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Arabidopsis Rad51B is important for double-strand DNA breaks repair in somatic cells

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Abstract

Rad51 paralogs belong to the Rad52 epistasis group of proteins and are involved in homologous recombination (HR), especially the assembly and stabilization of Rad51, which is a homolog of RecA in eukaryotes. We previously cloned and characterized two RAD51 paralogous genes in Arabidopsis, named AtRAD51C and AtXRCC3, which are considered the counterparts of human RAD51C and XRCC3, respectively. Here we describe the identification of RAD51B homologue in Arabidopsis, AtRAD51B. We found a higher expression of AtRAD51B in flower buds and roots. Expression of AtRAD51B was induced by genotoxic stresses such as ionizing irradiation and treatment with a cross-linking reagent, cisplatin. Yeast two-hybrid analysis showed that AtRad51B interacted with AtRad51C. We also found and characterized T-DNA insertion mutant lines. The mutant lines were devoid of AtRAD51B expression, viable and fertile. The mutants were moderately sensitive to γ-ray and hypersensitive to cisplatin. Our results suggest that AtRAD51B gene product is involved in the repair of double-strand DNA breaks (DSBs) via HR

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Abbreviations

RACE:

rapid amplification of cDNA ends

RT-PCR:

reverse transcriptase polymerase chain reaction

X-gal:

5-bromo-4-chloro-3-indolyl-β-D-galactopyranoside

References

  • J.S. Albala M.P. Thelen C. Prange W. Fan M. Christensen L.H. Thompson G.G. Lennon (1997) ArticleTitleIdentification of a novel human RAD51 homolog RAD51B Genomics 46 476–479 Occurrence Handle10.1006/geno.1997.5062 Occurrence Handle1:CAS:528:DyaK1cXmt12ntw%3D%3D Occurrence Handle9441753

    Article  CAS  PubMed  Google Scholar 

  • D.K. Bishop D. Park L. Xu N. Kleckner (1992) ArticleTitleDMC1: A meiosis-specific yeast homolog of E. coli recA required for recombination synaptonemal complex formation and cell cycle progression Cell 69 439–456 Occurrence Handle10.1016/0092-8674(92)90446-J Occurrence Handle1:CAS:528:DyaK3sXkt1Wltr0%3D Occurrence Handle1581960

    Article  CAS  PubMed  Google Scholar 

  • D.K. Bishop U. Ear A. Bhattacharyya C. Calderone M. Beckett R.R. Weichselbaum A. Shinohara (1998) ArticleTitleXrcc3 is required for assembly of Rad51 complexes in vivo J. Biol. Chem. 273 21482–21488 Occurrence Handle10.1074/jbc.273.34.21482 Occurrence Handle1:CAS:528:DyaK1cXlsFOrur0%3D Occurrence Handle9705276

    Article  CAS  PubMed  Google Scholar 

  • J.-Y. Bleuyard C.I. White (2004) ArticleTitleThe Arabidopsis homologue of Xrcc3 plays an essential role in meiosis EMBO J. 23 439–449 Occurrence Handle10.1038/sj.emboj.7600055 Occurrence Handle1:CAS:528:DC%2BD2cXhtVeqtro%3D Occurrence Handle14726957

    Article  CAS  PubMed  Google Scholar 

  • J.P. Braybrooke J.L. Li L. Wu F. Caple F.E. Benson I.D. Hickson (2003) ArticleTitleFunctional interaction between the Bloom’s syndrome helicase and the RAD51 paralog RAD51L3 (RAD51D) J. Biol. Chem. 278 48357–48366 Occurrence Handle10.1074/jbc.M308838200 Occurrence Handle1:CAS:528:DC%2BD3sXpt1Gjt7o%3D Occurrence Handle12975363

    Article  CAS  PubMed  Google Scholar 

  • P. Bundock P. Hooykaas (2002) ArticleTitleSevere developmental defects hypersensitivity to DNA-damaging agents and lengthened telomeres in Arabidopsis MRE11 mutants Plant Cell 14 2451–2462 Occurrence Handle10.1105/tpc.005959 Occurrence Handle1:CAS:528:DC%2BD38XotFelsL4%3D Occurrence Handle12368497

