Compartmental cross-talk in the regulation of light harvesting complex transcription under short-term light and temperature stress in Chlamydomonas reinhardtii

Botany

Volumn 87, Issue 4, 2009, Pages 375-386

  Humby, Penny L ^a   Cunningham, Michelle L ^a   Saunders, Holly L ^a   Price, Julie A ^a   Durnford, Dion G ^a  

^a UNIVERSITY OF NEW BRUNSWICK   (Canada)

Author keywords

Chlamydomonas; Light stress; Light harvesting complex; Photoacclimation; Retrograde signalling

Indexed keywords

ENVIRONMENTAL STRESS; GENE EXPRESSION; GREEN ALGA; INHIBITOR; LIGHT EFFECT; METABOLITE; MITOCHONDRION; PHOTOSYNTHESIS; PLASTID; TEMPERATURE EFFECT;

CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII;

EID: 68049127968     PISSN: 19162804     EISSN: None     Source Type: Journal    
DOI: 10.1139/B09-005     Document Type: Article

References (72)

1. Adamiec, M., Drath, M., and Jackowski, G. 2008. Redox state of plastoquinone pool regulates expression of Arabidopsis thaliana genes in response to elevated irradiance. Acta Biochim. Pol. 55: 161-173. PMID:18231654.
2. Allen, J.F. 1992. Protein phosphorylation in regulation of photosynthesis. Biochim. Biophys. Acta, 1098: 275-335. PMID: 1310622.
3. Anderson, J.M., Chow, W.S., and Park, Y.I. 1995. The grand design of photosynthesis: acclimation of the photosynthetic apparatus to environmental cues. Photosynth. Res. 46: 129-139. doi:10.1007/BF00020423.
4. Bailey, S., Walters, R., Jansson, S., and Horton, P. 2001. Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta, 213: 794-801. doi:10.1007/s004250100556. PMID:11678285.
5. Beck, C.F. 2005. Signaling pathways from the chloroplast to the nucleus. Planta, 222: 743-756. doi:10.1007/s00425-005-0021-2. PMID:16231154.
6. Chen, Y.B., Durnford, D.G., Koblizek, M., and Falkowski, P.G. 2004. Plastid regulation of Lhcb1 transcription in the chlorophyte alga Dunaliella tertiolecta. Plant Physiol. 136: 3737- 3750. doi:10.1104/pp.104.038919. PMID:15516517.
7. Cleland, R.E. 1998. Voltametric measurement of the plastoquinone redox state in isolated thylakoids. Photosynth. Res. 58: 183-192. doi:10.1023/A: 1006165501184.
8. Davies, J., Weeks, D., and Grossman, A. 1992. Expression of the arylsulfatase gene from the b2-tubulin promoter in Chlamydomonas reinhardtii. Nucleic Acids Res. 20: 2959-2965. doi:10. 1093/nar/20.12.2959. PMID:1620590.
9. Debuchy, R., Purton, S., and Rochaix, J. 1989. The argininosuccinate lyase gene of Chlamydomonas reinhardtii: an important tool for nuclear transformation and for correlating the genetic and molecular maps of the ARG7 locus. EMBO J. 8: 2803- 2809. PMID:2583083.
10. Durnford, D.G., and Falkowski, P.G. 1997. Chloroplast redox regulation of nuclear gene transcription during photoacclimation. Photosynth. Res. 53: 229-241. doi:10.1023/A:1005815725371.
11. Durnford, D.G., Price, J.A., McKim, S.M., and Sarchfield, M.L. 2003. Light-harvesting complex gene expression is controlled by both transcriptional and post-transcriptional mechanisms during photoacclimation in Chlamydomonas reinhardtii. Physiol. Plant. 118: 193-205. doi:10.1034/j.1399-3054.2003.00078.x.
12. Elrad, D., and Grossman, A.R. 2004. A genome's-eye view of the light-harvesting polypeptides of Chlamydomonas reinhardtii. Curr. Genet. 45: 61-75. doi:10.1007/s00294-003-0460-x. PMID: 14652691.
13. Ensminger, I., Busch, F., and Huner, N.P.A. 2006. Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiol. Plant. 126: 28-44. doi:10.1111/j.1399-3054.2006. 00627.x.
