Defective etioplasts observed in variegation mutants may reveal the light-independent regulation of white/yellow sectors of Arabidopsis leaves

Journal of Integrative Plant Biology

Volumn 53, Issue 11, 2011, Pages 846-857

  Wu, Wenjuan ^a   Elsheery, Nabil ^a   Wei, Qing ^a,b   Zhang, Lingang ^a,c   Huang, Jirong ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b MAYO CLINIC   (United States)

^c OKAYAMA UNIVERSITY   (Japan)

Author keywords

Arabidopsis; Chloroplast; Chloroplast development; Etioplast; Pchlide oxidoreductase; Pchllide oxidoreductase; THF1 Psb29; Variegation

Indexed keywords

ARABIDOPSIS PROTEIN; MEMBRANE PROTEIN; OXIDOREDUCTASE; PROTOCHLOROPHYLLIDE REDUCTASE; THF1 PROTEIN, ARABIDOPSIS;

CHLOROPLAST; COLOR; GENE EXPRESSION; LEAF AREA; LIGHT EFFECT; MOLECULAR ANALYSIS; MUTATION; OBSERVATIONAL METHOD; PLANT; ULTRASTRUCTURE;

ARABIDOPSIS; ARTICLE; CHLOROPLAST; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; NORTHERN BLOTTING; PLANT LEAF; PLASTID; RADIATION EXPOSURE; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BLOTTING, NORTHERN; CHLOROPLASTS; GENE EXPRESSION REGULATION, PLANT; LIGHT; MEMBRANE PROTEINS; OXIDOREDUCTASES; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PLASTIDS;

ARABIDOPSIS;

EID: 81255205457     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/j.1744-7909.2011.01079.x     Document Type: Article

References (62)