    Article  CAS  PubMed  Google Scholar 

  • R. Cartwright A.M. Dunn P.J. Simpson C.E. Tambini J. Thacker (1998) ArticleTitleIsolation of novel human and mouse genes of the recA/RAD51 recombination-repair gene family Nucleic Acids Res. 26 1653–1659 Occurrence Handle10.1093/nar/26.7.1653 Occurrence Handle1:CAS:528:DyaK1cXis1Ojtb8%3D Occurrence Handle9512535

    Article  CAS  PubMed  Google Scholar 

  • R. Cartwright C.E. Tambini P.J. Simpson J. Thacker (1998b) ArticleTitleThe XRCC2 DNA repair gene from human and mouse encodes a novel member of the recA/RAD51 family Nucleic Acids Res. 26 3084–3089 Occurrence Handle10.1093/nar/26.13.3084 Occurrence Handle1:CAS:528:DyaK1cXks1Cls7o%3D

    Article  CAS  Google Scholar 

  • F. Couteau F. Belzile C. Horlow O. Grandjean D. Vezon M.P. Doutriaux (1999) ArticleTitleRandom chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis Plant Cell 11 1623–1634 Occurrence Handle10.1105/tpc.11.9.1623 Occurrence Handle1:CAS:528:DyaK1MXms1aiu70%3D Occurrence Handle10488231

    Article  CAS  PubMed  Google Scholar 

  • B. Deans C.S. Griffin M. Maconochie J. Thacker (2000) ArticleTitleXrcc2 is required for genetic stability embryonic neurogenesis and viability in mice EMBO J. 19 6675–6685 Occurrence Handle10.1093/emboj/19.24.6675 Occurrence Handle1:CAS:528:DC%2BD3MXns1agtQ%3D%3D Occurrence Handle11118202

    Article  CAS  PubMed  Google Scholar 

  • M. Dizdaroglu D.S. Bergtold (1986) ArticleTitleCharacterization of free radical-induced base damage in DNA at biologically relevant levels Anal. Biochem. 156 182–188 Occurrence Handle1:CAS:528:DyaL28XkslCitro%3D Occurrence Handle3017148

    CAS  PubMed  Google Scholar 

  • M.K. Dosanjh D.W. Collins W. Fan G. Lennon J.S. Albana Z. Shen D. Schild (1998) ArticleTitleIsolation and characterization of RAD51C a new human member of the RAD51 family of related genes Nucleic Acids Res. 26 1179–1184 Occurrence Handle1:CAS:528:DyaK1cXhvFarsbg%3D Occurrence Handle9469824

    CAS  PubMed  Google Scholar 

  • M.-P. Doutriaux F. Couteau C. Bergounioux C. White (1998) ArticleTitleIsolation and characterization of the RAD51 and DMC1 homologs from Arabidopsis thaliana Mol. Gen. Genet. 257 283–291 Occurrence Handle1:CAS:528:DyaK1cXitVOltLg%3D Occurrence Handle9520262

    CAS  PubMed  Google Scholar 

  • A. Dudas M. Chovanec (2004) ArticleTitleDNA double-strand break repair by homologous recombination Mutat. Res. 566 131–167 Occurrence Handle1:CAS:528:DC%2BD2cXhtFWmurg%3D Occurrence Handle15164978

    CAS  PubMed  Google Scholar 

  • J. Essers H. Steeg Particlevan J. Wit Particlede S.M. Swagemakers M. Vermeij J.H. Hoeijmakers R. Kanaar (2000) ArticleTitleHomologous and non-homologous recombination differentially affect DNA damage repair in mice EMBO J. 19 1703–1710 Occurrence Handle1:CAS:528:DC%2BD3cXislymtLg%3D Occurrence Handle10747037

    CAS  PubMed  Google Scholar 

  • M.E. Gallego M. Jeanneau F. Granier D. Bouchez N. Bechtold C.I. White (2001) ArticleTitleDisruption of the Arabidopsis RAD50 gene leads to plant sterility and MMS sensitivity Plant J. 25 31–41 Occurrence Handle1:CAS:528:DC%2BD3MXhsVWrtrk%3D Occurrence Handle11169180

