Loss of chloroplast protease SPPA function alters high light acclimation processes in Arabidopsis thaliana L. (Heynh.)

Journal of Experimental Botany

Volumn 60, Issue 6, 2009, Pages 1715-1727

  Wetzel, Carolyn M ^a   Harmacek, Laura D ^a   Yuan, Lee H ^a   Wopereis, Judith L M ^a   Chubb, Rhiannon ^a   Turini, Paula ^a  

^a SMITH COLLEGE   (United States)

Author keywords

Anthocyanin; Chloroplast; High light acclimation; NPQ; Protease; SPPA

Indexed keywords

ANTHOCYANIN; ARABIDOPSIS PROTEIN; CHLOROPHYLL; SERINE PROTEINASE; SPPA PROTEIN, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; CHLOROPLAST; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; LIGHT; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; RADIATION EXPOSURE;

ANTHOCYANINS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHLOROPHYLL; CHLOROPLASTS; LIGHT; MUTAGENESIS, INSERTIONAL; PHOTOSYNTHESIS; SERINE ENDOPEPTIDASES;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 65349094034     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erp051     Document Type: Article

References (67)

1. Adam Z, Clarke AK. 2002. Cutting edge of chloroplast proteolysis. Trends in Plant Science 7, 451-456.
2. Adam Z, Rudella A, van Wijk KJ. 2006. Recent advances in the study of Clp, FtsH and other proteases located in chloroplasts. Current Opinion in Plant Biology 9, 234-240.
3. Adamska I. 2001. The Elip family of stress proteins in the thylakoid membranes of Pro- and Eukaryota. In: Aro E-M, Andersson B, eds. Regulation of photosynthesis. Dordrecht: Kluwer Academic Publishers, 487-505.
4. Adamska I, Kloppstech K, Ohad I. 1993. Early light-inducible protein in pea is stable during light stress but is degraded during recovery at low light intensity. Journal of Biological Chemistry 268, 5438-5444.
5. Adamska I, Lindahl M, Roobal-Bóza M, Andersson B. 1996. Degradation of the light-stress protein is mediated by an ATP-independent, serine-type protease under low-light conditions. European Journal of Biochemistry 236, 591-599.
6. Alonso JM, Stepanova AN, Leisse TJ, et al. 2003. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653-657.
7. Anderson MD, Prasad TK, Stewart CR. 1995. Changes in isozyme profiles of catalase, peroxidase, and glutathione reductase during acclimation to chilling in mesocotyls of maize seedlings. Plant Physiology 109, 1247-1257.
8. Arnon D. 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1-15.
9. Aro E-M, Andersson B, (eds). 2001. Regulation of photosynthesis. Dordrecht: Kluwer Academic Publishers.
10. Aro E-M, Virgin I, Andersson B. 1993. Photoinhibition of photosystem II: inactivation, protein damage and turnover. Biochimica et Biophysica Acta 1143, 113-134.
11. Bailey S, Walters RG, Jansson S. 2001. Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213, 794-801.
12. Ballottari M, Dall'Osto L, Morosinotto T, Bassi R. 2007. Contrasting behaviour of higher plant photosystem I and II antenna systems during acclimation. Journal of Biological Chemistry 282, 8947-8958.
13. Barber J, Andersson B. 1992. Too much of a good thing: light can be bad for photosynthesis. Trends in Biochemical Sciences 17, 61-66.
14. Bhalerao R, Keskitalo J, Sterky F, et al. 2003. Gene expression in autumn leaves. Plant Physiology 131, 430-442.
15. Binyamin L, Falah M, Portnoy V, Soudry E, Gepstein S. 2001. The early light-induced protein is also produced during leaf senescence of Nicotiana tabacum. Planta 212, 591-597.
16. Casazza AP, Rossini S, Rosso MG, Soave C. 2005. Mutational and expression analysis of ELIP1 and ELIP2 in Arabidopsis thaliana. Plant Molecular Biology 58, 41-51.
17. Casazza AP, Tarantino D, Soave C. 2001. Preparation and functional characterization of thylakoids from Arabidopsis thaliana. Photosynthesis Research 68, 175-180.
18. Close DC, Beadle CL. 2003. The ecophysiology of foliar anthocyanin. The Botanical Review 69, 149-161.
19. Constan D, Froehlich JE, Rangarajan S, Keegstra K. 2004. A stromal Hsp100 protein is required for normal chloroplast development and function in Arabidopsis. Plant Physiology 136, 3605-3615.
20. Dall'Osta L, Cazzaniga S, North H, Marion-Poll A, Bassi R. 2007. The Arabidopsis aba4-1 mutant reveals a specific function for neoxanthin in protection against photooxidative stress. The Plant Cell 19, 1048-1064.
21. Esteban R, Fernández-Marín B, Becerril JM, García-Plazaola JI. 2008. Photoprotective implications of leaf variegation in E. dens-canis L. and P. officinalis L. Journal of Plant Physiology 165, 1255-1263.
