Abstract
Main conclusion
Expression of PAP genes is strongly coordinated and represents a highly selective cell-specific marker associated with the development of chloroplasts in photosynthetically active organs of Arabidopsis seedlings and adult plants.
Transcription in plastids of plants depends on the activity of phage-type single-subunit nuclear-encoded RNA polymerases (NEP) and a prokaryotic multi-subunit plastid-encoded RNA polymerase (PEP). PEP is comprised of the core subunits α, β, β′ and β″ encoded by rpoA, rpoB/C1/C2 genes located on the plastome. This core enzyme needs to interact with nuclear-encoded sigma factors for proper promoter recognition. In chloroplasts, the core enzyme is surrounded by additional 12 nuclear-encoded subunits, all of eukaryotic origin. These PEP-associated proteins (PAPs) were found to be essential for chloroplast biogenesis as Arabidopsis inactivation mutants for each of them revealed albino or pale-green phenotypes. In silico analysis of transcriptomic data suggests that PAP genes represent a tightly controlled regulon, whereas wetlab data are sparse and correspond to the expression of individual genes mostly studied at the seedling stage. Using RT-PCR, transient, and stable expression assays of PAP promoter-GUS-constructs, we do provide, in this study, a comprehensive expression catalogue for PAP genes throughout the life cycle of Arabidopsis. We demonstrate a selective impact of light on PAP gene expression and uncover a high tissue specificity that is coupled to developmental progression especially during the transition from skotomorphogenesis to photomorphogenesis. Our data imply that PAP gene expression precedes the formation of chloroplasts rendering PAP genes a tissue- and cell-specific marker of chloroplast biogenesis.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- HY5:
-
Elongated hypocotyl 5
- NEP:
-
Nuclear-encoded RNA polymerases
- PEP:
-
Plastid-encoded RNA polymerase
- PAPs:
-
PEP-associated proteins
References
Allorent G, Courtois F, Chevalier F, Lerbs-Mache S (2013) Plastid gene expression during chloroplast differentiation and dedifferentiation into non-photosynthetic plastids during seed formation. Plant Mol Biol 82(1–2):59–70. https://doi.org/10.1007/s11103-013-0037-0
Allorent G, Osorio S, Vu JL, Falconet D, Jouhet J, Kuntz M, Fernie AR, Lerbs-Mache S, Macherel D, Courtois F, Finazzi G (2015) Adjustments of embryonic photosynthetic activity modulate seed fitness in Arabidopsis thaliana. New Phytol 205(2):707–719. https://doi.org/10.1111/nph.13044
Ambrose BA, Lerner DR, Ciceri P, Padilla CM, Yanofsky MF, Schmidt RJ (2000) Molecular and genetic analyses of the silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol Cell 5(3):569–579
Ang LH, Chattopadhyay S, Wei N, Oyama T, Okada K, Batschauer A, Deng XW (1998) Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell 1:213–222
Arsova B, Hoja U, Wimmelbacher M, Greiner E, Üstün S, Melzer M, Petersen K, Lein W, Börnke F (2010) Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana. Plant Cell 22(5):1498–1515. https://doi.org/10.1105/tpc.109.071001
Barton KA, Schattat MH, Jakob T, Hause G, Wilhelm C, McKenna JF, Mathe C, Runions J, Van Damme D, Mathur J (2016) Epidermal pavement cells of Arabidopsis have chloroplasts. Plant Physiol 171(2):723–726. https://doi.org/10.1104/pp.16.00608
Bastien O, Botella C, Chevalier F, Block MA, Jouhet J, Breton C, Girard-Egrot A, Marechal E (2016) New insights on thylakoid biogenesis in plant cells. Int Rev Cell Mol Biol 323:1–30. https://doi.org/10.1016/bs.ircmb.2015.12.001
Baumgartner BJ, Rapp JC, Mullet JE (1989) Plastid transcription activity and DNA copy number increase early in barley chloroplast development. Plant Physiol 89(3):1011–1018
