Shedding light on the chloroplast as a remote control of nuclear gene expression

Plant Signaling and Behavior

Volumn 9, Issue 11, 2014, Pages

  Godoy Herz, Micaela A ^a   Kornblihtt, Alberto R ^a   Barta, Andrea ^b   Kalyna, Maria ^c   Petrillo, Ezequiel ^b  

^a INSTITUTO DE FISIOLOGÍA   (Argentina)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

Alternative splicing; Chloroplast; Light; Retrograde signal; RNA

Indexed keywords

VISUAL PROTEINS AND PIGMENTS;

CELL NUCLEUS; CHLOROPLAST; GENE EXPRESSION REGULATION; GENETICS; LIGHT; METABOLISM; PHOTOTRANSDUCTION; RADIATION RESPONSE;

CELL NUCLEUS; CHLOROPLASTS; GENE EXPRESSION REGULATION, PLANT; LIGHT; LIGHT SIGNAL TRANSDUCTION; PHOTORECEPTORS, PLANT;

EID: 84922311511     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/15592324.2014.976150     Document Type: Article

References (42)

1. Jiao Y, Lau OS, Deng XW. Light-regulated transcriptional networks in higher plants. Nat Rev Gen 2007; 8:217-30; http://dx.doi.org/10.1038/nrg2049.
2. Fisher AJ, Franklin KA. Chromatin remodelling in plant light signalling. Physiol Plant 2011; 142:305-13; PMID:21457270; http://dx.doi.org/10.1111/j.1399- 3054.2011.01476.x.
3. Casal JJ, Yanovsky MJ. Regulation of gene expression by light. Int J Dev Biol 2005; 49:501-11; PMID:16096960; http://dx.doi.org/10.1387/ ijdb.051973jc.
4. Leivar P, Quail PH. PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci 2011; 16:19-28; PMID:20833098; http://dx.doi.org/10.1016/j. tplants.2010.08.003.
5. Liu MJ, Wu SH, Chen HM, Wu SH. Widespread translational control contributes to the regulation of Arabidopsis photomorphogenesis. Mol Syst Biol 2012; 8:566; PMID:22252389; http://dx.doi.org/10.1038/ msb.2011.97.
6. Chico JM, Fern_andez-Barbero G, Chini A, Fern_andez- Calvo P, D_ıez-D_ıaz M, Solano R. Repression of jasmonate- dependent defenses by shade involves differential regulation of protein stability of MYC transcription factors and their JAZ repressors in Arabidopsis. Plant Cell 2014; 26:1967–1980; PMID:24824488; http:// dx.doi.org/10.1105/tpc.114.125047.
7. Marquez Y, Brown JW, Simpson C, Barta A, Kalyna M. Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Res 2012; 22:1184-95; PMID:22391557; http://dx.doi.org/10.1101/gr.134106.111.
8. Wu HP, Su YS, Chen HC, Chen YR, Wu CC, Lin WD, Tu SL. Genome-wide analysis of light-regulated alternative splicing mediated by photoreceptors in Physcomitrella patens. Genome Biol 2014; 15:R10; PMID:24398233; http://dx.doi.org/10.1186/gb-2014-15-1-r10.
9. Petrillo E, Godoy Herz MA, Fuchs A, Reifer D, Fuller J, Yanovsky MJ, Simpson C, Brown JW, Barta A, Kalyna M, et al. A chloroplast retrograde signal regulates nuclear alternative splicing. Science 2014; 344:427-30;PMID:24763593; http://dx.doi.org/10.1126/science.1250322.
10. Wu SH. Gene expression regulation in photomorphogenesis from the perspective of the central dogma. Annu Rev Plant Biol 2014; 65:311-33; PMID:24779996; http://dx.doi.org/10.1146/annurevarplant- 050213-040337.
11. Kuno N, Muramatsu T, Hamazato F, Furuya M. Identification by large-scale screening of phytochrome-regulated genes in etiolated seedlings of Arabidopsis using a fluorescent differential display technique. Plant Phys 2000; 122:15-24; http://dx.doi.org/10.1104/pp.122.1.15.
12. Fankhauser C, Chory, J. Light control of plant development. Annu Rev Cell Dev Biol 1997; 13:203-29; PMID:9442873; http://dx.doi.org/10.1146/annurev. cellbio.13.1.203.