14. Escoubas, J.M., Lomas, M., Laroche, J., and Falkowski, P.G. 1995. Light-intensity regulation of cab gene-transcription is signaled by the redox state of the plastoquinone pool. Proc. Natl. Acad. Sci. U.S.A. 92: 10237-10241. doi:10.1073/pnas.92.22.10237. PMID:7479759.
15. Fey, V., Wagner, R., Bräutigam, K., Wirtz, M., Hell, R., Dietzmann, A., Leister, D., Oelmüller, R., and Pfannschmidt, T. 2004. Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. J. Biol. Chem. 280: 5318-5328. doi:10.1074/jbc.M406358200. PMID:15561727.
16. Fischer, B.B., Wiesendanger, M., and Eggen, R.I.L. 2006. Growth condition-dependent sensitivity, photodamage and stress response of Chlamydomonas reinhardtii exposed to high light conditions. Plant Cell Physiol. 47: 1135-1145. doi:10.1093/pcp/pcj085. PMID:16857695.
17. Frigerio, S., Campoli, C., Zorzan, S., Fantoni, L., Crosatti, C., Drepper, F., Haehnel, W., Cattivelli, L., Morosinotto, T., and Bassi, R. 2007. Photosynthetic antenna size in higher plants is controlled by the plastoquinone redox state at the posttranscriptional rather than transcriptional level. J. Biol. Chem. 282: 29457-29469. doi:10.1074/jbc.M705132200. PMID: 17675669.
18. Fujita, Y., Iwama, Y., Ohki, K., Murakami, A., and Hagiwara, N. 1989. Regulation of the size of light-harvesting antennae in response to light-intensity in the green alga Chlorella pyrenoidosa. Plant Cell Physiol. 30: 1029-1037.
19. Gray, J.C., Sullivan, J.A., Wang, J.H., Jerome, C.A., and MacLean, D. 2003. Coordination of plastid and nuclear gene expression. Philos. Trans. Royal Soc. Philos. Trans. R. Soc. Lond. Ser. B, 358: 135-144. doi:10.1098/rstb.2002. 1180.
20. Hahn, D., and Kück, U. 1999. Identification of DNA sequencescontrolling light- and chloroplast- dependent expression of the Lhcb1 gene from Chlamydomonas reinhardtii. Curr. Genet. 34: 459-466. doi:10.1007/s002940050420. PMID:9933357.
21. Harris, E.H. 1989. The Chlamydomonas sourcebook - a comprehansive guide to biology and laboratory use. Academic Press, San Diego, Calif.
22. Hedtke, B., Wagner, I., Börner, T., and Hess, W.R. 1999. Interorganellar cross-talk in higher plants: impaired chloroplast development affects mitochondrial gene and transcript levels. Plant J. 19: 635-643. doi:10.1046/j.1365-313x.1999.00554.x. PMID:10571849.
23. Heifetz, P.B., Forster, B., Osmond, C.B., Giles, L.J., and Boynton, J.E. 2000. Effects of acetate on facultative autotrophy in Chlamydomonas reinhardtii assessed by photosynthetic measurements and stable isotope analyses. Plant Physiol. 122: 1439-1445. doi:10.1104/pp.122.4.1439. PMID:10759539.
24. Hermsmeier, D., Schulz, R., and Senger, H. 1994. Formation of light-harvesting complexes of photosystem-II in Scenedesmus.1. Correlations between amounts of photosynthetic pigments, LHC messenger-RNAs and LHC apoproteins during constitutional dark-dependent and light-dependent LHC-gene expression. Planta, 193: 398-405. doi:10.1007/BF00201819.
25. Hihara, Y., Sonoike, K., Kanehisa, M., and Ikeuchi, M. 2003. DNA microarray analysis of redox-responsive genes in the genome of the cyanobacterium Synechocystis sp. Strain PCC 6803. J. Bacteriol. 185: 1719-1725. doi:10.1128/JB.185.5.1719-1725.2003. PMID:12591891.
26. Hoefnagel, M.H.N., Atkin, O.K., and Wiskich, J.T. 1998. Interdependence between chloroplasts and mitochondria in the light and the dark. Biochim. Biophys. Acta, 1366: 235-255. doi:10. 1016/S0005-2728(98)00126-131
