Plastid Transcriptomics: An Important Tool For Plastid Functional Genomics

Author(s): Niaz Ahmad*, Brent L. Nielsen

Journal Name: Protein & Peptide Letters

Volume 28 , Issue 8 , 2021


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Abstract:

Plastids in higher plants carry out specialized roles such as photosynthesis, nitrogen assimilation, biosynthesis of amino acids, fatty acids, isoprenoids, and various metabolites. Plastids arise from undifferentiated precursors known as proplastids, which are found in the root and shoot meristems. They are highly dynamic as they change their number, morphology, and physiology according to the tissue they are present. In addition to housing various metabolic activities, plastids also serve as a global sensor for both internal and external environmental cues including different stresses, and help plants to respond/adjust accordingly. They relay information to the nucleus, which then responds by changing the expression levels of specific genes. It has been shown that plants with impaired plastid functions exhibit abnormalities. One of the sources emanating these signals to the nucleus is plastid transcription. Normal plastid functioning is therefore critical for plant survival. Despite immense significance for plant acclimation, the plastid transcriptome is largely an unstudied research area. In this review, we discuss the importance of plastid transcriptomics for the acclimation of plants under changing environmental conditions and summarize the key literature published in this field.

Keywords: Proplastids, plastid transcriptome, mRNA processing, functional genomics, RNA-Seq, nucleus.

