Limiting etioplast gene expression induces apical hook twisting during skotomorphogenesis of Arabidopsis seedlings.
Arabidopsis thaliana
AOX1A
apical hook bending
gene expression
mitochondria
plastids
reactive oxygen species
rifampicin
skotomorphogenesis
spectinomycin
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
04 2023
04 2023
Historique:
revised:
20
01
2023
received:
20
04
2022
accepted:
01
02
2023
medline:
11
4
2023
pubmed:
8
2
2023
entrez:
7
2
2023
Statut:
ppublish
Résumé
When covered by a layer of soil, seedling development follows a dark-specific program (skotomorphogenesis). In the dark, seedlings consist of small, non-green cotyledons, a long hypocotyl, and an apical hook to protect meristematic cells. We recently highlighted the role played by mitochondria in the high energy-consuming reprogramming of Arabidopsis skotomorphogenesis. Here, the role played by plastids, another energy-supplying organelle, in skotomorphogenesis is investigated. This study was conducted in dark conditions to exclude light signals so as to better focus on those produced by plastids. It was found that limitation of plastid gene expression (PGE) induced an exaggerated apical hook bending. Inhibition of PGE was obtained at the levels of transcription and translation using the antibiotics rifampicin (RIF) and spectinomycin, respectively, as well as plastid RPOTp RNA polymerase mutants. RIF-treated seedlings also showed expression induction of marker nuclear genes for mitochondrial stress, perturbation of mitochondrial metabolism, increased ROS levels, and an augmented capacity of oxygen consumption by mitochondrial alternative oxidases (AOXs). AOXs act to prevent overreduction of the mitochondrial electron transport chain. Previously, we reported that AOX1A, the main AOX isoform, is a key component in the developmental response to mitochondrial respiration deficiency. In this work, we suggest the involvement of AOX1A in the response to PGE dysfunction and propose the importance of signaling between plastids and mitochondria. Finally, it was found that seedling architecture reprogramming in response to RIF was independent of canonical organelle retrograde pathways and the ethylene signaling pathway.
Substances chimiques
Arabidopsis Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
293-309Informations de copyright
© 2023 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Bailly, C. & Merendino, L. (2021) Oxidative signalling in seed germination and early seedling growth: an emerging role for ROS trafficking and inter-organelle communication. The Biochemical Journal, 478, 1977-1984.
Benjamini, Y. & Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society, Series B, 57, 289-300. Available from: https://www.jstor.org/stable/2346101 [Accessed 18th November 2019]
Courtois, F., Merendino, L., Demarsy, E., Mache, R. & Lerbs-Mache, S. (2007) Phage-type RNA polymerase RPOTmp transcribes the rrn operon from the PC promoter at early developmental stages in Arabidopsis. Plant Physiology, 145, 712-721. Available from: http://www.plantphysiol.org/cgi/doi/10.1104/pp.107.103846 [Accessed 22nd May 2018]
Deng, X.-W. & Quail, P.H. (1992) Genetic and phenotypic characterization of cop1 mutants of Arabidopsis thaliana. The Plant Journal, 2, 83-95. Available from: http://doi.wiley.com/10.1111/j.1365-313X.1992.00083.x [Accessed 29th July 2019]
Ellis, R.J., Mcdonald, I.R., Parenti, F., Margulies, M.M., Schwartz, J.H., Meyer, R. et al. (1970) Further similarities between chloroplast and bacterial ribosomes. Planta, 91, 329-335.
Fiehn, O. (2006) Metabolite profiling in Arabidopsis. Methods in Molecular Biology, 323, 439-447.
Fiehn, O., Wohlgemuth, G., Scholz, M., Kind, T., Lee, D.Y., Lu, Y. et al. (2008) Quality control for plant metabolomics: reporting MSI-compliant studies. The Plant Journal, 53, 691-704.
