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UV-B-induced DNA damage mediates expression changes of cell cycle regulatory genes in Arabidopsis root tips

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Abstract

Even though a number of studies have shown that UV-B radiation inhibits plant growth and regulates the cell cycle progress, little is known about the molecular and cellular mechanisms. Here, we developed a synchronous root-tip cell system to investigate expression changes of cell cycle marker genes and DNA damage under UV-B radiation. Expression analysis of cell cycle marker genes revealed that G1-to-S transition in root-tip cells was accomplished within 6 h. In the in vivo synchronous root-tip cells, high level of UV-B radiation (0.45 W m−2) induced expression changes of the cell cycle regulatory genes. Genes involved in G1-to-S transition, Histone H4 and E2Fa, were down-regulated by UV-B radiation during 2–6 h; whereas transcripts for KRP2, a negative regulator of G1-to-S transition, were up-regulated by UV-B at 2 h. The peak time for transcript level of CYCD3;1, a positive factor in G1-to-S transition, was delayed by UV-B radiation. Interestingly, a medium level of UV-B radiation (0.25 W m−2) did not change the expression of these genes in root tip cells from wild type. However, cell cycle regulatory genes were greatly affected in uvh1 mutant, which exhibited higher content of cyclobutane pyrimidine dimers (CPDs). Ascorbic acid treatment did not change the expression pattern of cell cycle regulatory genes that were affected by high-level UV-B. Our results implied that UV-B-induced DNA damage results in the delay of G1-to-S transition of plant cell cycle. UV-B-induced G1-to-S arrest may be a protective mechanism that prevents cells with damaged DNA from dividing and may explain the plant growth inhibition under increased solar UV-B radiation.

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Abbreviations

AsA:

Ascorbic acid

ATM:

Ataxia-telangiectasia mutated

ATR:

Ataxia-telangiectasia and Rad3-related

CDKs:

Cyclin-dependent kinases

CPDs:

Cyclobutane pyrimidine dimers

HU:

Hydroxyurea

KRPs:

Kip-related proteins

NAA:

1-naphthalene acetic acid

NPA:

N-1-naphthylphthalamic acid

ROS:

Reactive oxygen species

XPF:

Xeroderma pigmentosum group F

References

  • Abraham RT (2001) Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev 15:2177–2196

    Article  PubMed  CAS  Google Scholar 

  • Bergounioux C, Perennes C, Brown SC, Gadal P (1988) Cytometric analysis of growth regulator-dependent transcription and cell cycle progression in P. hybrida protoplast cultures. Planta 175:500–505

    Article  CAS  Google Scholar 

  • Björn LO, McKenzie RL (2008) Ozone depletion and the effects of ultraviolet radiation. In: Björn LO (ed) Photobiology: the science of life and light. Springer Press, New York, pp 511–523

    Chapter  Google Scholar 

  • Björn LO, Callaghan TV, Johnsen I, Lee JA, Manetas Y, Paul ND, Sonesson M, Wellburn AR, Coop D, Heide-Jørgensen HS, Gehrke C, Gwynn-Jones D, Johanson U, Kyparissis A, Levizou E, Nikolopoulos D, Petropoulou Y, Stephanou M (1997) The effects of UV-B radiation on European heathland species. Plant Ecol 128:253–264

    Article  Google Scholar 

  • Boniotti MB, Gutierrez C (2001) A cell-cycle-regulated kinase activity phosphorylates plant retinoblastoma protein and contains, in Arabidopsis, a CDKA/cyclin D complex. Plant J 28:341–350

    Article  PubMed  CAS  Google Scholar 

  • Britt AB (1996) DNA damage and repair in plants. Annu Rev Plant Physiol Plant Mol Biol 47:75–100

    Article  PubMed  CAS  Google Scholar 

  • Burssens S, Himanen K, van de Cotte B, Beeckman T, Van Montagu M, Inze D, Verbruggen N (2000) Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana. Planta 211:632–640

    Article  PubMed  CAS  Google Scholar 

  • Caldwell MM (1971) Solar UV-B irradiation and the growth and development of higher plant. In: Giese AC (ed) Photophysiology, vol 6. Academic Press, New York, pp 131–171

    Google Scholar 

  • Caldwell MM, Bornman JF, Ballare CL, Flint SD, Kulandaivelu G (2007) Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with bother climate change factors. Photochem Photobiol Sci 6:252–266

    Article  PubMed  CAS  Google Scholar 

  • Casati P, Walbot V (2003) Gene expression profiling in response to ultraviolet radiation in maize genotypes with varying flavonoid content. Plant Physiol 132:1739–1754