    CAS  PubMed  Google Scholar 

  • B.C. Godthelp W.W. Wiegant A. Duijn-Goedhart Particlevan O.D. Scharer P.P. Buul Particlevan R. Kanaar M.Z. Zdzienicka (2002) ArticleTitleMammalian Rad51C contributes to DNA cross-link resistance sister chromatid cohesion and genomic stability Nucleic Acids Res. 30 2172–2182 Occurrence Handle1:CAS:528:DC%2BD38XktFyktr8%3D Occurrence Handle12000837

    CAS  PubMed  Google Scholar 

  • R.C. Gupta L.R. Bazemore E.I. Golub C.M. Radding (1997) ArticleTitleActivities of human recombination protein Rad51 Proc. Natl. Acad. Sci. USA 94 463–468 Occurrence Handle1:CAS:528:DyaK2sXnslagtw%3D%3D Occurrence Handle9012806

    CAS  PubMed  Google Scholar 

  • J.H.J. Hoeijmakers (2001) ArticleTitleGenome maintenance mechanisms for preventing cancer Nature 411 366–374 Occurrence Handle10.1038/35077232 Occurrence Handle1:CAS:528:DC%2BD3MXktVSjs74%3D Occurrence Handle11357144

    Article  CAS  PubMed  Google Scholar 

  • L.C. Huang K.C. Clarkin G.M. Wahl (1996) ArticleTitleSensitivity and selectivity of the DNA damage sensor responsible for activating p53-dependent G1 arrest Proc. Natl. Acad. Sci. USA 93 4827–4832 Occurrence Handle1:CAS:528:DyaK28XjtVKlsbo%3D Occurrence Handle8643488

    CAS  PubMed  Google Scholar 

  • J.A. Kans R.K. Mortimer (1991) ArticleTitleNucleotide sequence of the RAD57 gene of Saccharomyces cerevisiae Gene 105 139–140 Occurrence Handle1:CAS:528:DyaK3sXhvVWmsw%3D%3D Occurrence Handle1937004

    CAS  PubMed  Google Scholar 

  • V.I. Klimyuk J.D.G. Jones (1997) ArticleTitleAtDMC1 the Arabidopsis homologue of the yeast DMC1 gene: Characterization transposon-induced allelic variation and meiosis-associated expression Plant J. 11 1–14 Occurrence Handle1:CAS:528:DyaK2sXhtFGjs7k%3D Occurrence Handle9025299

    CAS  PubMed  Google Scholar 

  • A. Kuzminov (2001) ArticleTitleDNA replication meets genetic exchange: chromosomal damage and its repair by homologous recombination Proc. Natl. Acad. Sci. USA 98 8461–8468 Occurrence Handle1:CAS:528:DC%2BD3MXls1WisLw%3D Occurrence Handle11459990

    CAS  PubMed  Google Scholar 

  • P. Laufs O. Grandjean C. Jonak K. Kieu J. Traas (1998) ArticleTitleCellular parameters of the shoot apical meristem in Arabidopsis Plant Cell 1998 1375–1390

    Google Scholar 

  • W. Li C. Chen U. Markmann-Mulisch L. Timofejeva E. Schmelzer H. Ma B. Reiss (2004) ArticleTitleThe Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis Proc. Natl. Acad. Sci. USA 101 10597–10601

    Google Scholar 

  • Y.C. Lio A.V. Mazin S.C. Kowalczykowski D.J. Chen (2003) ArticleTitleComplex formation by the human Rad51B and Rad51C DNA repair proteins and their activities in vitro J. Biol. Chem. 278 2469–24678 Occurrence Handle1:CAS:528:DC%2BD3sXksFantQ%3D%3D Occurrence Handle12427746

    CAS  PubMed  Google Scholar 

  • N. Liu J.E. Lamerdin R.S. Tebbs D. Schild J.D. Tucker M.R. Shen K.W. Brookman M.J. Siciliano C.A. Walter W. Fan L.S. Narayana Z.Q. Zhou A.W. Adamson K.J. Sorensen D.J. Chen N.J. Jones L.H. Thompson (1998) ArticleTitleXRCC2 and XRCC3 new human Rad51-family members promote chromosome stability and protect against DNA cross-links and other damages Mol. Cell 1 783–793 Occurrence Handle1:CAS:528:DyaK1cXjslSjt7s%3D Occurrence Handle9660962

