Coordinating light responses between the nucleus and the chloroplast, a role for plant cryptochromes and phytochromes.
Journal
Physiologia plantarum
ISSN: 1399-3054
Titre abrégé: Physiol Plant
Pays: Denmark
ID NLM: 1256322
Informations de publication
Date de publication:
Aug 2020
Aug 2020
Historique:
received:
23
01
2020
revised:
04
06
2020
accepted:
05
06
2020
pubmed:
11
6
2020
medline:
25
9
2020
entrez:
11
6
2020
Statut:
ppublish
Résumé
To promote photomorphogenesis, including plastid development and metabolism, the phytochrome (phy) and the cryptochrome (cry) photoreceptors orchestrate genome-wide changes in gene expression in response to Red (R)- and Blue (B)-light cues. While phys and crys have a clear role in modulating photosynthesis, their role in the coordination of the nuclear genome and the plastome, essential for functional chloroplasts, remains underexplored. Using publicly available genome datasets for WT and phyABCDE or cry1cry2 Arabidopsis seedlings, grown, respectively, under R- or B-light, we bioinformatically analyzed the influence of light inputs and photoreceptors in the control of nuclear genes with a function in the chloroplast, and evaluated the role of phyB in the modulation of plastome-encoded genes. We show gene co-induction by R-phys and B-crys for genes with a chloroplastic function, and also apparent photoreceptor-driven preferential responses. Evidence from phyB in Arabidopsis together with published evidence from CRY2 in tomato also supports the participation of both photoreceptor families in the global modulation of the plastome genes. To begin addressing how these light-sensors orchestrate changes in an organellar genome, we evaluated their effect over genes with potential functions in plastid gene-expression regulation based on their TAIR annotation. Results indicate that both crys and phys modulate 'plastome-regulatory genes' with enrichment in the contribution of crys to all processes and of phys to post-transcription and transcription. Furthermore, we identified a new role for HY5 as a relevant light-signaling component in photoreceptor-based anterograde signaling leading to plastome gene regulation.
Substances chimiques
Arabidopsis Proteins
0
Cryptochromes
0
Phytochrome
11121-56-5
Phytochrome B
136250-22-1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
515-528Subventions
Organisme : Lancaster University
Organisme : Royal Society
ID : RG150711
Informations de copyright
© 2020 The Authors. Physiologia Plantarum published by John Wiley & Sons Ltd on behalf of Scandinavian Plant Physiology Society.
Références
Barkan A (2011) Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold. Plant Physiol 155: 1520-1532
Barneche F, Winter V, Crececoeur M, Rochaix J (2006) ATAB2 is a novel factor in the signaling pathway of light-controlled synthesis of photosystem proteins. EMBO J 25: 5907-5918
Belbin FE, Noordally ZB, Wetherill SJ, Atkins KA, Franklin KA, Dodd AN (2017) Integration of light and circadian signals that regulate chloroplast transcription by a nuclear-encoded sigma factor. New Phytol 213: 727-738
Berg M, Rogers R, Muralla R, Meinke D (2005) Requirement of aminoacyl-tRNA synthetases for gametogenesis and embryo development in Arabidopsis. Plant J 44: 866-878
Berry JO, Yerramsetty P, Zielinkski AM, Mure CM (2013) Photosynthetic gene expression in higher plants. Photosynth Res 117: 91-120
Chang BHW and Tian W (2015). GSA-Lightning: Ultra Fast Permutation-based Gene Set Analysis. Bioinformatics. https://doi.org/10.1093/bioinformatics/btw349