Gommers, C.M.M. & Monte, E. (2018) Update on photomorphogenesis seedling establishment: a dimmer switch-regulated process between dark and light signaling 1[OPEN]. Plant Physiology, 176, 1061-1074. Available from: www.plantphysiol.org/cgi/doi/10.1104/pp.17.01460 [Accessed 23th February 2023]
Gommers, C.M.M., Ruiz-Sola, M.Á., Ayats, A., Pereira, L., Pujol, M. & Monte, E. (2020) GENOMES UNCOUPLED1-independent retrograde signaling targets the ethylene pathway to repress photomorphogenesis. Plant Physiology, 185, 67-76. Available from: https://academic.oup.com/plphys/advance-article/doi/10.1093/plphys/kiaa015/5991408 [Accessed 8th February 2021]
Grübler, B., Merendino, L., Twardziok, S.O., Mininno, M., Allorent, G., Chevalier, F. et al. (2017) Light and plastid signals regulate different sets of genes in the albino mutant pap7-1. Plant Physiology, 175, 1203-1219.
Guzmán, P. & Ecker, J.R. (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell, 2, 513-523. Available from: http://www.plantcell.org/cgi/doi/10.1105/tpc.2.6.513 [Accessed 22nd May 2018]
Hernández-Verdeja, T. & Strand, Å. (2018) Retrograde signals navigate the path to chloroplast development. Plant Physiology, 176, 967-976. Available from: http://www.plantphysiol.org/lookup/doi/10.1104/pp.17.01299 [Accessed 19th February 2019]
Hernández-Verdeja, T., Vuorijoki, L., Jin, X., Vergara, A., Dubreuil, C. & Strand, A. (2022) GENOMES UNCOUPLED1 plays a key role during the de-etiolation process in Arabidopsis. The New Phytologist, 235, 188-203. Available from: https://nph.onlinelibrary.wiley.com/doi/10.1111/nph.18115 [Accessed 13th January 2023]
Hricová, A., Quesada, V. & Micol, J.L. (2006) The SCABRA3 nuclear gene encodes the plastid RpoTp RNA polymerase, which is required for chloroplast biogenesis and mesophyll cell proliferation in Arabidopsis. Plant Physiology, 141, 942-956. Available from: www.plantphysiol.org/cgi/doi/10.1104/pp.106.080069.942 [Accessed 30th September 2020]
Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U. et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics, 4, 249-264. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12925520 [Accessed 18th November 2019]
Jayawardhane, J., Cochrane, D.W., Vyas, P., Bykova, N.V., Vanlerberghe, G.C. & Igamberdiev, A.U. (2020) Roles for plant mitochondrial alternative oxidase under Normoxia, hypoxia, and Reoxygenation conditions. Frontiers in Plant Science, 11, 566. Available from: https://pubmed.ncbi.nlm.nih.gov/32499803/ [Accessed 12th February 2021]
Jurdak, R., Launay-Avon, A., Paysant-Le Roux, C. & Bailly, C. (2020) Retrograde signaling from the mitochondria to the nucleus translates the positive effect of ethylene on dormancy breaking of Arabidopsis thaliana seeds. The New Phytologist, 229, 2192-2205. Available from: https://pubmed.ncbi.nlm.nih.gov/33020928/ [Accessed 3rd November 2020]
Kambakam, S., Bhattacharjee, U., Petrich, J. & Rodermel, S. (2016) PTOX mediates novel pathways of electron transport in Etioplasts of Arabidopsis. Molecular Plant, 9, 1240-1259. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27353362 [Accessed 29th May 2019]
Kühn, K., Richter, U., Meyer, E.H. et al. (2009) Phage-type RNA polymerase RPOTmp performs gene-specific transcription in mitochondria of Arabidopsis thaliana. Plant Cell, 21, 2762-2779. Available from: http://www.plantcell.org/cgi/doi/10.1105/tpc.109.068536 [Accessed 8th October 2018]
Kühn, K., Yin, G., Duncan, O. et al. (2015) Decreasing electron flux through the cytochrome and/or alternative respiratory pathways triggers common and distinct cellular responses dependent on growth conditions. Plant Physiology, 167, 228-250. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25378695 [Accessed 23rd May 2018]
Lama, S., Broda, M., Abbas, Z., Vaneechoutte, D., Belt, K., Säll, T. et al. (2019) Neofunctionalization of mitochondrial proteins and incorporation into signaling networks in plants M. Purugganan, ed. Molecular Biology and Evolution, 36, 974-989. Available from: http://www.ncbi.nlm.nih.gov/pubmed/30938771 [Accessed 19th July 2019]
Lamattina, L., Gonzalez, D., Gualberto, J. & Grienenberger, J.M. (1993) Higher plant mitochondria encode an homologue of the nuclear-encoded 30-kDa subunit of bovine mitochondrial complex I. European Journal of Biochemistry, 217, 831-838. Available from: http://www.ncbi.nlm.nih.gov/pubmed/8223639 [Accessed 22nd May 2018]
Liebers, M., Grübler, B., Chevalier, F., Lerbs-Mache, S., Merendino, L., Blanvillain, R. et al. (2017) Regulatory shifts in plastid transcription play a key role in morphological conversions of plastids during plant development. Frontiers in Plant Science, 8, 23.