    CAS  PubMed  Google Scholar 

  • N. Liu D. Schild M.P. Thelen L.H. Thompson (2002) ArticleTitleInvolvement of Rad51C in two distinct protein complexes of Rad51 paralogs in human cells Nucleic Acids Res. 30 1009–1015 Occurrence Handle1:CAS:528:DC%2BD38Xhs1Chs74%3D Occurrence Handle11842113

    CAS  PubMed  Google Scholar 

  • Y. Liu J.-Y. Masson R. Shah P. O’Regan S.C. West (2004) ArticleTitleRAD51C is required for holliday junction processing in mammalian cells Science 303 243–246 Occurrence Handle1:CAS:528:DC%2BD2cXhtlGhtQ%3D%3D Occurrence Handle14716019

    CAS  PubMed  Google Scholar 

  • S.T. Lovett (1994) ArticleTitleSequence of the RAD55 gene of Saccharomyces cerevisiae: similar to prokaryotic RecA and other RecA-like proteins Gene 142 103–106 Occurrence Handle1:CAS:528:DyaK2cXltVSqs7s%3D Occurrence Handle8181742

    CAS  PubMed  Google Scholar 

  • J.-Y. Masson A.Z. Stasiak A. Stasiak F. Benson S.C. West (2001) ArticleTitleComplex formation by the human RAD51C and XRCC3 recombination repair proteins Proc. Natl. Acad. Sci. USA 98 8440–8446 Occurrence Handle1:CAS:528:DC%2BD3MXls1Wis7c%3D Occurrence Handle11459987

    CAS  PubMed  Google Scholar 

  • K.A. Miller D. Sawicka D. Barsky J.S. Albala (2004) ArticleTitleDomain mapping of the Rad51 paralog protein complexes Nucleic Acids Res. 32 169–178 Occurrence Handle1:CAS:528:DC%2BD2cXhtlKgurY%3D Occurrence Handle14704354

    CAS  PubMed  Google Scholar 

  • T. Ogawa X. Yu A. Shinohara E.H. Egleman (1993) ArticleTitleSimilarity of the yeast RAD51 filament to the bacterial RecA filament Science 259 1896–1899 Occurrence Handle1:CAS:528:DyaK3sXitVyjs7s%3D Occurrence Handle8456314

    CAS  PubMed  Google Scholar 

  • P. O’Regan C. Wilson S. Townsend J. Thacker (2001) ArticleTitleXRCC2 is a nuclear RAD51-like protein required for damage-dependent RAD51 focus formation without the need for ATP binding J. Biol. Chem. 22 22148–22153

    Google Scholar 

  • K. Osakabe T. Yoshioka H. Ichikawa S. Toki (2002) ArticleTitleMolecular cloning and characterization of RAD51-like genes from Arabidopsis thaliana Plant Mol. Biol. 50 71–81 Occurrence Handle1:CAS:528:DC%2BD38XkslKltLc%3D Occurrence Handle12139010

    CAS  PubMed  Google Scholar 

  • R.D.M. Page (1996) ArticleTitleTREEVIEW: an application to display phylogenetic trees on personal computers Comput. Appl. Biosci. 12 357–358 Occurrence Handle1:STN:280:ByiD2MfgtlA%3D Occurrence Handle8902363

    CAS  PubMed  Google Scholar 

  • D.L. Pittman L.R. Weinberg J.C. Schimenti (1998) ArticleTitleIdentification characterization and genetic mapping of Rad51d a new mouse and human RAD51/RecA-related gene Genomics 49 103–111 Occurrence Handle1:CAS:528:DyaK1cXivFSmt7g%3D Occurrence Handle9570954

    CAS  PubMed  Google Scholar 

  • D.L. Pittman J.C. Schimenti (2000) ArticleTitleMidgestation lethality in mice deficient for the RecA-related gene Rad51d/Rad51l3 Genesis 26 167–173 Occurrence Handle1:CAS:528:DC%2BD3cXis1yrurs%3D Occurrence Handle10705376