[1]
Waters, M.T.; Langdale, J.A. The making of a chloroplast. EMBO J., 2009, 28(19), 2861-2873.
[http://dx.doi.org/10.1038/emboj.2009.264] [PMID: 19745808]
[2]
Small, I.D.; Rackham, O.; Filipovska, A. Organelle transcriptomes: products of a deconstructed genome. Curr. Opin. Microbiol., 2013, 16(5), 652-658.
[http://dx.doi.org/10.1016/j.mib.2013.07.011] [PMID: 23932204]
[3]
Barkan, A. Expression of plastid genes: organelle-specific elaborations on a prokaryotic scaffold. Plant Physiol., 2011, 155(4), 1520-1532.
[http://dx.doi.org/10.1104/pp.110.171231] [PMID: 21346173]
[4]
Williams, P.M.; Barkan, A. A chloroplast-localized PPR protein required for plastid ribosome accumulation. Plant J., 2003, 36(5), 675-686.
[http://dx.doi.org/10.1046/j.1365-313X.2003.01915.x] [PMID: 14617068]
[5]
Lopez-Juez, E.; Pyke, K.A. Plastids unleashed: their development and their integration in plant development. Int. J. Dev. Biol., 2005, 49(5-6), 557-577.
[http://dx.doi.org/10.1387/ijdb.051997el] [PMID: 16096965]
[6]
Pyke, K.A. Plastid division and development. Plant Cell, 1999, 11(4), 549-556.
[http://dx.doi.org/10.1105/tpc.11.4.549] [PMID: 10213777]
[7]
Morley, S.A.; Ahmad, N.; Nielsen, B.L. Plant organelle genome replication. Plants (Basel), 2019, 8(10), 358.
[http://dx.doi.org/10.3390/plants8100358] [PMID: 31546578]
[8]
Jarvis, P.; López-Juez, E. Biogenesis and homeostasis of chloroplasts and other plastids. Nat. Rev. Mol. Cell Biol., 2013, 14(12), 787-802.
[http://dx.doi.org/10.1038/nrm3702] [PMID: 24263360]
[9]
Zoschke, R.; Bock, R. Chloroplast translation: structural and functional organization, operational control, and regulation. Plant Cell, 2018, 30(4), 745-770.
[http://dx.doi.org/10.1105/tpc.18.00016] [PMID: 29610211]
[10]
Börner, T. Chloroplast Gene Expression—RNA Synthesis and Processing. In: Plastid Biology; Theg, S.M.; Wollman, F-A., Eds.; Springer: New York, NY, 2014; pp. 3-47.
[http://dx.doi.org/10.1007/978-1-4939-1136-3_1]
[11]
Khan, M.S. Transplastomics: A Convergence of Genomics and Biotechnology In: PlantOmics: The Omics of Plant Science; Barh, D.; Khan, M.S.; Davies, E., Eds.; Springer: India, 2015; pp. 559-571.
[http://dx.doi.org/10.1007/978-81-322-2172-2_19]
[12]
Kanamaru, K.; Tanaka, K. Roles of chloroplast RNA polymerase sigma factors in chloroplast development and stress response in higher plants. Biosci. Biotechnol. Biochem., 2004, 68(11), 2215-2223.
[http://dx.doi.org/10.1271/bbb.68.2215] [PMID: 15564657]
[13]
Leister, D.; Wang, L.; Kleine, T. Organellar gene expression and acclimation of plants to environmental stress. Front. Plant Sci., 2017, 8, 387.
[http://dx.doi.org/10.3389/fpls.2017.00387] [PMID: 28377785]
[14]
Pyke, K. Plastid biology, 1st Ed; Cambridge: Cambridge University Press, 2009.
[http://dx.doi.org/10.1017/CBO9780511626715]
[15]
Börner, T. Chloroplast RNA polymerases: role in chloroplast biogenesis. Biochi. Biophy. Acta., 2015, 1847(9), 761-769.
[http://dx.doi.org/10.1016/j.bbabio.2015.02.004]
[16]
Bock, R. Engineering plastid genomes: methods, tools, and applications in basic research and biotechnology. Annu. Rev. Plant Biol., 2015, 66(3), 211-241.
[http://dx.doi.org/10.1146/annurev-arplant-050213-040212] [PMID: 25494465]
[17]
Schmitz-Linneweber, C.; Barkan, A. RNA splicing and RNA editing in chloroplasts. In: Cell and Molecular Biology of Plastids; Bock, R., Ed.; Springer: Berlin, Heidelberg, 2007; pp. 213-248.
[http://dx.doi.org/10.1007/4735_2007_0233]
[18]
Ruf, S.; Bock, R. In vivo analysis of RNA editing in plastids. In: RNA and DNA Editing; Aphasizhev, R., Ed.; Humana Press, 2011; pp. 137-150.
[http://dx.doi.org/10.1007/978-1-61779-018-8_8]
[19]
Stern, D.B.; Goldschmidt-Clermont, M.; Hanson, M.R. Chloroplast RNA metabolism. Annu. Rev. Plant Biol., 2010, 61, 125-155.
[http://dx.doi.org/10.1146/annurev-arplant-042809-112242] [PMID: 20192740]
[20]
de Luna-Valdez, L. Chloroplast omics. In: PlantOmics: The Omics of Plant Science; Barh, D.; Khan, M.S.; Davies, E., Eds.; Springer: India, 2015; pp. 533-558.
[21]
Feng, P.; Guo, H.; Chi, W.; Chai, X.; Sun, X.; Xu, X.; Ma, J.; Rochaix, J.D.; Leister, D.; Wang, H.; Lu, C.; Zhang, L. Chloroplast retrograde signal regulates flowering. Proc. Natl. Acad. Sci. USA, 2016, 113(38), 10708-10713.
[http://dx.doi.org/10.1073/pnas.1521599113] [PMID: 27601637]
[22]
Cejudo, F.J.; Ojeda, V.; Delgado-Requerey, V.; González, M.; Pérez-Ruiz, J.M. Chloroplast redox regulatory mechanisms in plant adaptation to light and darkness. Front. Plant Sci., 2019, 10(380), 380.
[http://dx.doi.org/10.3389/fpls.2019.00380] [PMID: 31019520]
[23]
Dalal, V.; Dagan, S.; Friedlander, G.; Aviv, E.; Bock, R.; Charuvi, D.; Reich, Z.; Adam, Z. Transcriptome analysis highlights nuclear control of chloroplast development in the shoot apex. Sci. Rep., 2018, 8(1), 8881-8881.
