L, Maranzana G (2000) Light and adaptive responses in red macroalgae: an overview. J Photochem Photobiol 56:1–11 Tanaka K, Hanaoka M (2012) The early days of plastid retrograde signaling with respect to replication and transcription. Front Plant Sci 3:301 Terui S, Suzuki K, Takahashi H, Itoh R, Kuroiwa T (1995) Synchronization of chloroplast division in the ultramicroalga Cyanidioschyzon merolae (Rhodophyta) by treatment with light and aphidicolin. J Phycol 31:958–961 Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578 Ueno Y, Aikawa S, Kondo A, Akimoto S (2015) Light adaptation of the unicellular red alga, Cyanidioschyzon merolae, probed by time-resolved fluorescence spectroscopy. Photosynth Res 125:211–218 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 Wang ZY, Kenigsbuch D, Sun L, Harel E, Ong MS, Tobin EM (1997) A Myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. Plant Cell 9:491–507 Yagi Y, Shiina T (2014) Recent advances in the study of chloroplast gene expression and its evolution. Front Plant Sci 5:61