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• W3048776995 startingPage "108019" @default.
• W3048776995 abstract "•Plastid genome instability alters endoreplication and cell cycle•Plastid genome instability results in increased expression of cell-cycle-related genes•SOG1 mediates the activation of cell-cycle-related genes by plastid genome instability•ROS is required for communication of plastid genome with endoreplication and cell cycle Plastid-nucleus genome coordination is crucial for plastid activity, but the mechanisms remain unclear. By treating Arabidopsis plants with the organellar genome-damaging agent ciprofloxacin, we found that plastid genome instability can alter endoreplication and the cell cycle. Similar results are observed in the plastid genome instability mutants of reca1why1why3. Cell division and embryo development are disturbed in the reca1why1why3 mutant. Notably, SMR5 and SMR7 genes, which encode cell-cycle kinase inhibitors, are upregulated in plastid genome instability plants, and the mutation of SMR7 can restore the endoreplication and growth phenotype of reca1why1why3 plants. Furthermore, we establish that the DNA damage response transcription factor SOG1 mediates the alteration of endoreplication and cell cycle triggered by plastid genome instability. Finally, we demonstrate that reactive oxygen species produced in plastids are important for plastid-nucleus genome coordination. Our findings uncover a molecular mechanism for the coordination of plastid and nuclear genomes during plant growth and development. Plastid-nucleus genome coordination is crucial for plastid activity, but the mechanisms remain unclear. By treating Arabidopsis plants with the organellar genome-damaging agent ciprofloxacin, we found that plastid genome instability can alter endoreplication and the cell cycle. Similar results are observed in the plastid genome instability mutants of reca1why1why3. Cell division and embryo development are disturbed in the reca1why1why3 mutant. Notably, SMR5 and SMR7 genes, which encode cell-cycle kinase inhibitors, are upregulated in plastid genome instability plants, and the mutation of SMR7 can restore the endoreplication and growth phenotype of reca1why1why3 plants. Furthermore, we establish that the DNA damage response transcription factor SOG1 mediates the alteration of endoreplication and cell cycle triggered by plastid genome instability. Finally, we demonstrate that reactive oxygen species produced in plastids are important for plastid-nucleus genome coordination. Our findings uncover a molecular mechanism for the coordination of plastid and nuclear genomes during plant growth and development. Proper genome function depends on the maintenance of genome integrity (Aguilera and García-Muse, 2013Aguilera A. García-Muse T. Causes of genome instability.Annu. Rev. Genet. 2013; 47: 1-32Crossref PubMed Scopus (301) Google Scholar). Plant plastids are semi-autonomous organelles containing their own genomes, encoding several proteins that are necessary for the formation of functional photosynthetic and metabolic complexes (Green, 2011Green B.R. Chloroplast genomes of photosynthetic eukaryotes.Plant J. 2011; 66: 34-44Crossref PubMed Scopus (234) Google Scholar). Plastid genome stability is vital for plastid function and, consequently, plant growth and development (Kimura and Sakaguchi, 2006Kimura S. Sakaguchi K. DNA repair in plants.Chem. Rev. 2006; 106: 753-766Crossref PubMed Scopus (129) Google Scholar; Oldenburg and Bendich, 2015Oldenburg D.J. Bendich A.J. DNA maintenance in plastids and mitochondria of plants.Front. Plant Sci. 2015; 6: 883Crossref PubMed Scopus (92) Google Scholar). However, plastids are extremely sensitive to certain environmental conditions and stimuli that can damage their genome stability; in particular, double-strand