Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Dynamic response of the transcriptome of a psychrophilic diatom, Chaetoceros neogracile, to high irradiance

  • 610 Accesses

  • 37 Citations


Large-scale RNA profiling revealed that high irradiance differentially regulated 577 out of 1,439 non-redundant genes of the Antarctic marine diatom Chaetoceros neogracile, represented on a custom cDNA chip, during 6 h of treatment. Among genes that were up- or down-regulated more than twofold within 30 min of treatment (310/1,439), about half displayed an acclimatory response during 6 h under high light. Expression of the remaining non-acclimatory genes also rapidly returned to initial levels within 30 min following a shift to low irradiance. High light altered expression of most of the photosynthesis genes (48/70), in contrast to genes in other functional categories. In addition, opposite response patterns were provoked in genes encoding fucoxanthin chlorophyll a/c binding protein (FCP), the main component of the diatom light-harvesting complex; high irradiance caused a decrease in expression of most FCP genes, but drove the rapid and specific up-regulation of ten others. C. neogracile responded very promptly to a change in light intensity by rapidly adjusting the transcript levels of FCP genes up-regulated by high light, and these dynamic adjustments coincided well with diatoxanthin (Dtx) levels formed by the xanthophyll cycle under the same conditions. The observation that the non-photochemical quenching (NPQ) capacity of this polar diatom was highly dependent on Dtx, which could bind to FCP and trigger NPQ, suggests that the up-regulated FCP gene products may participate in a photoprotective process as Dtx-binding proteins.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7





Non-photochemical quenching






Diadinoxanthin de-epoxidase


Fucoxanthin chlorophyll a/c binding protein


Light-harvesting complex


  1. Ahn TK, Avenson TJ, Ballottari M, Cheng YC, Niyogi KK, Bassi R, Fleming GR (2008) Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320:794–797

  2. Allen JF, Pfannschmidt T (2000) Balancing the two photosystems: photosynthetic electron transfer governs transcription of reaction centre genes in chloroplasts. Phil Trans R Soc 355:1351–1359

  3. Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou S, Allen AE, Apt KE, Bechner M, Brzezinski MA, Chaal BK, Chiovitti A, Davis AK, Demarest MS, Detter JC, Glavina T, Goodstein D, Hadi MZ, Hellsten U, Hildebrand M, Jenkins BD, Jurka J, Kapitonov VV, Kroger N, Lau WW, Lane TW, Larimer FW, Lippmeier JC, Lucas S, Medina M, Montsant A, Obornik M, Parker MS, Palenik B, Pazour GJ, Richardson PM, Rynearson TA, Saito MA, Schwartz DC, Thamatrakoln K, Valentin K, Vardi A, Wilkerson FP, Rokhsar DS (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86

  4. Becker F, Rhiel E (2006) Immuno-electron microscopic quantification of the fucoxanthin chlorophyll a/c binding polypeptides Fcp2, Fcp4, and Fcp6 of Cyclotella cryptica grown under low- and high-light intensities. Int Microbiol 9:29–36

  5. Beer A, Gundermann K, Beckmann J, Büchel C (2006) Subunit composition and pigmentation of fucoxanthin-chlorophyll proteins in diatoms: evidence for a subunit involved in diadinoxanthin and diatoxanthin binding. Biochemistry 45:13046–13053

  6. Bhaya D, Grossman AR (1993) Characterization of gene clusters encoding the fucoxanthin chlorophyll proteins of the diatom Phaeodactylum tricornutum. Nucleic Acids Res 21:4458–4466