[http://dx.doi.org/10.1038/s41598-018-27305-4] [PMID: 29892011]
[24]
Allen, J.F. Photosynthesis: the processing of redox signals in chloroplasts. Curr. Biol., 2005, 15(22), R929-R932.
[http://dx.doi.org/10.1016/j.cub.2005.10.061] [PMID: 16303553]
[25]
Pfannschmidt, T.; Nilsson, A.; Allen, J.F. Photosynthetic control of chloroplast gene expression. Nature, 1999, 397(6720), 625.
[http://dx.doi.org/10.1038/17624]
[26]
Ahmad, N.; Nielsen, B.L. Plant organelle DNA maintenance. Plants, 2020, 9(6)(683)
[http://dx.doi.org/10.3390/plants9060683]
[27]
Smith, D.R.; Sanitá Lima, M. Unraveling chloroplast transcriptomes with ChloroSeq, an organelle RNA-Seq bioinformatics pipeline. Brief. Bioinform., 2017, 18(6), 1012-1016.
[PMID: 27677960]
[28]
Kindgren, P.; Dubreuil, C.; Strand, Å. The recovery of plastid function is required for optimal response to low temperatures in arabidopsis. PLoS One, 2015, 10(9), e0138010.
[http://dx.doi.org/10.1371/journal.pone.0138010] [PMID: 26366569]
[29]
Chiba, Y.; Mineta, K.; Hirai, M.Y.; Suzuki, Y.; Kanaya, S.; Takahashi, H.; Onouchi, H.; Yamaguchi, J.; Naito, S. Changes in mRNA stability associated with cold stress in Arabidopsis cells. Plant Cell Physiol., 2013, 54(2), 180-194.
[http://dx.doi.org/10.1093/pcp/pcs164] [PMID: 23220693]
[30]
Ahmad, N. Contrasting responses to stress displayed by tobacco overexpressing an algal plastid terminal oxidase in the chloroplast. Front. Plant Sci., 2020, 11, 501.
[http://dx.doi.org/10.3389/fpls.2020.00501]
[31]
Leister, D.; Wang, X.; Haberer, G.; Mayer, K.F.; Kleine, T. Intracompartmental and intercompartmental transcriptional networks coordinate the expression of genes for organellar functions. Plant Physiol., 2011, 157(1), 386-404.
[http://dx.doi.org/10.1104/pp.111.177691] [PMID: 21775496]
[32]
Kahlau, S.; Bock, R. Plastid transcriptomics and translatomics of tomato fruit development and chloroplast-to-chromoplast differentiation: chromoplast gene expression largely serves the production of a single protein. Plant Cell, 2008, 20(4), 856-874.
[http://dx.doi.org/10.1105/tpc.107.055202] [PMID: 18441214]
[33]
Demarsy, E.; Buhr, F.; Lambert, E.; Lerbs-Mache, S. Characterization of the plastid-specific germination and seedling establishment transcriptional programme. J. Exp. Bot., 2012, 63(2), 925-939.
[http://dx.doi.org/10.1093/jxb/err322] [PMID: 22048039]
[34]
Allorent, G.; Courtois, F.; Chevalier, F.; Lerbs-Mache, S. Plastid gene expression during chloroplast differentiation and dedifferentiation into non-photosynthetic plastids during seed formation. Plant Mol. Biol., 2013, 82(1-2), 59-70.
[http://dx.doi.org/10.1007/s11103-013-0037-0] [PMID: 23494253]
[35]
Wu, G-Z.; Meyer, E.H.; Wu, S.; Bock, R. Extensive posttranscriptional regulation of nuclear gene expression by plastid retrograde signals. Plant Physiol., 2019, 180(4), 2034-2048.
[http://dx.doi.org/10.1104/pp.19.00421] [PMID: 31138622]
[36]
Courtois, F.; Merendino, L. Mapping plastid transcript population by circular reverse transcription polymerase chain reaction. In: Plastids; Maréchal, E., Ed.; Humana Press: New York, NY, 2018; pp. 273-278.
[http://dx.doi.org/10.1007/978-1-4939-8654-5_18]
[37]
Malbert, B. Bioinformatic analysis of chloroplast gene expression and RNA posttranscriptional maturations using RNA sequencing. In: Plastids, Maréchal, E., Ed.; Humana Press: New York, NY, 2018; pp. 279-294.
[http://dx.doi.org/10.1007/978-1-4939-8654-5_19]
[38]
Michel, E.J. A guide to the chloroplast transcriptome analysis using RNA-Seq. In: Plastids; Maréchal, E., Ed.; Humana Press: New York, NY, 2018; pp. 295-313.
[http://dx.doi.org/10.1007/978-1-4939-8654-5_20]
[39]
Wang, Z.; Gerstein, M.; Snyder, M. RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet., 2009, 10(1), 57-63.
[http://dx.doi.org/10.1038/nrg2484] [PMID: 19015660]
[40]
Ahmad, N.; Mehmood, M.J.N.G.S.A. RNA-Seq: a Powerful Tool for Cataloguing the Transcriptome. Next Generat. Sequenc. Appl., 2015, 2, e103.
[41]
McDermaid, A.; Monier, B.; Zhao, J.; Liu, B.; Ma, Q. Interpretation of differential gene expression results of RNA-seq data: review and integration. Brief. Bioinform., 2019, 20(6), 2044-2054.
[http://dx.doi.org/10.1093/bib/bby067] [PMID: 30099484]
[42]
Greiner, S.; Lehwark, P.; Bock, R. OrganellarGenomeDRAW (OGDRAW) version 1.3.1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Research, 2019, 47(W1), W59-W64.
[http://dx.doi.org/10.1093/nar/gkz238] [PMID: 30949694]


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Article Details

VOLUME: 28
ISSUE: 8
Year: 2021
Published on: 28 January, 2021
Page: [855 - 860]
Pages: 6
DOI: 10.2174/0929866528999210128210555
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