Belmonte MF, Kirkbride RC, Stone SL, Pelletier JM, Bui AQ, Yeung EC, Hashimoto M, Fei J, Harada CM, Munoz MD, Le BH, Drews GN, Brady SM, Goldberg RB, Harada JJ (2013) Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed. Proc Natl Acad Sci USA 110(5):E435–E444. https://doi.org/10.1073/pnas.1222061110
Bendich AJ (2013) DNA abandonment and the mechanisms of uniparental inheritance of mitochondria and chloroplasts. Chromosome Res 21(3):287–296. https://doi.org/10.1007/s10577-013-9349-9
Blanvillain R (2000) Etude d’un marqueur génétique du suspenseur chez Arabidopsis thaliana et application d’un système d’activation de gène à la recherche de sa fonction. University of Perpignan, Ph.D. thesis, Perpignan
Blanvillain R, Boavida LC, McCormick S, Ow DW (2008) Exportin1 genes are essential for development and function of the gametophytes in Arabidopsis thaliana. Genetics 180(3):1493–1500. https://doi.org/10.1534/genetics.108.094896
Blanvillain R, Young B, Cai YM, Hecht V, Varoquaux F, Delorme V, Lancelin JM, Delseny M, Gallois P (2011) The Arabidopsis peptide kiss of death is an inducer of programmed cell death. EMBO J 30(6):1173–1183. https://doi.org/10.1038/emboj.2011.14
Börner T, Aleynikova AY, Zubo YO, Kusnetsov VV (2015) Chloroplast RNA polymerases: role in chloroplast biogenesis. Biochim Biophys Acta 1847(9):761–769. https://doi.org/10.1016/j.bbabio.2015.02.004
Charuvi D, Kiss V, Nevo R, Shimoni E, Adam Z, Reich Z (2012) Gain and loss of photosynthetic membranes during plastid differentiation in the shoot apex of Arabidopsis. Plant Cell 24(3):1143–1157. https://doi.org/10.1105/tpc.111.094458
Chen M, Galvão RM, Li M, Burger B, Bugea J, Bolado J, Chory J (2010) Arabidopsis HEMERA/pTAC12 initiates photomorphogenesis by phytochromes. Cell 141(7):1230–1240. https://doi.org/10.1016/j.cell.2010.05.007
Chiang YH, Zubo YO, Tapken W, Kim HJ, Lavanway AM, Howard L, Pilon M, Kieber JJ, Schaller GE (2012) Functional characterization of the GATA transcription factors GNC and CGA1 reveals their key role in chloroplast development, growth, and division in Arabidopsis. Plant Physiol 160(1):332–348. https://doi.org/10.1104/pp.112.198705
Chory J, Peto CA (1990) Mutations in the DET1 gene affect cell-type-specific expression of light-regulated genes and chloroplast development in Arabidopsis. Proc Natl Acad Sci USA 87(22):8776–8780
Chotewutmontri P, Barkan A (2016) Dynamics of chloroplast translation during chloroplast differentiation in maize. PLoS Genet 12(7):e1006106. https://doi.org/10.1371/journal.pgen.1006106
Clément C, Pacini E (2001) Anther plastids in angiosperms. Bot Rev 67:54
Deng XW, Matsui M, Wei N, Wagner D, Chu AM, Feldmann KA, Quail PH (1992) COP1, an Arabidopsis regulatory gene, encodes a protein with both a zinc-binding motif and a G beta homologous domain. Cell 71(5):791–801
Eckardt NA (2007) Light regulation of plant development: HY5 genomic binding sites. Plant Cell 19:727–729
Gao ZP, Yu QB, Zhao TT, Ma Q, Chen GX, Yang ZN (2011) A functional component of the transcriptionally active chromosome complex, Arabidopsis pTAC14, interacts with pTAC12/HEMERA and regulates plastid gene expression. Plant Physiol 157(4):1733–1745. https://doi.org/10.1104/pp.111.184762
Gifford RM, Bremner PM (1981) Accumulation and conversion of sugars by developing wheat grains. II. Light requirement for kernels cultured in vitro. Funct Plant Biol 8:631–640
Gilkerson J, Perez-Ruiz JM, Chory J, Callis J (2012) The plastid-localized pfkB-type carbohydrate kinases FRUCTOKINASE-LIKE 1 and 2 are essential for growth and development of Arabidopsis thaliana. BMC Plant Biol 12:102. https://doi.org/10.1186/1471-2229-12-102
Grübler B, Merendino L, Twardziok SO, Mininno M, Allorent G, Chevalier F, Liebers M, Blanvillain R, Mayer K, Lerbs-Mache S, Ravanel S, Pfannschmidt T (2017) Light and plastid signals regulate different sets of genes in the albino mutant pap7-1. Plant Physiol 175(3):1203–1219. https://doi.org/10.1104/pp.17.00982