27. Hsu, B.D., Lee, J.Y., and Pan, R.L. 1986. The 2 binding-sites for DCMU in photosystem-II. Biochem. Biophys. Res. Commun. 141: 682-688. doi:10.1016/S0006-291X(86)80226-1. PMID: 3541937.
28. Humby, P.L., and Durnford, D.G. 2006. Photoacclimation: physiological and molecular responses to changes in light environments. In Plant-environment interactions. Edited by Bingru Huang. CRC Press, Boca Raton, Fla. pp. 69-99.
29. Huner, N.P.A., Ö quist, G., and Sarhan, F. 1998. Energy balance and acclimation to light and cold. Trends Plant Sci. 3: 224-230. doi:10.1016/S1360-1385(98)01248-1255
30. Hurry, V., Tobiaeson, M., Kromer, S., Gardestrom, P., and Öquist, G. 1995. Mitochondria contribute to increased photosynthetic capacity of leaves of winter rye (Secale cereale L) following cold-hardening. Plant Cell Environ. 18: 69-76. doi:10.1111/j. 1365-3040.1995.tb00545.x.
31. Im, C.S., and Grossman, A.R. 2002. Identification and regulation of high light-induced genes in Chlamydomonas reinhardtii. Plant J. 30: 301-313. doi:10.1046/j.1365-313X.2001.01287.x. PMID: 12000678.
32. Karpinski, S., Reynolds, H., Karpinska, B., Wingsle, G., Creissen, G., and Mullineaux, P. 1999. Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science (Wash.), 284: 654-657. doi:10.1126/science.284.5414.654. PMID:10213690.
33. Kindle, K.L. 1987. Expression of a gene for a light-harvesting chlorophyll a/b-binding protein in Chlamydomonas reinhardtii: effect of light and acetate. Plant Mol. Biol. 9: 547-563. doi:10. 1007/BF00020532.
34. Kindle, K.L. 1990. High frequency nuclear transformation of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. U.S.A. 87: 1228- 1232. doi:10.1073/pnas.87. 3.1228. PMID:2105499.
35. Kovács, L., Weissner, W., Kis, M., Nagy, F., Mende, D., and Demeter, S. 2000. Short- and long-term redox regulation of photosynthetic light energy distribution and photosystem stoichiometry by acetate metabolism in the green alga, Chlamydobotrys stellata. Photosynth. Res. 65: 231-247. doi:10.1023/A:1010650532693. PMID:16228490.
36. Laroche, J., Mortainbertrand, A., and Falkowski, P.G. 1991. Light intensity-induced changes in Cab messenger-RNA and light harvesting complex-II apoprotein levels in the unicellular chlorophyte Dunaliella tertiolecta. Plant Physiol. 97: 147-153. doi:10. 1104/pp.97.1.147. PMID:16668361.
37. Masuda, T., Polle, J.E.W., and Melis, A. 2002. Biosynthesis and distribution of chlorophyll among the photosystems during recovery of the green alga Dunaliella salina from irradiance stress. Plant Physiol. 128: 603-614. doi:10.1104/pp.010595. PMID:11842163.
38. Masuda, T., Tanaka, A., and Melis, A. 2003. Chlorophyll antenna size adjustments by irradiance in Dunaliella salina involve coordinate regulation of chlorophyll a oxygenase (CAO) and lhcb gene expression. Plant Mol. Biol. 51: 757-771. doi:10.1023/A:1022545118212. PMID:12678561.
39. Matsuo, M., and Obokata, J. 2006. Remote control of photosynthetic genes by the mitochondrial respiratory chain. Plant J. 47: 873- 882. doi:10.1111/j.1365-313X.2006.02839.x. PMID:16911586.
40. Maxwell, D.P., Falk, S., Trick, C.G., and Huner, N.P.A. 1994. Growth at low-temperature mimics high-light acclimation in Chlorella vulgaris. Plant Physiol. 105: 535-543. PMID: 12232221.
41. Maxwell, D.P., Laudenbach, D.E., and Huner, N.P.A. 1995. Redox regulation of light-harvesting complex-II and cab messenger- RNA abundance in Dunaliella salina. Plant Physiol. 109: 787- 795. PMID:12228633.