Lohse, M., Bolger, A.M., Nagel, A., Fernie, A.R., Lunn, J.E., Stitt, M. et al. (2012) RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Research, 40, W622-W627. Available from: https://academic.oup.com/nar/article-lookup/doi/10.1093/nar/gks540 [Accessed 18th November 2019]
Marín-Navarro, J., Manuell, A.L., Wu, J. & P. Mayfield, S. (2007) Chloroplast translation regulation. Photosynthesis Research, 94, 359-374. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17661159 [Accessed 19th February 2019]
Martín, G., Leivar, P., Ludevid, D., Tepperman, J.M., Quail, P.H. & Monte, E. (2016) Phytochrome and retrograde signalling pathways converge to antagonistically regulate a light-induced transcriptional network. Nature Communications, 7, 11431. Available from: http://www.nature.com/articles/ncomms11431 [Accessed 11th February 2019]
Mazzella, M.A., Casal, J.J., Muschietti, J.P. & Fox, A.R. (2014) Hormonal networks involved in apical hook development in darkness and their response to light. Frontiers in Plant Science, 5, 52. Available from: http://journal.frontiersin.org/article/10.3389/fpls.2014.00052/abstract [Accessed 22nd May 2018]
Merendino, L., Courtois, F., Grüble, B., Bastien, O., Straetmanns, V., Chevalier, F. et al. (2020) Retrograde signals from mitochondria reprogram skoto-morphogenesis in Arabidopsis thaliana via alternative oxidase 1a. Philosophical Transactions of the Royal Society B, 375, 20190567.
Ng, S., de Clercq, I., van Aken, O., Law, S.R., Ivanova, A., Willems, P. et al. (2014) Anterograde and retrograde regulation of nuclear genes encoding mitochondrial proteins during growth, development, and stress. Molecular Plant, 7, 1075-1093. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24711293 [Accessed 24th January 2019]
Ng, S., Ivanova, A., Duncan, O., Law, S.R., van Aken, O., de Clercq, I. et al. (2013) A membrane-bound NAC transcription factor, ANAC017, mediates mitochondrial retrograde signaling in Arabidopsis. Plant Cell, 25, 3450-3471. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24045017 [Accessed 23rd May 2018]
Pfannschmidt, T., Blanvillain, R., Merendino, L., Courtois, F., Chevalier, F., Liebers, M. et al. (2015) Plastid RNA polymerases: orchestration of enzymes with different evolutionary origins controls chloroplast biogenesis during the plant life cycle. Journal of Experimental Botany, 66, 6957-6973.
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 Molecular Biology, 25, 69-81. Available from: http://www.ncbi.nlm.nih.gov/pubmed/8003698 [Accessed 24th January 2019]
Saeed, A.I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N. et al. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques, 34, 374-378.