Hajdukiewicz PT, Allison LA, Maliga P (1997) The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J 16(13):4041–4048. https://doi.org/10.1093/emboj/16.13.4041
Hermkes R, Fu YF, Nürrenberg K, Budhiraja R, Schmelzer E, Elrouby N, Dohmen RJ, Bachmair A, Coupland G (2011) Distinct roles for Arabidopsis SUMO protease ESD4 and its closest homolog ELS1. Planta 233(1):63–73. https://doi.org/10.1007/s00425-010-1281-z
Hu J, Bogorad L (1990) Maize chloroplast RNA polymerase: the 180-, 120-, and 38-kilodalton polypeptides are encoded in chloroplast genes. Proc Natl Acad Sci USA 87(4):1531–1535
Igloi GL, Meinke A, Döry I, Kössel H (1990) Nucleotide sequence of the maize chloroplast rpo B/C1/C2 operon: comparison between the derived protein primary structures from various organisms with respect to functional domains. Mol Gen Genet 221(3):379–394
Jin X, Zhu J, Zeiger E (2001) The hypocotyl chloroplast plays a role in phototropic bending of Arabidopsis seedlings: developmental and genetic evidence. J Exp Bot 52(354):91–97
Kindgren P, Strand A (2015) Chloroplast transcription, untangling the Gordian Knot. New Phytol 206:889–891
Kobayashi K, Baba S, Obayashi T, Sato M, Toyooka K, Keränen M, Aro EM, Fukaki H, Ohta H, Sugimoto K, Masuda T (2012) Regulation of root greening by light and auxin/cytokinin signaling in Arabidopsis. Plant Cell 24(3):1081–1095. https://doi.org/10.1105/tpc.111.092254
Kremnev D, Strand A (2014) Plastid encoded RNA polymerase activity and expression of photosynthesis genes required for embryo and seed development in Arabidopsis. Front Plant Sci 5:385. https://doi.org/10.3389/fpls.2014.00385
Le BH, Cheng C, Bui AQ, Wagmaister JA, Henry KF, Pelletier J, Kwong L, Belmonte M, Kirkbride R, Horvath S, Drews GN, Fischer RL, Okamuro JK, Harada JJ, Goldberg RB (2010) Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc Natl Acad Sci USA 107(18):8063–8070. https://doi.org/10.1073/pnas.1003530107
Lee J, He K, Stolc V, Lee H, Figueroa P, Gao Y, Tongprasit W, Zhao H, Lee I, Deng XW (2007) Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19:731–749
Lerbs-Mache S (2011) Function of plastid sigma factors in higher plants: regulation of plastid gene expression or just preservation of constitutive transcription? Plant Mol Biol 76:235–249
Li J, Li G, Wang H, Deng XW (2011) Phytochrome signaling mechanisms. Arabidopsis Book 9:e0148. https://doi.org/10.1199/tab.0148
Liebers M, Grübler B, Chevalier F, Lerbs-Mache S, Merendino L, Blanvillain R, Pfannschmidt T (2017) Regulatory shifts in plastid transcription play a key role in morphological conversions of plastids during plant development. Front Plant Sci 8:23. https://doi.org/10.3389/fpls.2017.00023
Liere K, Weihe A, Börner T (2011) The transcription machineries of plant mitochondria and chloroplasts: composition, function, and regulation. J Plant Physiol 168(12):1345–1360. https://doi.org/10.1016/j.jplph.2011.01.005
Liu H, Wang X, Ren K, Li K, Wei M, Wang W, Sheng X (2017) Light deprivation-induced inhibition of chloroplast biogenesis does not arrest embryo morphogenesis but strongly reduces the accumulation of storage reserves during embryo maturation in Arabidopsis. Front Plant Sci 8:1287
Lopez-Juez E, Pyke KA (2005) Plastids unleashed: their development and their integration in plant development. Int J Dev Biol 49(5–6):557–577. https://doi.org/10.1387/ijdb.051997el
Majeran W, Friso G, Asakura Y, Qu X, Huang M, Ponnala L, Watkins KP, Barkan A, van Wijk KJ (2012) Nucleoid-enriched proteomes in developing plastids and chloroplasts from maize leaves: a new conceptual framework for nucleoid functions. Plant Physiol 158(1):156–189. https://doi.org/10.1104/pp.111.188474
Melonek J, Matros A, Trösch M, Mock HP, Krupinska K (2012) The core of chloroplast nucleoids contains architectural SWIB domain proteins. Plant Cell 24(7):3060–3073. https://doi.org/10.1105/tpc.112.099721
Mullet JE, Klein RR (1987) Transcription and RNA stability are important determinants of higher plant chloroplast RNA levels. EMBO J 6(6):1571–1579