42. McKim, S.M., and Durnford, D.G. 2006. Translational regulation of light-harvesting complex expression during photoacclimation to high-light in Chlamydomonas reinhardtii. Plant Physiol. Biochem. 44: 857-865. doi:10.1016/j.plaphy.2006.10.018. PMID: 17097295.
43. Mittler, R., Vanderauwera, S., Gollery, M., and Van Breusegem, F. 2004. Reactive oxygen gene network of plants. Trends Plant Sci. 9: 490-498. doi:10.1016/j.tplants.2004.08.009. PMID: 15465684.
44. Mussgnug, J.H., Wobbe, L., Elles, I., Claus, C., Hamilton, M., Fink, A., Kahmann, U., Kapazoglou, A., Mullineaux, C.W., Hippler, M., Nickelsen, J., Nixon, P.J., and Kruse, O. 2005. NAB1 is an RNA binding protein involved in the light-regulated differential expression of the light-harvesting antenna of Chlamydomonas reinhardtii. Plant Cell, 17: 3409-3421. doi:10.1105/tpc. 105.035774. PMID:16284312.
45. Niyogi, K.K. 2000. Safety valves for photosynthesis. Curr. Opin. Plant Biol. 3: 455-460. doi:10.1016/S1369-5266(00)00113-8. PMID:11074375.
46. Noctor, G., Dutilleul, C., De Paepe, R., and Foyer, C.H. 2004. Use of mitochondrial electron transport mutants to evaluate the effects of redox state on photosynthesis, stress tolerance and the integration of carbon/nitrogen metabolism. J. Exp. Bot. 55: 49- 57. doi:10.1093/jxb/erh021. PMID:14623904.
47. Nott, A., Jung, H.-S., Koussevitzky, S., and Chory, J. 2006. Plastidto- nucleus retrograde signaling. Annu. Rev. Plant Biol. 57: 739- 759. doi:10.1146/annurev.arplant.57.032905.105310. PMID: 16669780.
48. Ohresser, M., Matagne, R.F., and Loppes, R. 1997. Expression of the arylsulphatase reporter gene under the control of the nit1 promoter in Chlamydomonas reinhardtii. Curr. Genet. 31: 264- 271. doi:10.1007/s002940050204. PMID:9065390.
49. Oswald, O., Martin, T., Dominy, P.J., and Graham, I.A. 2001. Plas-tid redox state and sugars: interactive regulators of nuclearencoded photosynthetic gene expression. Proc. Natl. Acad. Sci. U.S.A. 98: 2047-2052. doi:10.1073/pnas.021449998. PMID: 11172073.
50. Pesaresi, P., Masiero, S., Eubel, H., Braun, H.P., Bhushan, S., Glaser, E., Salamini, F., and Leister, D. 2006. Nuclear photosynthetic gene expression is synergistically modulated by rates of protein synthesis in chloroplasts and mitochondria. Plant Cell, 18: 970-991. doi:10.1105/tpc.105.039073. PMID:16517761.
51. 18: 970-991. doi:10.1105/tpc.105.039073. PMID:16517761. Pfannschmidt, T., Nilsson, A., and Allen, J.F. 1999. Photosynthetic control of chloroplast gene expression. Nature (London), 397: 625-628. doi:10.1038/17624.
52. Pfannschmidt, T., Allen, J.F., and Oelmueller, R. 2001. Principles of redox control in photosynthesis gene expression. Physiol. Plant. 112: 1-9. doi:10.1034/j.1399-3054.2001.1120101.x. (Pubitemid 32402491)
53. Piippo, M., Allahverdiyeva, Y., Paakkarinen, V., Suoranta, U.-M., Battchikova, N., and Aro, E.-M. 2006. Chloroplast-mediated regulation of nuclear genes in Arabidopsis thaliana in the absence of light stress. Physiol. Genomics, 25: 142-152. doi:10. 1152/physiolgenomics.00256.2005. PMID:16403842.
54. Pursiheimo, S., Mulo, P., Rintamäki, E., and Aro, E.M. 2001. Coregulation of light-harvesting complex II phosphorylation and Lhcb mRNA accumulation in winter rye. Plant J. 26: 317-327. doi:10.1046/j.1365-313X.2001. 01033.x. PMID:11439120.
55. Puthiyaveetil, S., and Allen, J.F. 2008. Transients in chloroplast gene transcription. Biochem. Biophys. Res. Commun. 368: 871- 874. doi:10.1016/j.bbrc.2008.01.167. PMID:18275851.
56. Raghavendra, A.S., and Padmasree, K. 2003. Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci. 8: 546-553. doi:10.1016/j. tplants.2003.09.015. PMID:14607100.