22. Finucane MM, Samet JH, Horton NJ. 2007. Translational methods in biostatistics: linear mixed effect regression models of alcohol consumption and HIV disease progression over time. Epidemiologic Perspectives and Innovations 4, doi:10.1186/1742-5573-4-8.
23. Fitzmaurice GM, Laird NM, Ware JH. 2004. Applied longitudinal analysis. New York: John Wiley and Sons.
24. Friso G, Ytterberg AJ, Giacomelli L, Peltier JB, Rudella A, Sun Q, van Wijk KJ. 2004. In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts; new proteins, functions and a plastid proteome database. The Plant Cell 16, 478-499.
25. Giacomelli L, Rudella A, van Wijk KJ. 2006. High light response of the thylakoid proteome in Arabidopsis wild type and the ascorbate-deficient mutant vtc2-2. A comparative proteomics study. Plant Physiology 141, 685-701.
26. Giusti MM, Wrolstad RE. 2000. Characterization and measurement of anthocyanins by UV-visible spectroscopy. In: Wrolstad RE, Acree TE, Decker EA, Penner MH, Reid DS, Schwartz SJ, Shoemaker CF, Smith D, Sporns P, eds. Current protocols in food analytical chemistry. New York: John Wiley and SonsUnit F1.2.
27. Golan T, Müller-Moule P, Niyogi KK. 2006. Photoprotection mutants of Arabidopsis thaliana acclimate to high light by increasing photosynthesis and specific antioxidants. Plant, Cell, and Environment 29, 879-887.
28. Gray GR, Savitch LV, Ivanov AG, Huner NPA. 1996. Photosystem II excitation pressure and development of resistance to photoinhibition. II. Adjustment of photosynthetic capacity in winter wheat and winter rye. Plant Physiology 110, 61-71.
29. Harari-Steinberg O, Ohad I, Chamovitz DA. 2001. Dissection of the light signal transduction pathways regulating the two Early Light-Induced Protein genes in Arabidopsis. Plant Physiology 127, 986-997.
30. Haußühl K, Andersson B, Adamska I. 2001. A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II. EMBO Journal 20, 713-722.
31. Havaux M, Kloppstech K. 2001. The protective functions of carotenoids and flavonoid pigments against excess visible radiation at chilling temperature investigated in Arabidopsis npq and tt mutants. Planta 213, 953-966.
32. Havaux M, Niyogi KK. 1999. The violaxanthin cycle protects plants from photooxidative stress by more than one mechanism. Proceedings of the National Academy of Sciences, USA 96, 8762-8767.
33. Havaux M, Eymery F, Porifirova S, Rey P, Dörmann P. 2005. Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. The Plant Cell 17, 3451-3469.
34. Heddad M, Norén H, Reiser V, Dunaeva M, Andersson B, Adamska I. 2006. Differential expression and localization of Early Light Inducible Proteins in Arabidopsis. Plant Physiology 142, 75-87.
35. Hughes NM, Morley CB, Smith WK. 2007. Coordination of anthocyanin decline and photosynthetic maturation in juvenile leaves of three deciduous tree species. New Phytologist 175, 675-685.
36. Huner NPA, Öquist G, Sarhan F. 1998. Energy balance and acclimation to light and cold. Trends in Plant Science 3, 224-230.
37. Hutin C, Nussaume L, Moise N, Moya I, Kloppstech K, Havaux M. 2003. Early light-induced proteins protect Arabidopsis from photooxidative stress. Proceedings of the National Academy of Sciences, USA 100, 4921-4926.
38. Inoue K, Baldwin AJ, Shipman RL, Matsui K, Theg SM, Ohme-Takagi M. 2005. Complete maturation of the plastid protein translocation channel requires a type I signal peptidase. Journal of Biological Chemistry 171, 425-430.
39. Ivanov AG, Sane PV, Krol M, Gray GR, Balseris A, Savitch LV, Öquist G, Huner NPA. 2006. Acclimation to temperature and irradiance modulates PSII charge recombination. FEBS Letters 580, 2797-2802.
40. Jackowski G, Olkiewicz P, Zelisko A. 2003. The acclimative response of the main light-harvesting chlorophyll a/b protein complex of photosystem II (LHCII) to elevated irradiances at the level of trimeric subunits. Journal of Photochemistry and Photobiology B 70, 163-170.
41. Kuroda H, Maliga P. 2003. The plastid clpP1 protease gene is essential for plant development. Nature 425, 86-89.
42. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
43. Lensch M, Hermann RG, Sokolenko A. 2001. Identification and characterization of SppA, a novel light-inducible chloroplast protease complex associated with thylakoid membranes. Journal of Biological Chemistry 276, 33645-33651.