Smyth, G.K. (2005) limma: linear models for microarray data. In: Bioinformatics and computational biology solutions using R and bioconductor. New York: Springer-Verlag, pp. 397-420. Available from: http://link.springer.com/10.1007/0-387-29362-0_23 [Accessed 18th November 2019]
Susek, R.E., Ausubel, F.M. & Chory, J. (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell, 74, 787-799. Available from: http://www.ncbi.nlm.nih.gov/pubmed/7690685 [Accessed 18th February 2019]
Tarasenko, V.I., Katyshev, A.I., Yakovleva, T.V., Garnik, E.Y., Chernikova, V.V., Konstantinov, Y.M. et al. (2016) RPOTmp, an Arabidopsis RNA polymerase with dual targeting, plays an important role in mitochondria, but not in chloroplasts. Journal of Experimental Botany, 67, 5657-5669. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27591433 [Accessed 22nd May 2018]
Team, R. (2017) R: a language and environment for statistical computing, Vol. 2016. Vienna: R Foundation for Statistical Computing. Available from: https://www.r-project.org [Accessed 23rd May 2018]
Uhrig, R.G., Labandera, A.-M., Tang, L.-Y., Sieben, N.A., Goudreault, M., Yeung, E. et al. (2017) Activation of mitochondrial protein phosphatase SLP2 by MIA40 regulates seed germination. Plant Physiology, 173, 956-969. Available from: http://www.plantphysiol.org/lookup/doi/10.1104/pp.16.01641 [Accessed 13th November 2019]
van Aken, O., de Clercq, I., Ivanova, A., Law, S.R., van Breusegem, F., Millar, A.H. et al. (2016) Mitochondrial and chloroplast stress responses are modulated in distinct touch and chemical inhibition phases. Plant Physiology, 171, 2150-2165. Available from: http://www.plantphysiol.org/lookup/doi/10.1104/pp.16.00273 [Accessed 23rd May 2018]
van Aken, O., Ford, E., Lister, R., Huang, S. & Millar, A.H. (2016) Retrograde signalling caused by heritable mitochondrial dysfunction is partially mediated by ANAC017 and improves plant performance. The Plant Journal, 88, 542-558. Available from: http://doi.wiley.com/10.1111/tpj.13276 [Accessed 23rd May 2018]
van Aken, O. & Whelan, J. (2012) Comparison of transcriptional changes to chloroplast and mitochondrial perturbations reveals common and specific responses in Arabidopsis. Frontiers in Plant Science, 3, 281. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23269925 [Accessed 11th September 2018]
Vanlerberghe, G. (2013) Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. International Journal of Molecular Sciences, 14, 6805-6847. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23531539 [Accessed 23rd May 2018]
Vishwakarma, A., Bashyam, L., Senthilkumaran, B., Scheibe, R. & Padmasree, K. (2014) Physiological role of AOX1a in photosynthesis and maintenance of cellular redox homeostasis under high light in Arabidopsis thaliana. Plant Physiology and Biochemistry, 81, 44-53. Available from: https://pubmed.ncbi.nlm.nih.gov/24560882/ [Accessed 12th February 2021]
Wang, Y., Berkowitz, O., Selinski, J., Xu, Y., Hartmann, A. & Whelan, J. (2018) Stress responsive mitochondrial proteins in Arabidopsis thaliana. Free Radical Biology & Medicine, 122, 28-39. Available from: https://pubmed.ncbi.nlm.nih.gov/29555593/ [Accessed 8th March 2021]
Wang, Y., Lyu, W., Berkowitz, O., Radomiljac, J.D., Law, S.R., Murcha, M.W. et al. (2016) Inactivation of mitochondrial complex I induces the expression of a twin cysteine protein that targets and affects cytosolic, Chloroplastidic and mitochondrial function. Molecular Plant, 9, 696-710. Available from: http://linkinghub.elsevier.com/retrieve/pii/S1674205216000113 [Accessed 23rd May 2018]
Wang, Y., Selinski, J., Mao, C., Zhu, Y., Berkowitz, O. & Whelan, J. (2020) Linking mitochondrial and chloroplast retrograde signalling in plants. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 375, 20190410. Available from: http://www.ncbi.nlm.nih.gov/pubmed/32362265 [Accessed 9th March 2021]
Woodson, J.D., Perez-Ruiz, J.M. & Chory, J. (2011) Heme synthesis by plastid ferrochelatase I regulates nuclear gene expression in plants. Current Biology, 21, 897-903. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0960982211004209 [Accessed 18th February 2019]
Wu, G.-Z. & Bock, R. GUN control in retrograde signaling: How GENOMES UNCOUPLED proteins adjust nuclear gene expression to plastid biogenesis. Available from: https://academic.oup.com/plcell/pages/General-Instructions [Accessed 13th December 2021]