breaks (DSBs) are considered the most threatening to genome instability. Spontaneously, the plastid genome-damaging agent ciprofloxacin (CIP) is a gyrase inhibitor that can also produce organellar DSBs (Evans-Roberts et al., 2016Evans-Roberts K.M. Mitchenall L.A. Wall M.K. Leroux J. Mylne J.S. Maxwell A. DNA Gyrase Is the Target for the Quinolone Drug Ciprofloxacin in Arabidopsis thaliana.J. Biol. Chem. 2016; 291: 3136-3144Abstract Full Text Full Text PDF PubMed Scopus (43) Google Scholar), which induce severe plastid DNA (ptDNA) rearrangements if improperly repaired (Odom et al., 2008Odom O.W. Baek K.H. Dani R.N. Herrin D.L. Chlamydomonas chloroplasts can use short dispersed repeats and multiple pathways to repair a double-strand break in the genome.Plant J. 2008; 53: 842-853Crossref PubMed Scopus (30) Google Scholar). However, our understanding of how plants maintain plastid genome stability is limited. Several factors involved in the maintenance of plastid genome stability have been identified in Arabidopsis thaliana: the single-stranded DNA-binding proteins WHIRLY (WHY) 1 and WHY3 are targeted to plastids and protect the plastid genome against rearrangements (Maréchal et al., 2009Maréchal A. Parent J.S. Véronneau-Lafortune F. Joyeux A. Lang B.F. Brisson N. Whirly proteins maintain plastid genome stability in Arabidopsis.Proc. Natl. Acad. Sci. USA. 2009; 106: 14693-14698Crossref PubMed Scopus (145) Google Scholar); chloroplast RECA1 is key for homologous recombination (HR) and maintenance of structural integrity of the plastid genome (Rowan et al., 2010Rowan B.A. Oldenburg D.J. Bendich A.J. RecA maintains the integrity of chloroplast DNA molecules in Arabidopsis.J. Exp. Bot. 2010; 61: 2575-2588Crossref PubMed Scopus (79) Google Scholar); and the type I polymerases, PolIB, perform ptDNA replication and repair in Arabidopsis (Parent et al., 2011Parent J.S. Lepage E. Brisson N. Divergent roles for the two PolI-like organelle DNA polymerases of Arabidopsis.Plant Physiol. 2011; 156: 254-262Crossref PubMed Scopus (78) Google Scholar). The plastid genome instability in the Arabidopsis polibwhy1why3 triple mutant leads to the generation of reactive oxygen species (ROS) and induces stress-related nuclear genetic reprogramming, which correlates with yellow-variegated leaves and environmental stress adaption (Lepage et al., 2013Lepage É. Zampini É. Brisson N. Plastid genome instability leads to reactive oxygen species production and plastid-to-nucleus retrograde signaling in Arabidopsis.Plant Physiol. 2013; 163: 867-881Crossref PubMed Scopus (40) Google Scholar). The reca1why1why3 triple mutant, which is characterized by white variegation and a severe growth-retardation phenotype, accumulates much more short-range ptDNA rearrangements than the wild type (WT), leading to plastid genomic instability (Zampini et al., 2015Zampini É. Lepage É. Tremblay-Belzile S. Truche S. Brisson N. Organelle DNA rearrangement mapping reveals U-turn-like inversions as a major source of genomic instability in Arabidopsis and humans.Genome Res. 2015; 25: 645-654Crossref PubMed Scopus (34) Google Scholar), but the relationship between plastid genomic instability and plant growth remains unclear. More than 95% of plastid proteins are encoded by the nuclear genome (Green, 2011Green B.R. Chloroplast genomes of photosynthetic eukaryotes.Plant J. 2011; 66: 34-44Crossref PubMed Scopus (234) Google Scholar), which contains all of the genetic information required for plastid function and plant survival (Woodson and Chory, 2008Woodson J.D. Chory J. Coordination of gene expression between organellar and nuclear genomes.Nat. Rev. Genet. 