1. Aluru MR, Bae H, Wu D, Rodermel SR (2001) The Arabidopsis immutans mutation affects plastid differentiation and the morphogenesis of white and green sectors in variegated plants. Plant Physiol. 127, 67-77.
2. Aluru M, Yu F, Fu A, Rodermel SR (2006) Arabidopsis variegation mutants: New insights into chloroplast biogenesis. J. Exp. Bot. 57, 1871-1881.
3. Armstrong GA, Runge S, Frick G, Sperling U, Apel K (1995) Identification of NADPH:protochlorophyllide oxidoreductases A and B: A branched pathway for light-dependent chlorophyll biosynthesis in Arabidopsis thaliana. Plant Physiol. 108, 1505-1517.
4. Arnon DI (1949) Copper enzymes in isolated chloroplasts: Polyphenol oxidase in Beta vulgaris. Plant Physiol. 24, 1-15.
5. Bailey S, Thompson E, Nixon PJ, Horton P, Mullineaux CW, Robinson C, Mann NH (2002) A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo. J. Biol. Chem. 277, 2006-2011.
6. Blomqvist LA, Ryberg M, Sundqvist C (2008) Proteomic analysis of highly purified prolamellar bodies reveals their significance in chloroplast development. Photosynth. Res. 96, 37-50.
7. Butler WL, Briggs WR (1966) The relation between structure and pigments during the first stages of proplastid greening. Biochim. Biophys. Acta 112, 45-53.
8. Carol P, Stevenson D, Bisanz C, Breitenbach J, Sandmann G, Mache R, Coupland G, Kuntz M (1999) Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell 11, 57-68.
9. Chen M, Choi Y, Voytas DF, Rodermel S (2000) Mutations in the Arabidopsis VAR2 locus cause leaf variegation due to the loss of a chloroplast FtsH protease. Plant J. 22, 303-313.
10. Dehesh K, Ryberg M (1985) The NADPH-protochlorophyllide oxidoreductase is the major protein constituent of prolamellar bodies in wheat (Triticum aestivum L.). Planta 164, 396-399.
11. Denev I.D, Yahubyan GT, Minkov IN, Sundqvist C (2005) Organization of protochlorophyllide oxidoreductase in prolamellar bodies isolated from etiolated carotenoid-deficient wheat leaves as revealed by fluorescence probes. Biochim. Biophys. Acta 1716, 97-103.
12. Falbel TG, Staehelin LA (1996) Partial block in the early steps of the chlorophyll synthesis pathway: A common feature of chlorophyll b-deficient mutants. Plant Physiol. 97, 311-320.
13. Franck F, Sperling U, Frick G, Pochert B, van Cleve B, Apel K, Armstrong GA (2000) Regulation of etioplast pigment-protein complexes, inner membrane architecture, and protochlorophyllide a chemical heterogeneity by light-dependent NADPH: Protochlorophyllide oxidoreductases A and B. Plant Physiol. 124, 1678-1696.
14. Goslings D, Meskauskiene R, Kim C, Lee KP, Nater M Apel K (2004) Concurrent interactions of heme and FLU with Glu tRNA reductase (HEMA1), the target of metabolic feedback inhibition of tetrapyrrole biosynthesis, in dark and light grown Arabidopsis plants. Plant J. 40, 957-967.
15. Harris N, Spence J, Oparka KJ (1994) A practical approach. In: Harris N, Oparka KJ, eds. Plant Cell Biology. Oxford University Press, UK. pp. 51-68.
16. Huang J, Takano T, Akita S (2000) Expression of α-expansin genes in young seedlings of rice (Oryza sativa L.). Planta 211, 467-473.
17. Huang J, Taylor JP, Chen JG, Uhrig JF, Schnell DJ, Nakagawa T, Korth KL, Jones AM (2006) The plastid protein THYLAKOID FORMATION1 and the plasma membrane G-protein GPA1 interact in a novel sugar-signaling mechanism in Arabidopsis. Plant Cell 18, 1226-1238.
18. Kanervo E, Singh M, Suorsa M, Paakkarinen V, Aro E, Battchikova N, Aro EM (2008) Expression of protein complexes and individual proteins upon transition of etioplasts to chloroplasts in pea (Pisum sativum). Plant Cell Physiol. 49, 396-410.
19. Kashino Y, Lauber WM, Carroll JA, Wang Q, Whitmarsh J, Satoh K, Pakrasi HB (2002) Proteomic analysis of a highly active photosystem II preparation from the cyanobacterium Synechocystis sp. PCC 6803 reveals the presence of novel polypeptides. Biochemistry 41, 8004-8012.
20. Kato Y, Miura E, Ido K, Ifuku K, Sakamoto W (2009) The variegated mutants lacking chloroplastic FtsHs are defective in D1 degradation and accumulate reactive oxygen species. Plant Physiol. 151, 1790-1801.