    Article  PubMed  CAS  Google Scholar 

  • Casati P, Walbot V (2004) Rapid transcriptome responses of maize (Zea mays) to UV-B in irradiated and shielded tissues. Genome Biol 5:R16. doi:10.1186/gb-2004-5-3-r16

  • Couteau F, Belzile F, Horlow C, Grandjean O, Vezon D, Doutriaux MP (1999) Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. Plant Cell 11:1623–1634

    Article  PubMed  CAS  Google Scholar 

  • Culligan K, Tissier A, Britt A (2004) ATR regulates a G2-phase cell-cycle checkpoint in Arabidopsis thaliana. Plant Cell 16:1091–1104

    Article  PubMed  CAS  Google Scholar 

  • Dai QJ, Yan B, Huang SB, Liu XZ, Peng SB, Miranda MLL, Chavez AQ, Vergara BS, Olszyk DM (1997) Response of oxidative stress defense systems in rice (Oryza sativa) leaves with supplemental UV-B radiation. Physiol Plant 101:301–308

    Article  CAS  Google Scholar 

  • De Veylder L, Beemster GTS, Beeckman T, Inzé D (2001) CKS1At overexpression in Arabidopsis thaliana inhibits growth by reducing meristem size and inhibiting cell-cycle progression. Plant J 25:617–626

    Article  PubMed  Google Scholar 

  • De Veylder L, Beeckman T, Beemster GTS, Engler JD, Ormenese S, Maes S, Naudts M, Van der Schueren E, Jacqmard A, Engler G, Inzé D (2002) Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-DPa transcription factor. EMBO J 21:1360–1368

    Article  PubMed  Google Scholar 

  • De Veylder L, Joubès J, Inzé D (2003) Plant cell cycle transitions. Curr Opin Plant Biol 6:536–543

    Article  PubMed  Google Scholar 

  • Dewitte W, Murray JAH (2003) The plant cell cycle. Annu Rev Plant Biol 54:235–264

    Article  PubMed  CAS  Google Scholar 

  • Doležel J, Číhalíkvá J, Weiserová J, Lucretti S (1999) Cell cycle synchronization in plant root meristems. Methods Cell Sci 21:95–107

    Article  PubMed  Google Scholar 

  • Dulic V, Kaufmann WK, Wilson SJ, Tisty TD, Lees E, Harper JW, Elledge SJ, Reed SI (1994) p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell 76:1013–1023

    Article  PubMed  CAS  Google Scholar 

  • Favory JJ, Stec A, Gruber H, Rizzini L, Oravecz A, Funk M, Albert A, Cloix C, Jenkins GI, Oakeley EJ, Seidlitz HK, Nagy F, Ulm R (2009) Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO J 28:591–601

    Article  PubMed  CAS  Google Scholar 

  • Furukawa T, Curtis MJ, Tominey CM, Duong YH, Wilcox BWL, Aggoune D, Hays JB, Britt AB (2010) A shared DNA-damage-response pathway for induction of stem-cell death by UVB and by gamma irradiation. DNA Repair 9:940–948

    Article  PubMed  CAS  Google Scholar 

  • Garcia V, Bruchet H, Camescasse D, Granier F, Bouchez D, Tissier A (2003) AtATM is essential for meiosis and the somatic response to DNA damage in plants. Plant Cell 15:119–132

    Article  PubMed  CAS  Google Scholar 

  • Gerhardt KE, Wilson MI, Greenberg BM (1999) Tryptophan photolysis leads to a UVB-induced 66 kDa photoproduct of ribulose-1, 5-bisphosphate carboxylase/oxygenase (Rubisco) in vitro and in vivo. Photochem Photobiol 70:49–56

    CAS  Google Scholar 

  • Gutierrez C, Ramirez-Parra E, Castellano MM, del Pozo JC (2002) G(1) to S transition: more than a cell cycle engine switch. Curr Opin Plant Biol 5:480–486

    Article  PubMed  CAS  Google Scholar 

  • Gutierrez L, Mauriat M, Guenin S, Pelloux J, Lefebvre JF, Louvet R, Rusterucci C, Moritz T, Guerineau F, Bellini C, Van Wuytswinkel O (2008) The lack of a systematic validation of reference genes: a serious pitfall undervalued in reverse transcription-polymerase chain reaction (RT-PCR) analysis in plants. Plant Biotechnol J 6:609–618

    Article  PubMed  CAS  Google Scholar 

  • Hidema J, Zhang W, Yamamoto M, Sato T, Kumagai T (2005) Changes in grain size and grain storage protein of rice (Oryza sativa L.) in response to elevated UV-B radiation under outdoor conditions. J Radiat Res 46:143–149