2008; 9: 383-395Crossref PubMed Scopus (473) Google Scholar). The maintenance of nuclear genome integrity is fundamental for nuclear genome function. However, genome instability may result from failures at different steps of the DNA cycle (from replication to segregation) and failed or improper repair of DNA damage (Aguilera and García-Muse, 2013Aguilera A. García-Muse T. Causes of genome instability.Annu. Rev. Genet. 2013; 47: 1-32Crossref PubMed Scopus (301) Google Scholar; Sanchez et al., 2012Sanchez M.D. Costas C. Sequeira-Mendes J. Gutierrez C. Regulating DNA Replication in Plants.Csh Perspect Biol. 2012; 4: 12Google Scholar). Plants have developed an elaborate regulatory mechanism to ensure the integrity of the nuclear genome, which is required for normal growth and development (Hu et al., 2016Hu Z. Cools T. De Veylder L. Mechanisms Used by Plants to Cope with DNA Damage.Annu. Rev. Plant Biol. 2016; 67: 439-462Crossref PubMed Scopus (152) Google Scholar). Accurate control of the cell-cycle phases (G1, S, G2, and mitotic [M] phases) and critical checkpoints at G1/S, G2/M phase transition points, and metaphase (spindle assembly checkpoint [SAC]) are important for ensuring that cell division generates two identical daughter cells (De Veylder et al., 2003De Veylder L. Joubès J. Inzé D. Plant cell cycle transitions.Curr. Opin. Plant Biol. 2003; 6: 536-543Crossref PubMed Scopus (136) Google Scholar; Inzé and De Veylder, 2006Inzé D. De Veylder L. Cell cycle regulation in plant development.Annu. Rev. Genet. 2006; 40: 77-105Crossref PubMed Scopus (620) Google Scholar). The checkpoint at the G1/S transition ensures that sufficiently raw materials are available for the completion of DNA replication, while the G2/M transition checkpoint ensures that cells do not initiate mitosis before repairing damaged DNA, and the SAC ensures the equal segregation of chromosomes to the daughter cells (De Veylder et al., 2003De Veylder L. Joubès J. Inzé D. Plant cell cycle transitions.Curr. Opin. Plant Biol. 2003; 6: 536-543Crossref PubMed Scopus (136) Google Scholar; Inzé and De Veylder, 2006Inzé D. De Veylder L. Cell cycle regulation in plant development.Annu. Rev. Genet. 2006; 40: 77-105Crossref PubMed Scopus (620) Google Scholar). Cell-cycle progression is driven by conserved heterodimeric kinases, comprising regulatory cyclin subunits and catalytic cyclin-dependent kinase (CDK) subunits; these heterodimeric kinases are known as CDK-cyclin complexes. Plants possess different classes of CDKs and cyclins to regulate the transition from one cell-cycle phase to the next (De Veylder et al., 2003De Veylder L. Joubès J. Inzé D. Plant cell cycle transitions.Curr. Opin. Plant Biol. 2003; 6: 536-543Crossref PubMed Scopus (136) Google Scholar; Inzé and De Veylder, 2006Inzé D. De Veylder L. Cell cycle regulation in plant development.Annu. Rev. Genet. 2006; 40: 77-105Crossref PubMed Scopus (620) Google Scholar). For example, A-type cyclins (CYCA) and B-type cyclins (CYCB) have a function during G1/M and G2/M phase transitions, respectively (Inzé and De Veylder, 2006Inzé D. De Veylder L. Cell cycle regulation in plant development.Annu. Rev. Genet. 2006; 40: 77-105Crossref PubMed Scopus (620) Google Scholar; Gutierrez, 2009Gutierrez C. The Arabidopsis cell division cycle.Arabidopsis Book. 2009; 7: e0120Crossref PubMed Google Scholar; Boruc et al., 2010Boruc J. Van den Daele H. Hollunder J. Rombauts S. Mylle E. Hilson P. Inzé D. De Veylder L. Russinova E. Functional modules in the Arabidopsis core cell cycle binary protein-protein interaction network.Plant Cell. 2010; 22: 1264-1280Crossref PubMed Scopus (128) Google Scholar). Exogenous environmental factors and endogenous metabolic processes damage plant genome DNA and can lead to genomic instability. Plants have evolved a DNA damage response mechanism when DNA strands break to ensure genome integrity (Aguilera and García-Muse, 2013Aguilera A. García-Muse T. Causes of genome instability.Annu. Rev. Genet. 