Chang BHW (2020). GSALightning: Fast Permutation-based Gene Set Analysis. R package version 1.16.0. https://github.com/billyhw/GSALightning
Borner T, Aleynikova AY, Zubo YO, Kusnetsov V (2015) Chloroplast RNA polymerases: role in chloroplast biogenesis. Biochimica et Biophysica Acta (BBA) Bioenergetics 1847: 761-769
Chang CJ, Li Y, Chen L (2008) LFZ1, a HY5-regulated transcriptional factor, functions in Arabidopsis de-etiolation. Plant J 54: 205-219
Chen M, Chory J (2011) Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol 21: 664-671
Chen M, Galvao RM, Li M, Burger B, Bugea J, Bolado J, Chory J (2010) HEMERA/pTAC12 initiates photomorphogenesis by phytochromes. Cell 141: 1230-1240
Chotewutmontri P, Barkan A (2016) Dynamics of chloroplast translation during chloroplast differentiation in maize. PLoS Genet 12: e1006106
Del Campo EM (2009) Post-transcriptional control of chloroplast gene expression. Gene Regul Syst Biol 3: 31-47
Deng XW, Tonkyn J, Peter G, Thornber J, Gruissem W (1989) Post-transcriptional control of plastid mRNA accumulation during adaptation of chloroplasts to different light quality environments. Plant Cell 1: 645-654
Facella P, Carbone F, Placido A, Perrotta G (2017) Cryptochrome 2 extensively regulates transcription of chloroplast genome in tomato. FEBS Open Bio 7: 456-471
Franklin KA, Quail PH (2010) Phytochrome functions in Arabidopsis development. J Exp Bot 61: 11-24
He SB, Wang WX, Zhang JY, Xu F, Lian HL, Li L, Yang HQ (2015) The CNT1 domain of Arabidopsis CRY1 alone is sufficient to mediate blue light inhibition of hypocotyl elongation. Mol Plant 8: 822-825
Hu W, Franklin KA, Sharrock RA, Jones MA, Harmer SL, Lagarias JC (2013) Unanticipated regulatory roles for Arabidopsis phytochromes revealed by null mutant analysis. Proc Nat Acad Sci USA 110: 1542-1547
Kim BH, Malec P, Waloszek A, von Arnim AG (2012) Arabidopsis BPG2: a phytochrome-regulated gene whose protein product binds to plastid ribosomal RNAs. Planta 236: 677-690
Kim J, Mullet JE (2003) A mechanism for light-induced translation of the rbcL mRNA encoding the large subunit of Ribulose-1,5-bisphosphate carboxylase in barley chloroplasts. Plant Cell Physiol 44: 194-499
Kleine T (2012) Arabidopsis thaliana mTERF proteins: evolution and functional classification. Front Plant Sci 3: 1-15
Kolde R (2019) pheatmap: Pretty Heatmaps. R package version 1.0.12. https://CRAN.R-project.org/package=pheatmap
Lamb JR, Tugendreich S, Heiter P (1995) Tetratrico peptide repeat interactions: to TPR or not to TPR? Trends Biochem Sci 20: 257-259
Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21: 3448-3449
Martin W, Stoebe B, Goremykin V, Hansmann S, Hasegawa M, Kowallik KV (1998) Gene transfer to the nucleus and evolution of the chloroplasts. Nature 393: 162-165
Mellenthin M, Ellersiek U, Borger A, Baier M (2014) Expression of the Arabidopsis thaliana sigma factor SIG5 is photoreceptor and photosynthesis controlled. Plan Theory 3: 359-391
Michael TP, Breton G, Hazen SP, Priest H, Mockler TC, Kay SA, Chory J (2008) A morning-specific Phytohormone gene expression program underlying rhythmic plant growth. PLoS Biol 6: 1887-1898
Oh S, Montgomery BL (2014) Phytochrome-dependent coordinate control of distinct aspects of nuclear and plastid gene expression during anterograde signaling and photomorphogenesis. Front Plant Sci 5: 1-8
Oh S, Warnasooriya SN, Montgomery BL (2013) Downstream effectors of light- and phytochrome-dependent regulation of hypocotyl elongation in Arabidopsis thaliana. Plant Mol Biol 81: 627-640