    CAS  PubMed  Google Scholar 

  • S.B. Preuss A.B. Britt (2003) ArticleTitleA DNA-damage-induced cell cycle checkpoint in Arabidopsis Genetics 164 323–334 Occurrence Handle1:CAS:528:DC%2BD3sXkvFOiuro%3D Occurrence Handle12750343

    CAS  PubMed  Google Scholar 

  • J. Puizina J. Siroky P. Mokros D. Schweizer K. Riha (2004) ArticleTitleMre11 deficiency in Arabidopsis is associated with chromosomal instability in somatic cells and Spo11-dependent genome fragmentation during meiosis Plant Cell 16 1968–1978 Occurrence Handle1:CAS:528:DC%2BD2cXmvVansb8%3D Occurrence Handle15258261

    CAS  PubMed  Google Scholar 

  • M.C. Rice S.T. Smith F. Bullrich P. Havre E.B. Kmiec (1997) ArticleTitleIsolation of human and mouse genes based on homology to REC2 a recombinational repair gene from the fungus Ustilago maydis Proc. Natl. Acad. Sci. USA 94 7417–7422 Occurrence Handle1:CAS:528:DyaK2sXksFOmurg%3D Occurrence Handle9207106

    CAS  PubMed  Google Scholar 

  • C. Richardson M. Jasin (2000) ArticleTitleCoupled homologous and nonhomologous repair of a double-strand break preserves genomic integrity in mammalian cells Mol. Cell. Biol. 20 9068–9075 Occurrence Handle1:CAS:528:DC%2BD3MXitFGrsLs%3D Occurrence Handle11074004

    CAS  PubMed  Google Scholar 

  • M.S. Sasaki M. Takata E. Sonoda A. Tachibana S. Takeda (2004) ArticleTitleRecombination repair pathway in the maintenance of chromosomal integrity against DNA interstrand crosslinks Cytogenet. Genome Res. 104 28–34 Occurrence Handle1:CAS:528:DC%2BD2cXlvVGks7w%3D Occurrence Handle15162012

    CAS  PubMed  Google Scholar 

  • D. Schild Y.-C. Lio D.W. Collins T. Tsomondo D.J. Chen (2000) ArticleTitleEvidence for simultaneous protein interactions between human RAD51 paralogs J. Biol. Chem. 275 16443–16449 Occurrence Handle1:CAS:528:DC%2BD3cXjvFCnt7k%3D Occurrence Handle10749867

    CAS  PubMed  Google Scholar 

  • Z. Shu S. Smith L. Wang M.C. Rice E.B. Kmiec (1999) ArticleTitleDisruption of muREC2/RAD51L1 in mice results in early embryonic lethality which can be partially rescued in a p53−/− background Mol. Cell. Biol. 19 8686–8693 Occurrence Handle1:CAS:528:DyaK1MXns1ynsr0%3D Occurrence Handle10567591

    CAS  PubMed  Google Scholar 

  • S. Sigurdsson S. Komen Particlevan W. Bussen D. Schild J.S. Albala P. Sung (2001) ArticleTitleMediator function of the human Rad51B-Rad51C complex in Rad51/PRA-catalyzed DNA strand exchange Genes Dev. 15 3308–3318 Occurrence Handle1:CAS:528:DC%2BD38XivFyrsw%3D%3D Occurrence Handle11751636

    CAS  PubMed  Google Scholar 

  • E. Sonoda M.S. Sasaki J.M. Buerstedde O. Bezzubova A. Shinohara H. Ogawa M. Takata Y. Yamaguchi-Iwai S. Takeda (1998) ArticleTitleRad51-deficient vertebrate cells accumulate chromosome breaks prior to cell death EMBO J. 17 598–608 Occurrence Handle1:CAS:528:DyaK1cXos1ertQ%3D%3D Occurrence Handle9430650

    CAS  PubMed  Google Scholar 

  • P. Sung (1997) ArticleTitleYeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein A to promote DNA strand exchange by Rad51 recombinase Genes Dev. 11 1111–1121 Occurrence Handle1:CAS:528:DyaK2sXjtlartbk%3D Occurrence Handle9159392