    Article  PubMed  Google Scholar 

  • Himanen K, Boucheron E, Vanneste S, Engler JD, Inze D, Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14:2339–2351

    Article  PubMed  CAS  Google Scholar 

  • Himanen K, Vuylsteke M, Vanneste S, Vercruysse S, Boucheron E, Alard P, Chriqui D, Van Montagu M, Inze D, Beeckman T (2004) Transcript profiling of early lateral root initiation. Proc Natl Acad Sci USA 101:5146–5151

    Article  PubMed  CAS  Google Scholar 

  • Jansen MAK, Gaba V, Greenberg BM (1998) Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends Plant Sci 3:131–135

    Article  Google Scholar 

  • Jiang L, Wang Y, Björn LO, Li S (2009) Arabidopsis RADICAL-INDUCED CELL DEATH1 is involved in UV-B signaling. Photochem Photobiol Sci 8:838–846

    Article  PubMed  CAS  Google Scholar 

  • John PCL, Mews M, Moore R (2001) Cyclin/Cdk complexes: their involvement in cell cycle progression and mitotic division. Protoplasma 216:119–142

    Article  PubMed  CAS  Google Scholar 

  • Joubès J, Chevalier C, Dudits D, Heberle-Bors E, Inzé D, Umeda M, Renaudin JP (2000) CDK-related protein kinases in plants. Plant Mol Biol 43:607–620

    Article  PubMed  Google Scholar 

  • Kadota Y, Watanabe T, Fujii S, Higashi K, Sano T, Nagata T, Hasezawa S, Kuchitsu K (2004) Crosstalk between elicitor-induced cell death and cell cycle regulation in tobacco BY-2 cells. Plant J 40:131–142

    Article  PubMed  CAS  Google Scholar 

  • Krizek DT, Chalker-Scott L (2005) Ultraviolet radiation and terrestrial ecosystems. Photochem Photobiol 81:1021–1025

    Article  PubMed  CAS  Google Scholar 

  • Lakin ND, Jackson SP (1999) Regulation of p53 in response to DNA damage. Oncogene 18:7644–7655

    Article  PubMed  CAS  Google Scholar 

  • Landry LG, Stapleton AE, Lim J, Hoffman P, Hays JB, Walbot V, Last RL (1997) An Arabidopsis photolyase mutant is hypersensitive to ultraviolet-B radiation. Proc Natl Acad Sci USA 94:328–332

    Article  PubMed  CAS  Google Scholar 

  • Leasure CD, Tong HY, Yuen GG, Hou XW, Sun XF, He ZH (2009) ROOT UV-B SENSITIVE2 acts with ROOT UV-B SENSITIVE1 in a root ultraviolet B-sensing pathway. Plant Physiol 150:1902–1915

    Article  PubMed  CAS  Google Scholar 

  • Loignon M, Drobetsky EA (2002) The initiation of UV-induced G1 arrest in human cells is independent of the p53/p21/pRb pathway but can be attenuated through expression of the HPVE7 oncoprotein. Carcinogenesis 23:35–45

    Article  PubMed  CAS  Google Scholar 

  • Mackerness SAH, Surplus SL, Blake P, John CF, Buchanan-Wollaston V, Jordan BR, Thomas B (1999) Ultraviolet-B-induced stress and changes in gene expression in Arabidopsis thaliana: role of signalling pathways controlled by jasmonic acid, ethylene and reactive oxygen species. Plant Cell Environ 22:1413–1423

    Article  CAS  Google Scholar 

  • Matthews BF (1983) Isolation of mitotic chromosomes from partially synchronized carrot (D. carota) cell suspension cultures. Plant Sci Lett 31:165–172

    Article  Google Scholar 

  • Meijer M, Murray JAH (2000) The role and regulation of D-type cyclins in the plant cell cycle. Plant Mol Biol 43:621–633

    Article  PubMed  CAS  Google Scholar 

  • Menges M, Samland AK, Planchais S, Murray JAH (2006) The D-type cyclin CYCD3;1 is limiting for the G1-to-S-phase transition in Arabidopsis. Plant Cell 18:893–906

    Article  PubMed  CAS  Google Scholar 

  • Meskiene I, Bogre L, Dahl M, Pirck M, Cam Ha DT, Swoboda I, Heberle-Bors E, Ammerer G, Hirt H (1995) cycMs3, a novel B-type alfalfa cyclin gene, is induced in the G0- to G1 transition of the cell cycle. Plant Cell 7:759–771

    Article  PubMed  CAS  Google Scholar 

  • Mironov V, De Veylder L, Van Montagu M, Inzé D (1999) Cyclin-dependent kinases and cell division in plants—the nexus. Plant Cell 11:509–521