13. Li J, Terzaghi W, Deng XW. Genomic basis for light control of plant development. Protein Cell J 2012; 3:106-16; http://dx.doi.org/10.1007/s13238-012-2016-7.
14. Jiao Y, Ma L, Strickland E, Deng XW. Conservation and divergence of light-regulated genome expression patterns during seedling development in rice and Arabidopsis. Plant Cell 2005; 17:3239-56; PMID:16284311; http:// dx.doi.org/10.1105/tpc.105.035840.
15. Ma L, Li J, Qu L, Hager J, Chen Z, Zhao H, et al. Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell 2001; 13:2589-607; PMID:11752374; http:// dx.doi.org/10.1105/tpc.13.12.2589.
16. Van Zanten M, Tessadori F, McLoughlin F, Smith R, Millenaar FF, van Driel R, Voesenek LA, Peeters AJ, Fransz P. Photoreceptors CRYTOCHROME2 and phytochrome B control chromatin compaction in Arabidopsis. Plant Physiol 2010; 154:1686-96; PMID:20935177; http://dx.doi.org/10.1104/ pp.110.164616.
17. Liu X, Chen C-YY, Wang K-CC, Luo M, Tai R, Yuan L, Zhao M, Yang S, Tian G, Cui Y, et al. PHYTOCHROME INTERACTING FACTOR3 associates with the histone deacetylase HDA15 in repression of chlorophyll biosynthesis and photosynthesis in etiolated Arabidopsis seedlings. Plant Cell 2013; 25:1258-73; PMID:23548744; http://dx.doi.org/10.1105/ tpc.113.109710.
18. Szechy_nska-Hebda M, Karpi_nski S. Light intensitydependent retrograde signalling in higher plants. J Plant Phys 2013; 170:1501-16; http://dx.doi.org/10.1016/j.jplph.2013.06.005
19. Blanco NE, Guinea-D_ıaz M, Whelan J, Strand A. Interaction between plastid and mitochondrial retrograde signalling pathways during changes to plastid redox status. Phil Trans R Soc B Biol Sci 2014; 369:20130231; http://dx.doi.org/10.1098/rstb.2013.0231.
20. Jung HS, Chory J. Signaling between chloroplasts and the nucleus: can a systems biology approach bring clarity to a complex and highly regulated pathway? Plant Physiol 2010; 152:453-9; PMID:19933385; http://dx. doi.org/10.1104/pp.109.149070.
21. Pfannschmidt T. Plastidial retrograde signalling-a true “plastid factor” or just metabolite signatures? Trends Plant Sci 2010; 15:427-35; PMID:20580596; http://dx.doi.org/10.1016/j.tplants.2010.05.009.
22. Susek RE, Ausubel FM, Chory J. Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 1993; 74:787-99; PMID:7690685; http://dx.doi. org/10.1016/0092-8674(93)90459-4.
23. Strand A. Plastid-to-nucleus signalling. Curr Opin Plant Biol 2004; 7:621-5; PMID:15491909; http://dx. doi.org/10.1016/j.pbi.2004.09.004.
24. Ankele E, Kindgren P, Pesquet E, Strand A. In vivo visualization of Mg-protoporphyrin IX, a coordinator of photosynthetic gene expression in the nucleus and the chloroplast. Plant Cell 2007; 19:1964-79; PMID:17586657; http://dx.doi.org/10.1105/tpc.106. 048744.
25. Moulin M, McCormac AC, Terry MJ, Smith AG. Tetrapyrrole profiling in Arabidopsis seedlings reveals that retrograde plastid nuclear signaling is not due to Mgprotoporphyrin IX accumulation. Proc Natl Acad Sci USA 2008; 105:15178-83; PMID:18818314; http://dx.doi.org/10.1073/pnas.0803054105.
26. Leister D. Retrograde signaling in plants: from simple to complex scenarios. Front Plant Sci 2012; 3:135; PMID:22723802.
27. Kim C, Apel K. 1O2-mediated and EXECUTERdependent retrograde plastid-to-nucleus signaling in norflurazon-treated seedlings of Arabidopsis thaliana. Mol Plant 2013; 6:1580-91;PMID:23376773; http:// dx.doi.org/10.1093/mp/sst020.