21. Kato Y, Miura E, Matsushima R, Sakamoto W (2007) White leaf sectors in yellow variegated2 are formed by viable cells with undifferentiated plastids. Plant Physiol. 144, 952-960.
22. Keren N, Ohkawa H, Welsh EA, Liberton M, Pakrasi HB (2005) Psb29, a conserved 22-kD protein, functions in the biogenesis of photosystem II complexes in Synechocystis and Arabidopsis. Plant Cell 17, 2768-2781.
23. Kim C, Apel K (2004) Substrate-dependent and organ-specific chloroplast protein import in planta. Plant Cell 16, 88-98.
24. Klein S, Schiff JA (1972) The correlated appearance of prolamellar bodies, protochlorophyll(ide) species, and the Shibata shift during development of bean etioplasts in the dark. Plant Physiol. 49, 619-626.
25. 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. Plant Cell 12, 419-431.
26. Liu X, Rodermel SR, Yu F (2010a) A var2 leaf variegation suppressor locus, SUPPRESSOR OF VARIEGATION3, encodes a putative chloroplast translation elongation factor that is important for chloroplast development in the cold. BMC Plant Biol. 10, 287.
27. Liu X, Yu F, Rodermel SR (2010b) Arabidopsis chloroplast FtsH, var2 and suppressors of var2 leaf variegation: A review. J. Integr. Plant Biol. 52, 750-761.
28. Liu X, Yu F, Rodermel SR (2010c) An Arabidopsis pentatricopeptide repeat protein, SUPPRESSOR OF VARIEGATION7, is required for FtsH-mediated chloroplast biogenesis. Plant Physiol. 154, 1588-1601.
29. Lopez-Juez E, Pyke KA (2005) Plastids unleashed: Their development and their integration in plant development. Int. J. Dev. Biol. 49, 557-577.
30. Mansfield SG, Briarty LG (1991) Early embryogenesis in Arabidopsis thaliana. II. The developing embryo. Can. J. Bot. 69, 461-476.
31. Mansfield SG, Briarty LG (1992) Cotyledon cell development in Arabidopsis thaliana during reserve deposition. Can. J. Bot. 70, 151-164.
32. Masuda T, Fusada N, Oosawa N, Takamatsu K, Yamamoto YY, Ohto M, Nakamura K, Goto K, Shibata D, Shirano Y, Hayashi H, Kato T, Tabata S, Shimada H, Ohta H, Takamiya K (2003) Functional analysis of isoforms of NADPH: Protochlorophyllide oxidoreductase (POR), PORB and PORC, in Arabidopsis thaliana. Plant Cell Physiol. 44, 963-974.
33. McCormac AC, Terry MJ (2002) Loss of nuclear gene expression during the phytochrome A-mediated far-red block of greening response. Plant Physiol. 130, 402-414.
34. Meskauskiene R, Apel K (2002) Interaction of FLU, a negative regulator of tetrapyrrole biosynthesis, with the glutamyl-tRNA reductase requires the tetratricopeptide repeat domain of FLU. FEBS Lett. 532, 27-30.
35. Meskauskiene R, Nater M, Goslings D, Kessler F, op den Camp R, Apel K (2001) FLU: A negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 98, 12826-12831.
36. Miura E, Kato Y, Matsushima R, Albrecht V, Laalami S, Sakamoto W (2007) The balance between protein synthesis and degradation in chloroplasts determines leaf variegation in Arabidopsis yellow variegated mutants. Plant Cell 19, 1313-1328.
37. Okegawa Y, Kobayashi Y, Shikanai T (2010) Physiological links among alternative electron transport pathways that reduce and oxidize plastoquinone in Arabidopsis. Plant J. 63, 458-468.
38. Park H, Kreunen SS, Cuttriss AJ, DellaPenna D, Pogson BJ (2002) Identification of the carotenoid isomerase provides insight into carotenoid biosynthesis, prolamellar body formation, and photomorphogenesis. Plant Cell 14, 321-332.
39. Pogson BJ, Albrecht V (2011) Genetic dissection of chloroplast biogenesis and development: An overview. Plant Physiol. 155, 1545-1551.
40. Reiter RS, Coomber SA, Bourett T M, Bartley GE, Scolnik PA (1994) Control of leaf and chloroplast development by the Arabidopsis gene pale cress. Plant Cell 6, 1253-1264.
41. Rosso D, Bode R, Li W, Krol M, Saccon D, Wang S, Schillaci LA, Rodermel SR, Maxwell DP, Hüner NP (2009) Photosynthetic redox imbalance governs leaf sectoring in the Arabidopsis thaliana variegation mutants immutans, spotty, var1, and var2. Plant cell 21, 3473-3492.
42. Ruppel NJ, Logsdon CA, Whippo CW, Inoue K, Hangarter RP (2011) A mutation in Arabidopsis seedling plastid development1 affects plastid differentiation in embryo-derived tissues during seedling growth. Plant Physiol. 155, 342-353.