    CAS  PubMed  Google Scholar 

  • M. Takata M.S. Sasaki E. Sonoda T. Fukushima C. Morrison J. Albala M.A. Swagemakers R. Kanaar L.H. Thompson S. Takeda (2000) ArticleTitleThe Rad51 paralogs Rad51B promotes homologous recombinational repair Mol. Cell. Biol. 20 6476–6482 Occurrence Handle1:CAS:528:DC%2BD3cXlvFens74%3D Occurrence Handle10938124

    CAS  PubMed  Google Scholar 

  • M. Takata M.S. Sasaki S. Tachiiri T. Fukushima E. Sonoda D. Schild L.H. Thompson S. Takeda (2001) ArticleTitleChromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs Mol. Cell. Biol. 21 2858–2866 Occurrence Handle1:CAS:528:DC%2BD3MXisVyhtr0%3D Occurrence Handle11283264

    CAS  PubMed  Google Scholar 

  • R.S. Tebbs Y. Zhao J.D. Tucker J.B. Scheerer M.J. Siciliano M. Hwang N. Liu R.J. Legerski L.H. Thompson (1995) ArticleTitleCorrection of chromosomal instability and sensitivity to diverse mutagens by cDNA of the XRCC3 DNA repair gene Proc. Natl. Acad. Sci. USA 92 6354–6358 Occurrence Handle1:CAS:528:DyaK2MXmslKqtLc%3D Occurrence Handle7603995

    CAS  PubMed  Google Scholar 

  • J. Thacker (1999a) ArticleTitleA surfeit of RAD51-like genes? Trends Genet. 15 166–168 Occurrence Handle1:CAS:528:DyaK1MXjt12mtbs%3D

    CAS  Google Scholar 

  • J. Thacker (1999b) ArticleTitleRepair of ionizing radiation damage in mammalian cells: Alternative pathways and their fidelity C.A. Acad. Sci. Ser. III Life Sci. 322 103–108 Occurrence Handle1:CAS:528:DyaK1MXlvVOmtbk%3D

    CAS  Google Scholar 

  • J.D. Thompson D.G. Higgins T.J. Gibson (1994) ArticleTitleCLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting positions-specific gap penalties and weight matrix choice Nucleic Acids Res. 22 4673–4680 Occurrence Handle1:CAS:528:DyaK2MXitlSgu74%3D Occurrence Handle7984417

    CAS  PubMed  Google Scholar 

  • H. Yokoyama H. Kurumizaka S. Ikawa S. Yokoyama T. Shibata (2003) ArticleTitleHolliday junction binding activity of the human Rad51B protein J. Biol. Chem. 278 2767–2772 Occurrence Handle1:CAS:528:DC%2BD3sXksFarsA%3D%3D Occurrence Handle12441335

    CAS  PubMed  Google Scholar 

  • J.E. Walker M. Saraste M.J. Runswick N.J. Gay (1982) ArticleTitleDistantly related sequences in the a- and b-subunits of ATP-synthase myosin kinases and other ATP-requiring enzymes and a common nucleotide binding fold EMBO J. 1 945–951 Occurrence Handle1:CAS:528:DyaL3sXhtVensbY%3D Occurrence Handle6329717

    CAS  PubMed  Google Scholar 

  • D.B. Zamble S.J. Lippard (1995) ArticleTitleCisplatin and DNA in cancer chemotherapy Trends Biochem. Sci. 20 435–439 Occurrence Handle1:CAS:528:DyaK2MXptVajtbo%3D Occurrence Handle8533159

    CAS  PubMed  Google Scholar 

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Correspondence to Seiichi Toki.

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Accession numbers: AB194809 (AtRAD51Bα), AB194810 (AtRAD51Bβ), AB194811 (AtRAD51D).

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Osakabe, K., Abe, K., Yamanouchi, H. et al. Arabidopsis Rad51B is important for double-strand DNA breaks repair in somatic cells. Plant Mol Biol 57, 819–833 (2005). https://doi.org/10.1007/s11103-005-2187-1

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