Abstract
«Genome uncoupled» (gun) is a molecular phenotype manifesting in a high expression of a number of nuclear photosynthesis associated genes in plants with arrested chloroplast biogenesis. The chloroplast biogenesis arrest could be achieved by growing of plants in presence of lincomycin (plastid translation inhibitor) or norflurazon (carotenoid biosynthesis inhibitor). We have found that Arabidopsis thaliana gun1-1gun5-1 double mutant seedlings with gun phenotype associated with both lincomycin and norflurazon demonstrate a repressed root growth when germinated on lincomycin but not norflurazon-containing media. Statistical analysis has demonstrated a high negative correlation between root length and gun phenotype evaluated on both LHCB1.2 and HEMA1 genes expression in three gun mutants of Arabidopsis: gun1-1, cch1-1 and the double mutant gun1-1gun5-1. Our results demonstrate that regulatory signals of plastid origin might participate in root development.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Brunkard JO, Burch-Smith TM (2018) Ties that bind: the integration of plastid signalling pathways in plant cell metabolism. Essays Biochem 62(1):95–107. https://doi.org/10.1042/EBC20170011
Chi W, Sun X, Zhang L (2013) Intracellular signaling from plastid to nucleus. Annu Rev Plant Biol 64:559–582. https://doi.org/10.1146/annurev-arplant-050312-120147
Colombo M, Tadini L, Peracchio C, Ferrari R, Pesaresi P (2016) GUN1, a Jack-of-all-trades in chloroplast protein homeostasis and signaling. Front Plant Sci 7:1427. https://doi.org/10.3389/fpls.2016.01427
Cottage A, Mott EK, Kempster JA, Gray JC (2010) The Arabidopsis plastid-signalling mutant gun1 (genomes uncoupled1) shows altered sensitivity to sucrose and abscisic acid and alterations in early seedling development. J Exp Bot 61(13):3773–3786. https://doi.org/10.1093/jxb/erq186
Du SY, Zhang XF, Lu Z, Xin Q, Wu Z, Jiang T, Lu Y, Wang XF, Zhang DP (2012) Roles of the different components of magnesium chelatase in abscisic acid signal transduction. Plant Mol Biol 80:519–537. https://doi.org/10.1007/s11103-012-9965-3
Hernandez-Verdeja T, Strand A (2018) Retrograde signals navigate the path to chloroplast development. Plant Physiol 176(2):967–976. https://doi.org/10.1104/pp.17.01299
Hong SM, Bahn SC, Lyu A, Jung HS, Ahn JH (2010) Identification and testing of superior reference genes for a starting pool of transcript normalization in Arabidopsis. Plant Cell Physiol 51:1694–1706. https://doi.org/10.1093/pcp/pcq128
Kacprzak SM, Mochizuki N, Naranjo B, Xu D, Leister D, Kleine T, Okamoto H, Terry MJ (2019) Plastid-to-nucleus retrograde signalling during chloroplast biogenesis does not require ABI41. Plant Physiol 179(1):18–23
Kim C, Apel K (2013) 1O2-mediated and EXECUTER-dependent retrograde plastid-to-nucleus signaling in norflurazon-treated seedlings of Arabidopsis thaliana. Mol Plant 6(5):1580–1591. https://doi.org/10.1093/mp/sst020
Kobayashi K, Baba S, Obayashi T, Sato M, Toyooka K, Keranen 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
Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316(5825):715–719. https://doi.org/10.1126/science.1140516
Larkin RM (2016) Tetrapyrrole signaling in plants. Front Plant Sci 7:1586. https://doi.org/10.3389/fpls.2016.01586
Larkin RM, Alonso JM, Ecker JR, Chory J (2003) GUN4, a regulator of chlorophyll synthesis and intracellular signaling. Science 299(5608):902–906. https://doi.org/10.1126/science.1079978
Leister D, Kleine T (2016) Definition of a core module for the nuclear retrograde response to altered organellar gene expression identifies GLK overexpressors as gun mutants. Physiol Plant 157(3):297–309. https://doi.org/10.1111/ppl.12431
Liao JC, Hsieh WY, Tseng CC, Hsienh MH (2016) Dysfunctional chloroplasts up-regulate the expression of mitochondrial genes in Arabidopsis seedlings. Photosynth Res 127(2):151–159. https://doi.org/10.1007/s11120-015-0161-6