44. Lindahl M, Spetea C, Hundal T, Oppenheim AB, Adam Z, Andersson B. 2000. The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein. The Plant Cell 12, 419-431.
45. Logan BA, Kornyeyev D, Hardison J, Holaday AS. 2006. The role of antioxidant enzymes in photoprotection. Photosynthesis Research 88, 119-132.
46. 4 differentiation for chloroplast membrane proteomes in maize mesophyll and bundle sheath cells. Molecular and Cellular Proteomics 7, 1609-1638.
47. Maxwell DP, Falk S, Huner NPA. 1995. Photosystem II excitation pressure and development of resistance to photoinhibition. I. Light-harvesting complex II abundance and zeaxanthin content in Chlorella vulgaris. Plant Physiology 107, 687-694.
48. Maxwell K, Johnson GN. 2000. Chlorophyll fluorescence: a practical guide. Journal of Experimental Botany 51, 659-668.
49. Merzlyak MN, Melø TB, Naqvi KR. 2008. Effect of anthocyanins, carotenoids, and flavonols on chlorophyll fluorescence excitation spectra in apple fruit: signature analysis, assessment, modeling, and relevance to photoprotection. Journal of Experimental Botany 59, 349-359.
50. Mishra RK, Mishra NP, Kambourakis S, Orfanopoulos M, Ghanotakis DF. 1996. Generation and trapping of singlet oxygen during strong illumination of a photosystem II core complex. Plant Science 115, 151-155.
51. Montané M-H, Kloppstech K. 2000. The family of light-harvesting-related proteins (LHCs, ELIPs, HLIPs): was the harvesting of light their primary function? Gene 258, 1-8.
52. Müller P, Li X-P, Niyogi KK. 2001. Non-photochemical quenching. A response to excess light energy. Plant Physiology 125, 1558-1566.
53. Oelmüller R. 1989. Photooxidative destruction of chloroplasts and its effect on nuclear gene expression and extraplastidic enzyme levels. Photochemistry and Photobiology 49, 229-239.
54. Ostersetzer O, Kato Y, Adam Z, Sakamoto W. 2007. Multiple intracellular locations of Lon protease in Arabidopsis: rvidence for the localization of AtLon4 to chloroplasts. Plant and Cell Physiology 48, 881-885.
55. Pojidaeva E, Zinchenko V, Shestakov SV, Sokolenko A. 2004. Involvement of the SppA1 peptidase in acclimation to saturating light intensities in Synechocystis sp. strain PCC 6803. Journal of Bacterioogy 186, 3991-3999.
56. Porra RJ, Thompson WA, Kriedemann PE. 1989. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta 975, 384-394.
57. Prasil O, Adir N, Ohad I. 1992. Dynamics of photosystem II: mechanism of photoinhibition and recovery process. Topics in Photosynthesis 11, 295-348.
58. Rossini S, Casazza AP, Engelmann ECM, Havaux M, Jennings RC, Soave C. 2006. Suppression of both ELIP1 and ELIP2 in Arabidopsis thaliana does not affect tolerance to photoinhibition and photooxidative stress. Plant Physiology 141, 1264-1273.
59. Rosso MG, Li Y, Strizhov N, Reiss B, Dekker K, Weisshaar B. 2003. An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Molecular Biology 53, 247-259.
60. Rudella A, Friso G, Alonso JM, Ecker JR, van Wijk KJ. 2006. Down-regulation of ClpR2 leads to reduced accumulation of the ClpPRS protease complex and defects in chloroplast biogenesis in Arabidopsis. The Plant Cell 18, 1704-1721.
61. Sakamoto W. 2006. Protein degradation machineries in plastids. Annual Review of Plant Biology 57, 599-621.
62. Shikanai T, Shimizu K, Ueda K, Nishimura Y, Kuroiwa T, Hashimoto T. 2001. The chloroplast clpP gene, encoding a proteolytic subunit of ATP-dependent protease, is indispensable for chloroplast development in tobacco. Plant and Cell Physiology 42, 264-273.
63. Sokolenko A. 2005. SppA peptidases: family diversity from heterotrophic bacteria to photoautotrophic eukaryotes. Physiologia Plantarum 123, 391-398.
64. Tanaka R, Tanaka A. 2005. Effects of chlorophyllide a oxygenase overexpression on light acclimation in Arabidopsis thaliana. Photosynthesis Research 85, 327-340.
65. Tzvetkova-Chevolleau T, Franck F, Alawady AE, Dall'Osto L, Carrière F, Bassi R, Grimm B, Nussaume L, Havaux M. 2007. The light stress-induced protein ELIP2 is a regulator of chlorophyll synthesis in Arabidopsis thaliana. The Plant Journal 50, 795-809.
66. Vanderauwera S, Zimmermann P, Rombauts S, Vandenabeele S, Langebartels C, Gruissem W, Inzé D, van Breusegem F. 2005. Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiology 139, 806-821.
67. Yang D-H, Webster J, Adam Z, Lindahl M, Andersson B. 1998. Induction of acclimative proteolysis of the light-harvesting chlorophyll a/b protein of photosystem II in response to elevated light intensities. Plant Physiology 118, 827-834.