  7. Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP, Rayko E, Salamov A, Vandepoele K, Beszteri B, Gruber A, Heijde M, Katinka M, Mock T, Valentin K, Verret F, Berges JA, Brownlee C, Cadoret JP, Chiovitti A, Choi CJ, Coesel S, De Martino A, Detter JC, Durkin C, Falciatore A, Fournet J, Haruta M, Huysman MJJ, Jenkins BD, Jiroutova K, Jorgensen RE, Joubert Y, Kaplan A, Kroger N, Kroth PG, La Roche J, Lindquist E, Lommer M, Martin-Jezequel V, Lopez PJ, Lucas S, Mangogna M, McGinnis K, Medlin LK, Montsant A, Oudot-Le Secq MP, Napoli C, Obornik M, Parker MS, Petit JL, Porcel BM, Poulsen N, Robison M, Rychlewski L, Rynearson TA, Schmutz J, Shapiro H, Siaut M, Stanley M, Sussman MR, Taylor AR, Vardi A, von Dassow P, Vyverman W, Willis A, Wyrwicz LS, Rokhsar DS, Weissenbach J, Armbrust EV, Green BR, Van De Peer Y, Grigoriev IV (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456:239–244

  8. Choi HG, Joo HM, Jung W, Hong SS, Kang J-S, Kang S-H (2008) Morphology and phylogenetic relationships of some psychrophilic polar diatoms (Bacillariophyta). Nova Hedwig Beih 133:7–30

  9. Demmig-Adams B, Adams WWI, Heber U, Neimanis S, Winter K, Krüger A, Czygan F-C, Bilger W, Björkman O (1990) Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts. Plant Physiol 92:293–301

  10. Eppard M, Rhiel E (1998) The genes encoding light-harvesting subunits of Cyclotella cryptica (Bacillariophyceae) constitute a complex and heterogeneous family. Mol Gen Genet 260:335–345

  11. Eppard M, Krumbein WE, von Haeseler A, Rhiel E (2000) Characterization of fcp4 and fcp12, two additional genes encoding light harvesting proteins of Cyclotella cryptica (Bacillariophyceae) and phylogenetic analysis of this complex gene family. Plant Biol 2:283–289

  12. Gagne G, Guertin M (1992) The early genetic response to light in the green unicellular alga Chlamydomonas eugametos grown under light dark cycles involves genes that represent direct responses to light and photosynthesis. Plant Mol Biol 18:429–445

  13. Goss R, Mewes H, Wilhelm C (1999) Stimulation of the diadinoxanthin cycle by UV-B radiation in the diatom Phaeodactylum tricornutum. Photosynth Res 59:73–80

  14. Goss R, Ann Pinto E, Wilhelm C, Richter M (2006) The importance of a highly active and DpH-regulated diatoxanthin epoxidase for the regulation of the PS II antenna function in diadinoxanthin cycle containing algae. J Plant Physiol 163:1008–1021

  15. Goss R, Opitz C, Lepetit B, Wilhelm C (2008) The synthesis of NPQ-effective zeaxanthin depends on the presence of a transmembrane proton gradient and a slightly basic stromal side of the thylakoid membrane. Planta 228:999–1009

  16. Grossman AR, Bhaya D, Apt KE, Kehoe DM (1995) Light-harvesting complexes in oxygenic photosynthesis: diversity, control, and evolution. Ann Rev Genet 29:231–288

  17. Grouneva I, Jakob T, Wilhelm C, Goss R (2008) A new multicomponent NPQ mechanism in the diatom Cyclotella meneghiniana. Plant Cell Physiol 49:1217–1225

  18. Guglielmi G, Lavaud J, Rousseau B, Etienne AL, Houmard J, Ruban AV (2005) The light-harvesting antenna of the diatom Phaeodactylum tricornutum. Evidence for a diadinoxanthin-binding subcomplex. FEBS J 272:4339–4348

  19. Gundermann K, Büchel C (2008) The fluorescence yield of the trimeric fucoxanthin-chlorophyll-protein FCPa in the diatom Cyclotella meneghiniana is dependent on the amount of bound diatoxanthin. Photosynth Res 95:229–235

  20. Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc Natl Acad Sci USA 96:8762–8767

  21. Hihara Y, Kamei A, Kanehisa M, Kaplan A, Ikeuchi M (2001) DNA microarray analysis of cyanobacterial gene expression during acclimation to high light. Plant Cell 13:793–806