McCormac AC, Terry MJ (2004) The nuclear genes LHCB and HEMA1 are differentially sensitive to plastid signals and suggest distinct roles for the GUN1 and GUN5 plastid-signalling pathways during de-etiolation. Plant J 40(5):672–685. https://doi.org/10.1111/j.1365-313X.2004.02243.x
Mochizuki N, Susek R, Chory J (1996) An intracellular signal transduction pathway between the chloroplast and nucleus is involved in de-etiolation. Plant Physiol 112(4):1465–1469
Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J (2001) Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc Natl Acad Sci USA 98(4):2053–2058. https://doi.org/10.1073/pnas.98.4.2053
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15(3):473–497
Page MT, Kacprzak SM, Mochizuki N, Okamoto H, Smith AG, Terry MJ (2017) Seedlings lacking the PTM protein do not show a genomes uncoupled (gun) mutant phenotype. Plant Physiol 174(1):21–26. https://doi.org/10.1104/pp.16.01930
Pattanayak GK, Tripathy BC (2016) Modulation of biosynthesis of photosynthetic pigments and light-harvesting complex in wild-type and gun5 mutant of Arabidopsis thaliana during impaired chloroplast development. Protoplasma 253(3):747–752. https://doi.org/10.1007/s00709-016-0958-y
Pesaresi P, Kim C (2019) Current understanding of GUN1: a key mediator involved in biogenic retrograde signaling. Plant Cell Rep 38(7):819–823. https://doi.org/10.1007/s00299-019-02383-4
Song L, Chen Z, Larkin RM (2018) The genomes uncoupled mutants are more sensitive to norflurazon than wild type. Plant Physiol 178(3):965–971. https://doi.org/10.1104/pp.18.00982
Sun X, Feng P, Guo H, Ma J, Chi W, Lin R, Lu C, Zhang L (2011) A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus. Nat Commun 2:477. https://doi.org/10.1038/ncomms1486
Susek RE, Ausbel FM, Chory J (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74(5):787–799
Teng S, Keurentjes J, Bentsink L, Koornneef M, Smeekens S (2005) Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene. Plant Physiol 139(4):1840–1852. https://doi.org/10.1104/pp.105.066688
Wang J, Xia H, Zhao SZ, Hou L, Zhao CZ, Ma CL, Wang XJ, Li PC (2018) A role of GUNs-involved retrograde signaling in regulating acetyl-CoA carboxylase 2 in Arabidopsis. Biochem Biophys Res Commun 505(3):712–719. https://doi.org/10.1016/j.bbrc.2018.09.144
Woodson JD, Perez-Ruiz JM, Chory J (2011) Heme synthesis by plastid ferrochelatase i regulates nuclear gene expression in plants. Curr Biol 21(10):897–903. https://doi.org/10.1016/j.cub.2011.04.004
Woodson JD, Perez-Ruiz JM, Schmitz RJ, Ecker JR, Chory J (2013) Sigma factor-mediated plastid retrograde signals control nuclear gene expression. Plant J 73(1):1–13. https://doi.org/10.1111/tpj.12011
Wu GZ, Meyer EH, Wu S, Bock R (2019) Extensive post-transcriptional regulation of nuclear gene expression by plastid retrograde signals. Plant Physiol. https://doi.org/10.1104/pp.19.00421
Zhang DP (2007) Signaling to the nucleus with a loaded GUN. Science 316(5825):700–701. https://doi.org/10.1126/science.1142703
Zhang ZW, Zhang GC, Zhu F, Zhang DW, Yuan S (2015) The roles of tetrapyrroles in plastid retrograde signaling and tolerance to environmental stresses. Planta 242(6):1263–1276. https://doi.org/10.1007/s00425-015-2384-3
Zhao X, Huang J, Chory J (2018) Genome uncoupled1 mutants are hypersensitive to norflurazon and lincomycin. Plant Physiol 178(3):960–964
Acknowledgements
The authors are grateful to Assistant Professor in Kyoto University, Nobuyoshi Mochizuki for providing us with seeds of gun1-1 and gun1-1gun5-1 mutants. This work was financially supported by RAS Project VI.56.1.3. Equipment of the Bioanalitika Center for Collective Use, Siberian Institute of Plant Physiology and Biochemistry, Siberian Branch of the Russian Academy of Sciences, Irkutsk, was used in this study.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Garnik, E.Y., Tarasenko, V.I., Gorbunova, A.I. et al. Genome uncoupled (gun) phenotype is associated with root growth repression in Arabidopsis seedlings grown on lincomycin. Theor. Exp. Plant Physiol. 31, 445–454 (2019). https://doi.org/10.1007/s40626-019-00157-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40626-019-00157-7