Myouga F, Hosoda C, Umezawa T, Iizumi H, Kuromori T, Motohashi R, Shono Y, Nagata N, Ikeuchi M, Shinozaki K (2008) A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell 20(11):3148–3162. https://doi.org/10.1105/tpc.108.061341
Osterlund MT, Hardtke CS, Wei N, Deng XW (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405:462–466
Oyama T, Shimura Y, Okada K (1997) The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev 11:2983–2995
Pfalz J, Pfannschmidt T (2013) Essential nucleoid proteins in early chloroplast development. Trends Plant Sci 18(4):186–194. https://doi.org/10.1016/j.tplants.2012.11.003
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(1):176–197. https://doi.org/10.1105/tpc.105.036392
Pfalz J, Holtzegel U, Barkan A, Weisheit W, Mittag M, Pfannschmidt T (2015) ZmpTAC12 binds single-stranded nucleic acids and is essential for accumulation of the plastid-encoded polymerase complex in maize. New Phytol 206(3):1024–1037. https://doi.org/10.1111/nph.13248
Pfannschmidt T, Link G (1994) Separation of two classes of plastid DNA-dependent RNA polymerases that are differentially expressed in mustard (Sinapis alba L.) seedlings. Plant Mol Biol 25(1):69–81
Pfannschmidt T, Ogrzewalla K, Baginsky S, Sickmann A, Meyer HE, Link G (2000) The multisubunit chloroplast RNA polymerase A from mustard (Sinapis alba L.). Integration of a prokaryotic core into a larger complex with organelle-specific functions. Eur J Biochem 267(1):253–261
Pfannschmidt T, Blanvillain R, Merendino L, Courtois F, Chevalier F, Liebers M, Grübler B, Hommel E, Lerbs-Mache S (2015) Plastid RNA polymerases: orchestration of enzymes with different evolutionary origins controls chloroplast biogenesis during the plant life cycle. J Exp Bot 66:6957–6973. https://doi.org/10.1093/jxb/erv415
Pogson BJ, Ganguly D, Albrecht-Borth V (2015) Insights into chloroplast biogenesis and development. Biochim Biophys Acta 1847(9):1017–1024. https://doi.org/10.1016/j.bbabio.2015.02.003
Pribil M, Labs M, Leister D (2014) Structure and dynamics of thylakoids in land plants. J Exp Bot 65(8):1955–1972. https://doi.org/10.1093/jxb/eru090
Pyke KA, Leech RM (1994) A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol 104(1):201–207
Pyke KA, Page AM (1998) Plastid ontogeny during petal development in Arabidopsis. Plant Physiol 116(2):797–803
Quail PH (2002) Phytochrome photosensory signalling networks. Nat Rev Mol Cell Biol 3:85–93
Radchuk V, Borisjuk L (2014) Physical, metabolic and developmental functions of the seed coat. Front Plant Sci 5:510. https://doi.org/10.3389/fpls.2014.00510
Rodermel SR, Bogorad L (1985) Maize plastid photogenes: mapping and photoregulation of transcript levels during light-induced development. J Cell Biol 100:463–476
Saijo Y, Sullivan JA, Wang H, Yang J, Shen Y, Rubio V, Ma L, Hoecker U, Deng XW (2003) The COP1-SPA1 interaction defines a critical step in phytochrome A-mediated regulation of HY5 activity. Genes Dev 17:2642–2647
Schröter Y, Steiner S, Matthäi K, Pfannschmidt T (2010) Analysis of oligomeric protein complexes in the chloroplast sub-proteome of nucleic acid-binding proteins from mustard reveals potential redox regulators of plastid gene expression. Proteomics 10(11):2191–2204. https://doi.org/10.1002/pmic.200900678
Schröter Y, Steiner S, Weisheit W, Mittag M, Pfannschmidt T (2014) A purification strategy for analysis of the DNA/RNA-associated sub-proteome from chloroplasts of mustard cotyledons. Front Plant Sci 5:557. https://doi.org/10.3389/fpls.2014.00557
Solymosi K, Schoefs B (2010) Etioplast and etio-chloroplast formation under natural conditions: the dark side of chlorophyll biosynthesis in angiosperms. Photosynth Res 105(2):143–166. https://doi.org/10.1007/s11120-010-9568-2
Somers DE, Quail PH (1995) Temporal and spatial expression patterns of PHYA and PHYB genes in Arabidopsis. Plant J 7(3):413–427