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Neades R, Cox L, Pelling JC (1998) S-phase arrest in mouse keratinocytes exposed to multiple doses of ultraviolet B/A radiation. Mol Carcinog 23:159–167

    Article  PubMed  CAS  Google Scholar 

  • Nilssen EA, Synnes M, Kleckner N, Grallert Bt, Boye E (2003) Intra-G1 arrest in response to UV irradiation in fission yeast. Proc Natl Acad Sci USA 100:10758–10763

    Article  PubMed  CAS  Google Scholar 

  • Planchais S, Glab N, Inze D, Bergounioux C (2000) Chemical inhibitors: a tool for plant cell cycle studies. FEBS Lett 476:78–83

    Article  PubMed  CAS  Google Scholar 

  • Preuss SB, Britt AB (2003) A DNA-damage-induced cell cycle checkpoint in Arabidopsis. Genet 164:323–334

    CAS  Google Scholar 

  • Ramakers C, Ruijter JM, Deprez RH, Moorman AF (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66

    Article  PubMed  CAS  Google Scholar 

  • Renzing J, Hansen S, Lane DP (1996) Oxidative stress is involved in the UV activation of p53. J Cell Sci 109:1105–1112

    PubMed  CAS  Google Scholar 

  • Richard C, Lescot M, Inzé D, De Veylder L (2002) Effect of auxin, cytokinin, and sucrose on cell cycle gene expression in Arabidopsis thaliana cell suspension cultures. Plant Cell Tissue Organ Cult 69:167–176

    Article  CAS  Google Scholar 

  • Ries G, Heller W, Puchta H, Sandermann H, Seidlitz HK, Hohn B (2000) Elevated UV-B radiation reduces genome stability in plants. Nature 406:98–101

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto AN, Lan VT, Puripunyavanich V, Hase Y, Yokota Y, Shikazono N, Nakagawa M, Narumi I, Tanaka A (2009) A UVB-hypersensitive mutant in Arabidopsis thaliana is defective in the DNA damage response. Plant J 60:509–517

    Article  PubMed  CAS  Google Scholar 

  • Tong H, Leasure CD, Hou X, Yuen G, Briggs W, He Z-H (2008) Role of root UV-B sensing in Arabidopsis early seedling development. Proc Natl Acad Sci USA 105:21039–21044

    Article  PubMed  CAS  Google Scholar 

  • Vandepoele K, Raes J, De Veylder L, Rouze P, Rombauts S, Inze D (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14:903–916

    Article  PubMed  CAS  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: research0034

  • Verkest A, Manes CLD, Vercruysse S, Maes S, Van der Schueren E, Beeckman T, Genschik P, Kuiper M, Inzé D, De Veylder L (2005) The cyclin-dependent kinase inhibitor KRP2 controls the onset of the endoreduplication cycle during Arabidopsis leaf development through inhibition of mitotic CDKA;1 kinase complexes. Plant Cell 17:1723–1736

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Jiang L, Wang Y, Li S (2009) UV-B induced G1/S arrest in Arabidopsis root tips. Chin Bull Bot 44:426–433

    CAS  Google Scholar 

  • Zhou BB, Elledge SJ (2000) The DNA damage response: putting checkpoints in perspective. Nature 408:433–439

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Prof. Gareth Jenkins (University of Glasgow, UK) and Dr. Roman Ulm (University of Freiburg) for the critical reading of manuscript. This work was supported by the grants to Prof. Shaoshan Li from the National Natural Science Foundation of China [NSFC, No. 30470283 and No. 31070242], and the Research Fund for the Doctoral Program [20070574003] of Higher Education in China and the Scientific Research Foundation [2005-383] for the Returned Overseas Chinese Scholars, Ministry of Education, China.

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Authors and Affiliations

  1. Key Laboratory of Ecology and Environmental Science in Guangdong Higher Education, School of Life Science, South China Normal University, Guangzhou, 510631, China

    Lei Jiang, Lars Olof Björn & Shaoshan Li

  2. College of Life Science and Technology, Jinan University, Guangzhou, 510632, China

    Yan Wang

  3. Department of Biology, Lund University, Sölvegatan 35, 223 62, Lund, Sweden

    Lars Olof Björn

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  1. Lei Jiang
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Correspondence to Shaoshan Li.

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Jiang, L., Wang, Y., Björn, L.O. et al. UV-B-induced DNA damage mediates expression changes of cell cycle regulatory genes in Arabidopsis root tips. Planta 233, 831–841 (2011). https://doi.org/10.1007/s00425-010-1340-5

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