Ohgishi M, Saji K, Okada K, Sakai T (2004) Functional analysis of each blue light receptor cry1, cry2, phot1, and phot2, by using combinatorial multiple mutants in Arabidopsis. Proc Nat Acad Sci USA 101: 2223-2228
Oliveros J.C. (2007-2015) Venny. An interactive tool for comparing lists with Venn's diagrams. https://bioinfogp.cnb.csic.es/tools/venny/index.html
Osterlund MT, Hardtke CS, Wei N, Deng XW (2000) Target destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405: 462-466
Pfalz J, Liere K, Kandlbinder A, Dietz KJ, Oelmuller R (2006) pTAC2, −6, and −12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18: 176-197
Qiao J, Li J, Chu W, Luo M (2013) PRDA1, a novel chloroplast nucleoid protein, is required for early chloroplast development and is involved in the regulation of plastid gene expression in Arabidopsis. Plant Cell Physiol 54: 2071-2084
R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
R Core Team (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
Ruwe H, Kupsch C, Teubner M, Schmitz-Linneweber C (2011) The RNA-recognition motif in chloroplasts. J Plant Physiol 168: 1361-1371
Sato S, Nakamure Y, Kaneko T, Asamizu E, Tabata S (1999) Complete structure of the chloroplast genome of Arabidopsis thaliana. DNA Res 6: 283-290
Schuster G, Lisitsky I, Klaff P (1999) Polyadenylation and degradation of mRNA in the chloroplast. Plant Physiol 120: 937-944
Singh R, Singh S, Parihar P, Singh VP, Prasad SM (2015) Retrograde signaling between plastid and nucleus: a review. J Plant Physiol 181: 55-66
Soll J, Schleiff E (2004) Protein import into chloroplasts. Nat Rev Molecul Cell Biol 5: 198-208
Stern DB, Goldschmidt-Clermont M, Hanson MR (2010) Chloroplast RNA metabolism. Annu Rev Plant Biol 61: 125-155
Su J, Liu B, Liao J, Yang Z, Lin C, Oka Y (2017) Coordination of Cryptochrome and Phytochrome signals in the regulation of plant light responses. Agronomy 7: 1-22
Thum KE, Kim M, Christopher DA, Mullet JE (2000) Cryptochrome 1, Cryptochrome 2, and Phytochrome a co-activate the chloroplast psbD blue light-responsive promoter. Plant Cell 13: 2747-2760
Tsunoyama Y, Ishizaki Y, Morikawa K, Kobori M, Nakahira Y, Takeba G, Toyoshima Y, Shiina T (2004) Blue light-induced transcription of plastid-encoded psbD gene is mediated by a nuclear-encoded transcription initiation factor, AtSIG5. Proc Natl Acad Sci USA 101: 3304-3309
Wang P, Hendron R, Kelly S (2017) Transcriptional control of photosynthetic capacity: conservation and divergence from Arabidopsis to rice. New Phytol 216: 32-45
Yamaguchi K, Subramanian AR (2000) The plastid ribosomal proteins: identification of all the proteins in the 50S subunit of an organelle ribosome (chloroplast). J Biol Chem 275: 28466-28482
Yamaguchi K, Subramanian AR (2003) Proteomic identification of all plastid-specific ribosomal proteins in higher plant chloroplast 30S ribosomal subunit. Eur J Biochem 270: 190-205
Yang EJ, Yoo CY, Liu J, Wang H, Cao J, Li FW, Pryer KM, Sun TP, Weigel D, Zhou P, Chen M (2019) NCP activates chloroplast transcription by controlling phytochrome-dependent dual nuclear and plastidial switches. Nat Commun 10: 2630
Yoo CY, Pasoreck EK, Wang H, Cao J, Blaha GM, Weigel D, Chen M (2019) Phytochrome activates the plastid-encoded RNA polymerase for chloroplast biogenesis via nucleus-to-plastid signaling. Nat Commun 10: 2629
Zoschke R, Bock B (2018) Chloroplast translation: structural and functional organization, operational control, and regulation. Plant Cell 30: 745-770