2013; 47: 1-32Crossref PubMed Scopus (301) Google Scholar; Hu et al., 2016Hu Z. Cools T. De Veylder L. Mechanisms Used by Plants to Cope with DNA Damage.Annu. Rev. Plant Biol. 2016; 67: 439-462Crossref PubMed Scopus (152) Google Scholar). When DNA damage is beyond repair, plants initiate cell death to avoid transmitting damaged DNA to the next generation. However, if DNA damage is minimal, then plants activate cell-cycle arrest, endoreplication, and DNA damage repair to ensure genome integrity. Cell-cycle arrest at the main surveillance checkpoints, G1/S and G2/M, allows cells to take action to tackle DNA damage (Hu et al., 2016Hu Z. Cools T. De Veylder L. Mechanisms Used by Plants to Cope with DNA Damage.Annu. Rev. Plant Biol. 2016; 67: 439-462Crossref PubMed Scopus (152) Google Scholar). During endoreplication, DNA replication continues without cell division to ensure plant survival (De Veylder et al., 2011De Veylder L. Larkin J.C. Schnittger A. Molecular control and function of endoreplication in development and physiology.Trends Plant Sci. 2011; 16: 624-634Abstract Full Text Full Text PDF PubMed Scopus (224) Google Scholar; Breuer et al., 2014Breuer C. Braidwood L. Sugimoto K. Endocycling in the path of plant development.Curr. Opin. Plant Biol. 2014; 17: 78-85Crossref PubMed Scopus (48) Google Scholar). DNA repair mechanisms include mismatch repair, excision repair, and repair of DSBs via HR and nonhomologous end joining (NHEJ), and various DSB repair mechanisms have been reported in plants (Hu et al., 2016Hu Z. Cools T. De Veylder L. Mechanisms Used by Plants to Cope with DNA Damage.Annu. Rev. Plant Biol. 2016; 67: 439-462Crossref PubMed Scopus (152) Google Scholar). A set of specific proteins regulate the cell cycle in response to DNA damage. For example, the NAC domain family transcription factor SOG1, a plant functional analog of animal p53, controls the expression of genes responsible for cell-cycle regulation, including cell-cycle inhibition and DNA damage responses (Ogita et al., 2018Ogita N. Okushima Y. Tokizawa M. Yamamoto Y.Y. Tanaka M. Seki M. Makita Y. Matsui M. Okamoto-Yoshiyama K. Sakamoto T. et al.Identifying the target genes of SUPPRESSOR OF GAMMA RESPONSE 1, a master transcription factor controlling DNA damage response in Arabidopsis.Plant J. 2018; 94: 439-453Crossref PubMed Scopus (74) Google Scholar; Yoshiyama et al., 2009Yoshiyama K. Conklin P.A. Huefner N.D. Britt A.B. Suppressor of gamma response 1 (SOG1) encodes a putative transcription factor governing multiple responses to DNA damage.Proc. Natl. Acad. Sci. USA. 2009; 106: 12843-12848Crossref PubMed Scopus (179) Google Scholar, Yoshiyama, 2016Yoshiyama K.O. SOG1: a master regulator of the DNA damage response in plants.Genes Genet. Syst. 2016; 90: 209-216Crossref PubMed Scopus (48) Google Scholar, Yoshiyama et al., 2017Yoshiyama K.O. Kaminoyama K. Sakamoto T. Kimura S. Increased Phosphorylation of Ser-Gln Sites on SUPPRESSOR OF GAMMA RESPONSE1 Strengthens the DNA Damage Response in Arabidopsis thaliana.Plant Cell. 2017; 29: 3255-3268Crossref PubMed Scopus (29) Google Scholar). The activated SOG1 directly or indirectly regulates hundreds of genes and induces a broad cascade of transcriptional responses, which control cell-cycle regulation, endoreplication, DNA repair, and cell death to ensure genome integrity (Yoshiyama et al., 2017Yoshiyama K.O. Kaminoyama K. Sakamoto T. Kimura S. Increased Phosphorylation of Ser-Gln Sites on SUPPRESSOR OF GAMMA RESPONSE1 Strengthens the DNA Damage Response in Arabidopsis thaliana.Plant Cell. 2017; 29: 3255-3268Crossref PubMed Scopus (29) Google Scholar; Adachi et al., 2011Adachi S. Minamisawa K. Okushima Y. Inagaki S. Yoshiyama K. Kondou Y. Kaminuma E. Kawashima M. Toyoda T. Matsui M. et al.Programmed induction of endoreduplication by DNA double-strand breaks in Arabidopsis.Proc. Natl. Acad. Sci. USA. 