  22. Holt NE, Fleming GR, Niyogi KK (2004) Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 43:8281–8289

  23. Horton P, Wentworth M, Ruban A (2005) Control of the light harvesting function of chloroplast membranes: the LHCII-aggregation model for non-photochemical quenching. FEBS Lett 579:4201–4206

  24. Horton P, Johnson MP, Perez-Bueno ML, Kiss AZ, Ruban AV (2008) Photosynthetic acclimation: does the dynamic structure and macro-organisation of photosystem II in higher plant grana membranes regulate light harvesting states? FEBS J 275:1069–1079

  25. Hwang Y-s, Jung G, Jin E (2008) Transcriptome analysis of acclimatory responses to thermal stress in Antarctic algae. Biochem Biophys Res Commun 367:635–641

  26. Jin E, Yokthongwattana K, Polle JE, Melis A (2003) Role of the reversible xanthophyll cycle in the photosystem II damage and repair cycle in Dunaliella salina. Plant Physiol 132:352–364

  27. Jung G, Lee CG, Kang SH, Jin E (2007) Annotation and expression profile analysis of cDNAs from the Antarctic diatom Chaetoceros neogracile. J Microbiol Biotechnol 17:1330–1337

  28. Kiss AZ, Ruban AV, Horton P (2008) The PsbS protein controls the organization of the photosystem II antenna in higher plant thylakoid membranes. J of Biol Chem 283:3972–3978

  29. Kramer DM, Cruz JA, Kanazawa A (2003) Balancing the central roles of the thylakoid proton gradient. Trends Plant Sci 8:27–32

  30. Krell A, Beszteri B, Dieckmann G, Glöckner G, Valentin K, Mock T (2008) A new class of ice-binding proteins discovered in a salt-stress-induced cDNA library of the psychrophilic diatom Fragilariopsis cylindrus (Bacillariophyceae). Eur J Phycol 43:423–433

  31. Lavaud J, Rousseau B, van Gorkom HJ, Etienne AL (2002a) Influence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom Phaeodactylum tricornutum. Plant Physiol 129:1398–1406

  32. Lavaud J, Rousseau B, Etienne AL (2002b) In diatoms, a transthylakoid proton gradient alone is not sufficient to induce a non-photochemical fluorescence quenching. FEBS Lett 523:163–166

  33. Lavaud J, van Gorkom HJ, Etienne AL (2002c) Photosystem II electron transfer cycle and chlororespiration in planktonic diatoms. Photosynth Res 74:51–59

  34. Lavaud J, Rousseau B, Etienne AL (2003) Enrichment of the light-harvesting complex in diadinoxanthin and implications for the nonphotochemical fluorescence quenching in diatoms. Biochemistry 42:5802–5808

  35. Ledford HK, Niyogi KK (2005) Singlet oxygen and photo-oxidative stress management in plants and algae. Plant Cell Environ 28:1037–1045

  36. Li X-P, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395

  37. Li XP, Gilmore AM, Caffarri S, Bassi R, Golan T, Kramer D, Niyogi KK (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J of Biol Chem 279:22866–22874

  38. Lohr M, Wilhelm C (1999) Algae displaying the diadinoxanthin cycle also possess the violaxanthin cycle. Proc Natl Acad Sci USA 96:8784–8789

  39. Maheswari U, Montsant A, Goll J, Krishnasamy S, Rajyashri KR, Patell VM, Bowler C (2005) The diatom EST database. Nucleic Acids Res 33:D344–D347

  40. Mock T, Valentin K (2004) Photosynthesis and cold acclimation—molecular evidence from a polar diatom. J Phycol 40:732–741

  41. Mock T, Krell A, Glöckner G, Kolukisaoglu Ü, Valentin K (2006) Analysis of expressed sequence tags (ESTs) from the polar diatom Fragilariopsis cylindrus. J Phycol 42:78–85

  42. Morgan-Kiss RM, Priscu JC, Pocock T, Gudynaite-Savitch L, Huner NP (2006) Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiol Mol Mol Biol Rev 70:222–252

  43. Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

  44. Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Ann Rev Plant Phys Plant Mol Biol 50:333–359