Steiner S, Schröter Y, Pfalz J, Pfannschmidt T (2011) Identification of essential subunits in the plastid-encoded RNA polymerase complex reveals building blocks for proper plastid development. Plant Physiol 157(3):1043–1055. https://doi.org/10.1104/pp.111.184515
Sugiura M (1992) The chloroplast genome. Plant Mol Biol 19(1):149–168
Suzuki JY, Ytterberg AJ, Beardslee TA, Allison LA, Wijk KJ, Maliga P (2004) Affinity purification of the tobacco plastid RNA polymerase and in vitro reconstitution of the holoenzyme. Plant J 40(1):164–172. https://doi.org/10.1111/j.1365-313X.2004.02195.x
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
Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5(2):123–135. https://doi.org/10.1038/nrg1271
Tschiersch H, Liebsch G, Borisjuk L, Stangelmayer A, Rolletschek H (2012) An imaging method for oxygen distribution, respiration and photosynthesis at a microscopic level of resolution. New Phytol 196(3):926–936. https://doi.org/10.1111/j.1469-8137.2012.04295.x
Usami T, Mochizuki N, Kondo M, Nishimura M, Nagatani A (2004) Cryptochromes and phytochromes synergistically regulate Arabidopsis root greening under blue light. Plant Cell Physiol 45:1798–1808
Virdi KS, Wamboldt Y, Kundariya H, Laurie JD, Keren I, Kumar KR, Block A, Basset G, Luebker S, Elowsky C, Day PM, Roose JL, Bricker TM, Elthon T, Mackenzie SA (2016) MSH1 is a plant organellar DNA binding and thylakoid protein under precise spatial regulation to alter development. Mol Plant 9(2):245–260. https://doi.org/10.1016/j.molp.2015.10.011
Wagner R, Dietzel L, Bräutigam K, Fischer W, Pfannschmidt T (2008) The long-term response to fluctuating light quality is an important and distinct light acclimation mechanism that supports survival of Arabidopsis thaliana under low light conditions. Planta 228(4):573–587. https://doi.org/10.1007/s00425-008-0760-y
Wimmelbacher M, Börnke F (2014) Redox activity of thioredoxin z and fructokinase-like protein 1 is dispensable for autotrophic growth of Arabidopsis thaliana. J Exp Bot 65(9):2405–2413. https://doi.org/10.1093/jxb/eru122
Yagi Y, Ishizaki Y, Nakahira Y, Tozawa Y, Shiina T (2012) Eukaryotic-type plastid nucleoid protein pTAC3 is essential for transcription by the bacterial-type plastid RNA polymerase. Proc Natl Acad Sci USA 109(19):7541–7546. https://doi.org/10.1073/pnas.1119403109
Yu QB, Lu Y, Ma Q, Zhao TT, Huang C, Zhao HF, Zhang XL, Lv RH, Yang ZN (2013) TAC7, an essential component of the plastid transcriptionally active chromosome complex, interacts with FLN1, TAC10, TAC12 and TAC14 to regulate chloroplast gene expression in Arabidopsis thaliana. Physiol Plant 148(3):408–421. https://doi.org/10.1111/j.1399-3054.2012.01718.x
Zoschke R, Liere K, Börner T (2007) From seedling to mature plant: arabidopsis plastidial genome copy number, RNA accumulation and transcription are differentially regulated during leaf development. Plant J 50(4):710–722. https://doi.org/10.1111/j.1365-313X.2007.03084.x
Acknowledgements
This work was supported by a grant from the Deutsche Forschungsgemeinschaft to T.P. (PF323-5) and a grant from the AGIR programme of Université Grenoble-Alpes (UGA) to R.B. The project received further support by institutional grants to Laboratoire de Physiologie Cellulaire et Végétale by Labex Grenoble Alliance of Integrated Structural Biology (GRAL), UGA, Institut National de la Recherche Agronomique (INRA), and the Centre National de la Recherche Scientifique (CNRS). The authors thank Julia Engelhorn and Christel Carles for the help with in situ preparations and critical inputs.
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Liebers, M., Chevalier, F., Blanvillain, R. et al. PAP genes are tissue- and cell-specific markers of chloroplast development. Planta 248, 629–646 (2018). https://doi.org/10.1007/s00425-018-2924-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-018-2924-8