2011; 108: 10004-10009Crossref PubMed Scopus (194) Google Scholar). Given the endosymbiotic origins of plastids, the coordination of nuclear and plastid genomes is essential for ensuring eukaryotic cell integrity (Kobayashi et al., 2009Kobayashi Y. Kanesaki Y. Tanaka A. Kuroiwa H. Kuroiwa T. Tanaka K. Tetrapyrrole signal as a cell-cycle coordinator from organelle to nuclear DNA replication in plant cells.Proc. Natl. Acad. Sci. USA. 2009; 106: 803-807Crossref PubMed Scopus (96) Google Scholar). Research into both anterograde (nucleus to plastid) and retrograde (plastid to nucleus) genome communication mechanisms has focused on the coordination of gene expression between nuclear and plastid genomes, which is important for plastid function and plant growth and survival (Woodson and Chory, 2008Woodson J.D. Chory J. Coordination of gene expression between organellar and nuclear genomes.Nat. Rev. Genet. 2008; 9: 383-395Crossref PubMed Scopus (473) Google Scholar; Chan et al., 2016Chan K.X. Phua S.Y. Crisp P. McQuinn R. Pogson B.J. Learning the Languages of the Chloroplast: Retrograde Signaling and Beyond.Annu. Rev. Plant Biol. 2016; 67: 25-53Crossref PubMed Scopus (334) Google Scholar). A relatively constant nuclear:plastid genome ratio is required for normal plant growth and development, so coordination of the genome state between the nucleus and plastids is required for plant survival (Golczyk et al., 2014Golczyk H. Greiner S. Wanner G. Weihe A. Bock R. Börner T. Herrmann R.G. Chloroplast DNA in mature and senescing leaves: a reappraisal.Plant Cell. 2014; 26: 847-854Crossref PubMed Scopus (41) Google Scholar; Li et al., 2006Li W. Ruf S. Bock R. Constancy of organellar genome copy numbers during leaf development and senescence in higher plants.Mol. Genet. Genomics. 2006; 275: 185-192Crossref PubMed Scopus (46) Google Scholar). However, how plants coordinate the genome-stability state between plastids and the nucleus remains unknown. In this study, we explored the relationship between the state of the plastid and nuclear genomes. We found that plastid genome instability affects the status of the nuclear genome mediated by SOG1 through activating genes involved in enhancing endoreplication and cell-cycle regulation. We further revealed that plastid-nucleus genome communication involves increased ROS, thus controlling plant growth and development. To explore the relationship of genome status between plastid and nucleus, we introduce two plastid genome-damaging agents, including novobiocin (NOV), a gyrase inhibitor that does not induce DNA breaks or ptDNA rearrangements (Hardy and Cozzarelli, 2003Hardy C.D. Cozzarelli N.R. Alteration of Escherichia coli topoisomerase IV to novobiocin resistance.Antimicrob. Agents Chemother. 2003; 47: 941-947Crossref PubMed Scopus (52) Google Scholar), and CIP, another gyrase inhibitor that produces organellar DSBs, which induce severe ptDNA rearrangements (Evans-Roberts et al., 2016Evans-Roberts K.M. Mitchenall L.A. Wall M.K. Leroux J. Mylne J.S. Maxwell A. DNA Gyrase Is the Target for the Quinolone Drug Ciprofloxacin in Arabidopsis thaliana.J. Biol. Chem. 2016; 291: 3136-3144Abstract Full Text Full Text PDF PubMed Scopus (43) Google Scholar), leading to plastid genome instability (Figure 1A). DNA content is a key characteristic for endoreplication (Breuer et al., 2014Breuer C. Braidwood L. Sugimoto K. Endocycling in the path of plant development.Curr. Opin. Plant Biol. 2014; 17: 78-85Crossref PubMed Scopus (48) Google Scholar; De Veylder et al., 2011De Veylder L. Larkin J.C. Schnittger A. Molecular control and function of endoreplication in development and physiology.Trends Plant Sci. 2011; 16: 624-634Abstract Full Text Full Text PDF PubMed Scopus (224) Google Scholar), and the expression of the cell-cycle marker gene CYCB1;1 is important to the cell cycle in plants (Hemerly et al., 1992Hemerly A. Bergounioux C. Van Montagu M. Inzé D. Ferreira P. Genes regulating the plant cell cycle: isolation of a mitotic-like cyclin from Arabidopsis thaliana.Proc. Natl. Acad. Sci. USA. 1992; 89: 3295-3299Crossref PubMed Scopus (141) Google Scholar; Shultz et al., 2009Shultz R.W. Lee T.J. Allen G.C. Thompson W.F. Hanley-Bowdoin L. Dynamic localization of the DNA replication proteins MCM5 and MCM7 in plants.Plant Physiol. 