  45. Oeltjen A, Marquardt J, Rhiel E (2004) Differential circadian expression of genes fcp2 and fcp6 in Cyclotella cryptica. Int Microbiol 7:127–131

  46. Olaizola M, Yamamoto HY (2004) Short-term response of the diadinoxanthin cycle and fluorescence yield to high irradiance in Chaetoceros muelleri (Bacillariophyceae). J Phycol 30:606–612

  47. Park S, Polle JE, Melis A, Lee TK, Jin E (2006) Up-regulation of photoprotection and PSII-repair gene expression by irradiance in the unicellular green alga Dunaliella salina. Mar Biotechnol 8:120–128

  48. Pascal AA, Liu Z, Broess K, Oort Bv, Amerongen Hv, Wang C, Horton P, Robert B, Chang W, Ruban A (2005) Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nat Lett 436:134–137

  49. Pyszniak AM, Gibbs SP (1992) Immunocytochemical localization of photosystem I and the fucoxanthin-chlorophyll a/c light-harvesting complex in the diatom Phaeodactylum tricornutum. Protoplasma 166:208–217

  50. Rossel JB, Wilson IW, Pogson BJ (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol 130:1109–1120

  51. Ruban A, Lavaud J, Rousseau B, Guglielmi G, Horton P, Etienne AL (2004) The super-excess energy dissipation in diatom algae: comparative analysis with higher plants. Photosynth Res 82:165–175

  52. Savard F, Richard C, Guertin M (1996) The Chlamydomonas reinhardtii LI818 gene represents a distant relative of the cabI/II genes that is regulated during the cell cycle and in response to illumination. Plant Mol Biol 32:461–473

  53. Seki M, Narusaka M, Kamiya A, Ishida J, Satou M, Sakurai T, Nakajima M, Enju A, Akiyama K, Oono Y, Muramatsu M, Hayashizaki Y, Kawai J, Carninci P, Itoh M, Ishii Y, Arakawa T, Shibata K, Shinagawa A, Shinozaki K (2002) Functional annotation of a full-length Arabidopsis cDNA collection. Science 296:141–145

  54. Thomas DN, Dieckmann GS (2002) Antarctic Sea ice—a habitat for extremophiles. Science 295:641–644

  55. van de Poll WH, van Leeuwe MA, Roggeveld J, Buma AGJ (2005) Nutrient limitation and high irradiance acclimation reduce PAR and UV-induced viability loss in the Antarctic diatom Chaetoceros brevis (Bacillariophyceae). J Phycol 41:840–850

  56. Wilhelm C, Büchel C, Fisahn J, Goss R, Jakob T, Laroche J, Lavaud J, Lohr M, Riebesell U, Stehfest K, Valentin K, Kroth PG (2006) The regulation of carbon and nutrient assimilation in diatoms is significantly different from green algae. Protist 157:91–124

  57. Yamano T, Miura K, Fukuzawa H (2008) Expression analysis of genes associated with the induction of the carbon-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol 147:340–354

  58. Zhu S-H, Green BR (2008) Light-harvesting and photoprotection in diatoms: identification and expression of L818-like proteins. In: Allen JF, Gantt E, Golbeck JH, Osmond B (eds) Energy from the sun: 14th international congress on photosynthesis. Springer, The Netherlands, pp 261–264

Download references


This work was supported by the Research Fund of Hanyang University (HY/2006/S).

Author information

Correspondence to Yong-sic Hwang or EonSeon Jin.

Additional information

S. Park and G. Jung have equally contributed to the paper.

E. Jin and Y. Hwang are authors to whom correspondence should be addressed.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 1529 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Park, S., Jung, G., Hwang, Y. et al. Dynamic response of the transcriptome of a psychrophilic diatom, Chaetoceros neogracile, to high irradiance. Planta 231, 349 (2010).

Download citation


  • Transcriptome
  • Antarctic diatom
  • High irradiance
  • Xanthophyll cycle
  • Fucoxanthin chlorophyll a/c binding protein
  • NPQ (non-photochemical quenching)