28. Estavillo GM, Crisp PA, Pornsiriwong W, Wirtz M, Collinge D, Carrie C, Giraud E, Whelan J, David P, Javot H, et al. Evidence for a SAL1-PAP chloroplast retrograde pathway that functions in drought and high light signaling in Arabidopsis. Plant Cell 2011; 23:3992-4012; PMID:22128124; http://dx.doi.org/ 10.1105/tpc.111.091033.
29. Sun X, Feng P, Xu X, Guo H, Ma J, Chi W, Lin R, Lu C, Zhang L. A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus. Nat Commun 2011; 2:477; PMID:21934661; http://dx. doi.org/10.1038/ncomms1486.
30. Karpinski S, Escobar C, Karpinska B, Creissen G, Mullineaux PM. Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in Arabidopsis during excess light stress. Plant Cell 1997; 9:627-40; PMID:9144965; http://dx.doi.org/10.1105/ tpc.9.4.627.
31. Fey V, Wagner R, Brautigam K, Pfannschmidt T. Photosynthetic redox control of nuclear gene expression. J Exp Bot 2005; 56:1491-8; PMID:15863445; http://dx.doi.org/10.1093/jxb/eri180.
32. Filichkin SA, Priest HD, Givan SA, Shen R, Bryant DW, Fox SE, et al. Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res 2010; 20:45-58; PMID:19858364; http://dx.doi.org/ 10.1101/gr.093302.109.
33. Chang CY, Lin WD, Tu SL. Genome-wide analysis of heat-sensitive alternative splicing in Physcomitrella patens. Plant Physiol 2014; 165:826-40; PMID:24777346; http://dx.doi.org/10.1104/pp.113.230540.
34. Wang H, You C, Chang F, Wang Y, Wang L, Qi J, et al. Alternative splicing during Arabidopsis flower development results in constitutive and stage-regulated isoforms. Front Gene 2014; 5:25.
35. Drechsel G, Kahles A, Kesarwani AK, Stauffer E, Behr J, Drewe P, et al. Nonsense-mediated decay of alternative precursor mRNA splicing variants is a major determinant of the Arabidopsis steady state transcriptome. Plant Cell 2013; 25:3726-42; PMID:24163313; http://dx.doi.org/10.1105/tpc.113.115485.
36. Kalyna M, Simpson CG, Syed NH, Lewandowska D, Marquez Y, Kusenda B, Marshall J, Fuller J, Cardle L, McNicol J, et al. Alternative splicing and nonsensemediated decay modulate expression of important regulatory genes in Arabidopsis. Nucl Acids Res 2012; 40:2454-69; PMID:22127866; http://dx.doi.org/ 10.1093/nar/gkr932.
37. Kalyna M, Lopato S, Voronin V, Barta A. Evolutionary conservation and regulation of particular alternative splicing events in plant SR proteins. Nucl Acids Res 2006; 34:4395-405; PMID:16936312; http://dx.doi. org/10.1093/nar/gkl570.
38. Kim SH, Koroleva OA, Lewandowska D, Pendle AF, Clark GP, Simpson CG, Shaw PJ, Brown JW. Aberrant mRNA transcripts and the nonsense-mediated decay proteins UPF2 and UPF3 are enriched in the Arabidopsis nucleolus. Plant Cell 2009; 21:2045-57; PMID:19602621; http://dx.doi.org/10.1105/tpc.109. 067736.
39. Jung H-S, Mockler T. A new alternative in plant retrograde signaling. Genome Biol 2014; 15:117; PMID:25001637; http://dx.doi.org/10.1186/gb4178.
40. Pfalz J, Liebers M, Hirth M, Grubler B, Holtzegel U, Schroter Y, Dietzel L, Pfannschmidt T. Environmental control of plant nuclear gene expression by chloroplast redox signals. Front Plant Sci 2012; 3:257; PMID:23181068; http://dx.doi.org/10.3389/ fpls.2012.00257.
41. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P. Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 1999; 284(5414):654-657; PMID:10213690; http://dx.doi.org/10.1126/science.284.5414.654.
42. Szechy_nska-Hebda M, Kruk J, G_orecka M, Karpi_nska B, Karpi_nski S. Evidence for light wavelength-specific photoelectrophysiological signaling and memory of excess light episodes in Arabidopsis. Plant Cell 2010; 22:2201-18; PMID:20639446; http://dx.doi.org/10.1105/tpc.109.069302 www.