2009; 150: 658-669Crossref PubMed Scopus (40) Google Scholar). We treated WT plants with different concentrations of NOV, then measured the nuclear DNA content (C value). The results showed that plants did not exhibit an obvious alteration of nuclear DNA content (Figures 1B, 1C, S1A, and S1B). Furthermore, we monitored the expression of CYCB1;1 in NOV-treated plants, and the results showed that the expression of CYCB1;1 is also not affected (Figure 1D). When plants were treated with CIP of different concentrations, we found that the cell ploidy enhanced gradually with the increase in CIP concentration (Figures 1B, 1C, S1C, and S1D); especially when the concentration of CIP is 0.75 and 1 μM, these plants displayed decreased 2C and 4C DNA content, increased 8C and 16C DNA content, and even a 32C nuclear DNA content. Moreover, the alteration of cell ploidy of 1 μM is more significant (Figures 1E and 1F). The expression of CYCB1;1 in a 1-μM CIP-treated plant is also significantly upregulated (Figure 1G). These results suggest that plastid genome instability with severe ptDNA rearrangements modulates endoreplication and cell-cycle progression in plants. To ensure the effect of plastid genome instability on endoreplication and cell-cycle progression, we used the Arabidopsis triple mutant reca1why1why3, which also accumulates many more short-range ptDNA rearrangements, which exhibit plastid genome instability, to further evaluate the results obtained in CIP-treated plants (Zampini et al., 2015Zampini É. Lepage É. Tremblay-Belzile S. Truche S. Brisson N. Organelle DNA rearrangement mapping reveals U-turn-like inversions as a major source of genomic instability in Arabidopsis and humans.Genome Res. 2015; 25: 645-654Crossref PubMed Scopus (34) Google Scholar; Figure 2A). We used five pairs of primers to examine ptDNA rearrangements and a next-generation sequencing approach (Figure S2), referencing the previous report (Zampini et al., 2015Zampini É. Lepage É. Tremblay-Belzile S. Truche S. Brisson N. Organelle DNA rearrangement mapping reveals U-turn-like inversions as a major source of genomic instability in Arabidopsis and humans.Genome Res. 2015; 25: 645-654Crossref PubMed Scopus (34) Google Scholar), to ensure ptDNA instability in the reca1why1why3 mutant. We found that nuclear DNA content in reca1why1why3 mutants was similar to that in 1-μM CIP-treated plants (Figures 1E, 1F, 2B, and 2C) and that the expression of CYCB1;1 is also significantly increased (Figure 2D). These results further ensured that plastid genome instability has an effect on endoreplication and cell-cycle progression. The onset of endoreplication could be activated either by inherent developmental signals or DNA stress mostly caused by genotoxic drugs (Fox and Duronio, 2013Fox D.T. Duronio R.J. Endoreplication and polyploidy: insights into development and disease.Development. 