57. Rodermel, S. 2001. Pathways of plastid-to-nucleus signaling. Trends Plant Sci. 6: 471-478. doi:10.1016/S1360-1385(01) 02085-4. PMID:11590066.
58. Rolland, F., Baena-Gonzalez, E., and Sheen, J. 2006. Sugar sensing and signalling in plants: conserved and novel mechanisms. Annu. Rev. Plant Biol. 57: 675-709. doi:10.1146/annurev. arplant.57.032905.105441. PMID:16669778.
59. Rossel, J.B., Wilson, I.W., and Pogson, B.J. 2002. Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol. 130: 1109-1120. doi:10.1104/pp.005595. PMID: 12427978.
60. Shao, N., Vallon, O., Dent, R., Niyogi, K.K., and Beck, C.F. 2006. Defects in the cytochrome b6/f complex prevent light-induced expression of nuclear genes involved in chlorophyll biosynthesis. Plant Physiol. 141: 1128-1137. doi:10.1104/pp.106. 081059. PMID:16679422.
61. Sheen, J. 1990. Metabolic repression of transcription in higher plants. Plant Cell, 2: 1027-1038. doi:10.1105/tpc.2.10.1027. PMID:2136626.
62. Stitt, M., and Hurry, V. 2002. A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. Curr. Opin. Plant Biol. 5: 199-206. doi:10.1016/S1369-5266(02)00258-3. PMID:11960736.
63. Strand, A. 2004. Plastid-to-nucleus signalling. Curr. Opin. Plant Biol. 7: 621-625. doi:10.1016/j.pbi.2004.09.004. PMID:15491909.
64. Strand, A., Foyer, C.H., Gustafsson, P., Gardestrom, P., and Hurry, V. 2003. Altering flux through the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance. Plant Cell Environ. 26: 523-535. doi:10.1046/j.1365- 3040.2003.00983.x.
65. Teramoto, H., Nakamori, A., Minagawa, J., and Ono, T. 2002. Light-intensity-dependent expression of LHC gene family encoding light-harvesting chlorophyll-a/b proteins of Photosystem II in Chlamydomonas reinhardtii. Plant Physiol. 130: 325-333. doi:10.1104/pp.004622. PMID:12226512.
66. Tullberg, A., Alexciev, K., Pfannschmidt, T., and Allen, J.F. 2000. Photosynthetic electron flow regulates transcription of the psaB gene in pea (Pisum sativum L.) chloroplasts through the redox state of the plastoquinone pool. Plant Cell Physiol. 41: 1045- 1054. doi:10.1093/pcp/pcd031. PMID:11100777.
67. van Lis, R., and Atteia, A. 2004. Control of mitochondrial function via photosynthetic redox signals. Photosynth. Res. 79: 133-148. doi:10.1023/B:PRES. 0000015409.14871.68. PMID:16228388.
68. Walters, R.G., and Horton, P. 1995. Acclimation of Arabidopsis thaliana to the light environment - regulation of chloroplast composition. Planta, 197: 475-481. PMID:8580761.
69. Webb, M.R., and Melis, A. 1995. Chloroplast response in Dunaliella salina to irradiance stress - effect on thylakoid membraneprotein assembly and function. Plant Physiol. 107: 885-893. PMID:12228410.
70. Wilson, K.E., and Huner, N.P.A. 2000. The role of growth rate, redox- state of the plastoquinone pool and the trans-thylakoid delta pH in photoacclimation of Chlorella vulgaris to growth irradiance and temperature. Planta, 212: 93-102. doi:10.1007/s004250000368. PMID:11219589.
71. Wilson, K.E., Król, M., and Huner, N.P.A. 2003a. Temperature-induced greening of Chlorella vulgaris. The role of cellular energy balance and zeaxanthin-dependent nonphotochemical quenching. Planta, 217: 616-627. doi:10.1007/s00425-003- 1021-8. PMID:12905022.
72. Wilson, K.E., Sieger, S.M., and Huner, N.P.A. 2003b. The temperature- dependent accumulation of Mg-protoporphyrin IX and reactive oxygen species in Chlorella vulgaris. Physiol. Plant. 119: 126-136. doi:10.1034/j.1399-3054.2003. 00153.x.