43. Sakamoto W (2006) Protein degradation machineries in plastids. Annu. Rev. Plant Biol. 57, 559-621.
44. Sakamoto W, Uno Y, Zhang Q, Miura E, Kato Y, Sodmergen (2009) Arrested differentiation of proplastids into chloroplasts in variegated leaves characterized by plastid ultrastructure and nucleoid morphology. Plant Cell Physiol. 50, 2069-2083.
45. Sakamoto W, Miyagishima SY, Jarvis P (2008) Cloroplast biogenesis: Control of plastid development, protein import, division and inheritance. In: The Arabidopsis Book, Somerville CR and Meyerowitz EM eds. American Society of Plant Physiologists. Rockvelle, MD, USA doi:,.
46. Sakamoto W, Zaltsman A, Adam Z, Takahashi Y (2003) Coordinated regulation and complex formation of YELLOWVARIEGATED1 and YELLOWVARIEGATED2, chloroplastic FtsH metalloproteases involved in the repair cycle of photosystem II in Arabidopsis thylakoid membranes. Plant Cell 15, 2843-2855.
47. Solymosi K, Schoefs B (2010) Etioplast and etio-chloroplast formation under natural conditions: The dark side of chlorophyll biosynthesis in angiosperms. Photosynth. Res. 105, 143-166.
48. Tejos RI, Mercado AV, Meisel LA (2010) Analysis of chlorophyll fluorescence reveals stage specific patterns of chloroplast-containing cells during Arabidopsis embryogenesis. Biol. Res. 43, 99-111.
49. Wang Q, Sullivan RW, Kight A, Henry RL, Huang J, Jones AM, Korth KL (2004) Deletion of the chloroplast-localized thylakoid formation1 gene product in Arabidopsis leads to deficient thylakoid formation and variegated leaves. Plant Physiol. 136, 3594-3604.
50. Waters MT, Moylan EC, Langdale JA (2008) GLK transcription factors regulate chloroplast development in a cell-autonomous manner. Plant J. 56, 432-444.
51. Waters MT, Langdale JA (2009) The making of a chloroplast. EMBO J. 28, 2861-2873.
52. Wetzel CM, Jiang C, Meehan LJ, Voytas DF, Rodermel SR (1994) Nuclear-organelle interactions: The immutans variegation mutant of Arabidopsis is plastid autonomous and impaired in carotenoid biosynthesis. Plant J. 6, 161-175.
53. Wu D, Wright DA, Wetzel C, Voytas DF, Rodermel SR (1999) The IMMUTANS variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis. Plant Cell 11, 43-55.
54. Yu F, Park S, Rodermel SR (2004) The Arabidopsis FtsH metalloprotease gene family: Interchangeability of subunits in chloroplast oligomeric complexes. Plant J. 37, 864-876.
55. Yu F, Park S, Rodermel SR (2005) Functional redundancy of AtFtsH metalloproteases in thylakoid membrane complexes. Plant Physiol. 138, 1957-1966.
56. Yu F, Fu A, Aluru M, Park S, Xu Y, Liu H, Liu X, Foudree A, Nambogga M, Rodermel SR (2007) Variegation mutants and mechanisms of chloroplast biogenesis. Plant Cell Environ. 30, 350-365.
57. Yu F, Liu X, Alsheikh M, Park S, Rodermel S (2008) Mutations in SUPPRESSOR OF VARIEGATION1, a factor required for normal chloroplast translation, suppress var2-mediated leaf variegation in Arabidopsis. Plant Cell 20, 1786-1804.
58. Yu F, Park SS, Liu X, Foudree A, Fu A, Powikrowska M, Khrouchtchova A, Jensen PK, Kriger JN, Gray GR, Rodermel SR (2011) Suppressor of variations 4, a new var2 suppressor locus, encodes a pioneer protein that is required for chloroplast biogenesis. Mol. Plant 4, 229-240.
59. Zaltsman A, Ori N, Adam Z (2005a) Two types of FtsH protease subunits are required for chloroplast biogenesis and Photosystem II repair in Arabidopsis. Plant Cell 17, 2782-2790.
60. Zaltsman A, Feder A, Adam Z (2005b) Developmental and light effects on the accumulation of FtsH protease in Arabidopsis chloroplasts: Implications for thylakoid formation and photosystem II maintenance. Plant J. 42, 609-617.
61. Zhang L, Wei Q, Wu W, Cheng Y, Hu G, Hu F, Sun Y, Zhu Y, Sakamoto W, Huang J (2009) Activation of the heterotrimeric G protein α-subunit GPA1 suppresses the ftsh-mediated inhibition of chloroplast development in Arabidopsis. Plant J. 58, 1041-1053.
62. Zhang D, Kato Y, Zhang L, Fujimoto M, Tsutsumi N, Sodmergen, Sakamoto W (2011) The FtsH protease heterocomplex in Arabidopsis: Dispensability of Type-B protease activity for proper chloroplast development. Plant Cell 22, 3710-3725.