2013; 140: 3-12Crossref PubMed Scopus (233) Google Scholar). However, under DNA stress conditions, cells induce DNA damage responses, which contain the activation of endoreplication to maintain the integrity of the nuclear genome (Hu et al., 2016Hu Z. Cools T. De Veylder L. Mechanisms Used by Plants to Cope with DNA Damage.Annu. Rev. Plant Biol. 2016; 67: 439-462Crossref PubMed Scopus (152) Google Scholar). To determine whether the DNA damage responses occurred in the reca1why1why3 mutant, first, we ran the alkaline comet assay to examine nuclear DNA strand breaks in reca1why1why3 mutants; the H2O2-treated plants were used as a control. There were no differences between the plastid genome instability plants and WT plants in this assay (Figure 2E), suggesting that there is no obvious DNA strand break in the reca1why1why3 mutant. Second, we monitored the expression of several genes involved in various DNA repair pathways, including NHEJ (Ku70, PARP2C, and XRCC4) and HR (RAD51 and BRCA1) (Kimura and Sakaguchi, 2006Kimura S. Sakaguchi K. DNA repair in plants.Chem. Rev. 2006; 106: 753-766Crossref PubMed Scopus (129) Google Scholar). There was almost no difference in the expression of these genes between mutants and WT plants (Figure 2F). Third, trypan blue staining to detect cell death in leaves showed no differences between mutants and WT plants (Figure 2G). These results suggest that the plastid genome instability does not directly damage nuclear DNA and trigger DNA repair, as well as cell death; instead, it affects nuclear genome status by disturbing endoreplication and cell-cycle progression. To explore how plastid genome instability modulates the endoreplication and cell cycle, we analyzed the growth and development of the reca1why1why3 mutants. The mutants display a dwarf phenotype; the average leaf size in reca1why1why3 mutants was 3.01-fold smaller than that in WT plants (Figures 3A and 3C ). However, the average leaf epidermal cell area was 1.46-fold larger in the reca1why1why3 mutants compared with that in the WT (Figures 3B and 3D). This suggested that cell division was severely inhibited in reca1why1why3 plants. In Arabidopsis, several cell-cycle-related mutants exhibit defective embryo development, even causing embryo lethality and reduced silique fertility (Domenichini et al., 2012Domenichini S. Benhamed M. De Jaeger G. Van De Slijke E. Blanchet S. Bourge M. De Veylder L. Bergounioux C. Raynaud C. Evidence for a role of Arabidopsis CDT1 proteins in gametophyte development and maintenance of genome integrity.Plant Cell. 2012; 24: 2779-2791Crossref PubMed Scopus (21) Google Scholar; Ni et al., 2009Ni D.A. Sozzani R. Blanchet S. Domenichini S. Reuzeau C. Cella R. Bergounioux C. Raynaud C. The Arabidopsis MCM2 gene is essential to embryo development and its over-expression alters root meristem function.New Phytol. 2009; 184: 311-322Crossref PubMed Scopus (42) Google Scholar). At the reproductive stage, reca1why1why3 mutant siliques contained a large number of white ovules, in contrast to the green ovules of the WT (Figure 3E). We examined ovule development and found that reca1why1why3 mutant embryos displayed an abnormal shape at the late heart stage and late torpedo stage compared with the WT embryo (Figure 3F). Moreover, mutant plants exhibited lower fertility than WT plants, with significantly fewer seeds per silique in the mutant (mean value of 26.0) than in the WT (mean value of 48.7) (Figure 3G). In addition, the 1,000-grain weight was lower in reca1why1why3 than that in WT plants (Figure 3H). These results indicate that embryo development is disturbed in reca1why1why3 mutants. In all, abnormal development of leaves and embryos in the reca1why1why3 mutant was likely caused by defects in cell division and the cell cycle, which further supported that plastid genome instability modulates endoreplication and cell-cycle progression. To understand the molecular mechanisms underlying the endoreplication and cell-cycle progression in plastid genome instability plants, we performed reverse-transcriptase-quantitative PCR (RT-qPCR) to determine the expression levels of cell-cycle-related marker genes during different phases: G1 (CYCD3;3 and SMR6), G1/S (KRP2, E2FA, and FBL17), S (CYCD3;1, CYCD5;1, CDT1A, ASF1a, ASF1b, and ETG1), S/G2 (CYCA2;1 and WEE1), and G2/M (SMR5, SMR7, CCS52A1, and CCS52A2) (Boruc et al., 2010Boruc J. Van den Daele H. Hollunder J. Rombauts S. Mylle E. Hilson P. Inzé D. De Veylder L. Russinova E. Functional modules in the Arabidopsis core cell cycle binary protein-protein interaction network.Plant Cell. 2010; 22: 1264-1280Crossref PubMed Scopus (128) Google Scholar; Gutierrez, 2009Gutierrez C. The Arabidopsis cell division cycle.Arabidopsis Book. 2009; 7: e0120Crossref PubMed Google Scholar). Transcript levels of the SIAMESE-RELATED kinase inhibitors SMR5 and SMR7 were significantly increased in reca1why1why3 mutants and CIP-treated plants (Figure 4A). Genes associated with other phases were not obviously altered (Figures S3A and S3B). These results suggested that the alteration of cell-cycle progression in plastid genome instability plants is probably due to the increased expression of cell-cycle genes. To further determine the function of these altered cell-cycle-related genes in plastid genome instability plants, we crossed the cell-cycle gene mutant of smr7 with the reca1why1why3 mutant and obtained the quadruple mutant smr7reca1why1why3 (Figures 4B, 4C, and S3C). The growth phenotype of the quadruple mutants was partially recovered to that of the WT plants (Figures 4B and 4C). The obvious 32C nuclear DNA content was not seen in these quadruple mutants, and the DNA content recovered to the WT-like pattern in these quadruple mutants (Figures 4D and 4E). These results suggest that high expression levels of SMR5 and SMR7 are responsible for enhanced endoreplication and cell-cycle progression, as well as plant development in plastid genome instability mutants. To verify the relationship of the endoreplication and cell cycle with plastid genome-stability factors, we examined the expression of cell-cycle-related marker genes and endoreplication in reca1-1, why1, and why3 single mutants (Maréchal et al., 2009Maréchal A. Parent J.S. Véronneau-Lafortune F. Joyeux A. Lang B.F. Brisson N. Whirly proteins maintain plastid genome stability in Arabidopsis.Proc. Natl. Acad. Sci. USA. 2009; 106: 14693-14698Crossref PubMed Scopus (145) Google Scholar; Rowan et al., 2010Rowan B.A. Oldenburg D.J. Bendich A.J. RecA maintains the integrity of chloroplast DNA molecules in Arabidopsis.J. Exp. Bot. 2010; 61: 2575-2588Crossref PubMed Scopus (79) Google Scholar). There were no significant differences in the expression of cell-cycle-related genes among the single mutants and WT plants (Figure S4A). Similarly, cell ploidy was the same in the single mutants (reca1-1, why1, or why3) as it was in WT plants (Figures S4B and S4C). Thus, it is possible that plastid genome instability in the single mutants is not severe enough to cause changes in endoreplication and the cell cycle. The transcription factor of SOG1 directly controls the genes responsible for cell-cycle regulation, such as CDK inhibitors (Yi et al., 2014Yi D. Alvim Kamei C.L. Cools T. Vanderauwera S. Takahashi N. Okushima Y. Eekhout T. Yoshiyama K.O. Larkin J. Van den Daele H. et al.The Arabidopsis SIAMESE-RELATED cyclin-dependent kinase inhibitors SMR5 and SMR7 regulate the DNA damage checkpoint in response" @default.
• W3048776995 created "2020-08-18" @default.
• W3048776995 creator A5009994877 @default.
• W3048776995 creator A5021672168 @default.
• W3048776995 creator A5029666268 @default.
• W3048776995 creator A5073871300 @default.
• W3048776995 creator A5084589499 @default.
• W3048776995 date "2020-08-01" @default.
• W3048776995 modified "2023-10-14" @default.
• W3048776995 title "Signaling from Plastid Genome Stability Modulates Endoreplication and Cell Cycle during Plant Development" @default.
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• W3048776995 doi "https://doi.org/10.1016/j.celrep.2020.108019" @default.
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