review article dna damage and repair in plants under...

Review ArticleDNA Damage and Repair in Plants under Ultraviolet andIonizing Radiations

Sarvajeet S Gill1 Naser A Anjum2 Ritu Gill1 Manoranjan Jha1 and Narendra Tuteja3

1Stress Physiology and Molecular Biology Lab Centre for Biotechnology MD University Rohtak Haryana 124 001 India2Centre for Environmental and Marine Studies (CESAM) Department of Chemistry University of Aveiro 3810-193 Aveiro Portugal3Plant Molecular Biology Group International Center for Genetic Engineering and Biotechnology (ICGEB) Aruna Asaf Ali MargNew Delhi 110067 India

Correspondence should be addressed to Sarvajeet S Gill ssgill14yahoocoin and Narendra Tuteja narendraicgebresin

Received 30 July 2014 Revised 27 October 2014 Accepted 4 November 2014

Academic Editor Aryadeep Roychoudhury

Copyright copy 2015 Sarvajeet S Gill et alThis is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Being sessile plants are continuously exposed to DNA-damaging agents present in the environment such as ultraviolet (UV) andionizing radiations (IR) Sunlight acts as an energy source for photosynthetic plants hence avoidance of UV radiations (namelyUV-A 315ndash400 nmUV-B 280ndash315 nm andUV-Clt280 nm) is unpreventableDNA inparticular strongly absorbsUV-B thereforeit is the most important target for UV-B induced damage On the other hand IR causes water radiolysis which generates highlyreactive hydroxyl radicals (OH∙) and causes radiogenic damage to important cellular components However to maintain genomicintegrity under UVIR exposure plants make use of several DNA repair mechanisms In the light of recent breakthrough thecurrent minireview (a) introduces UVIR and overviews UVIR-mediated DNA damage products and (b) critically discusses thebiochemistry and genetics of major pathways responsible for the repair of UVIR-accrued DNA damage The outcome of thediscussion may be helpful in devising future research in the current context

1 Introduction

Having sessile nature plants have to cope with constantexposure of environmental stressors which includes UV-B ozone desiccation rehydration salinity low and hightemperature and air and soil pollutants including metals-metalloids Several chemical mutagens and crosslinkingagents (eg mitomycin C cisplatin) alkylating agents aro-matic compounds ionizing radiations and fungal and bacte-rial toxins are included as the other important environmentalDNA-damaging agents [1] Apart from severely impactingplant structural enzymatic and nonenzymatic componentsthe aforesaid stressors may also negatively threaten plantgenomes Despite the very stable nature of plant genomenuclear DNA is an inherently unstable molecule and canbe damaged spontaneously metabolically or by aforesaidstress factors The overproduction of reactive oxygen species

(ROS) as byproducts of normal cellular metabolism or asa result of abiotic stress conditions leads to DNA damagein the cell [2 3] In addition to producing both single-strand DNA breaks (SSBs) and double-strand DNA breaks(DSBs) intrinsic DNA damage may include the loss of a baseto form an abasic site chemical modification of a base toform a miscoding or noncoding lesion and sugar-phosphatebackbone breakage [4 5]The accumulation of such damages(unrecognized and unrepaired DNA damage) may causelethal mutations which in turn can reduce plant genomestability growth and productivity and also threaten theorganismrsquos immediate survival [2 3 5ndash7]Therefore effectivedetection of DNA damage removal of damaged nucleotidesreplacementwith undamaged nucleotides viaDNAsynthesisand repair of DNA damage are essential to eliminate thechance of permanent genetic alterations and hence to ensurethe stability of the plant genome [2 7 8]

Hindawi Publishing Corporatione Scientific World JournalVolume 2015 Article ID 250158 11 pageshttpdxdoiorg1011552015250158

2 The Scientific World Journal

2 Ultraviolet (UV) Ionizing Radiations (IR)and Cellular DNA

Plants because of their sessile nature are especially suscep-tible to damage caused by environmental factors Thoughsunlight is obligatory for photosynthesis and survival ofplants it also represents one of the major threats to theirgenomic integrity Sunlight contains energy rich UV-A (320ndash400 nm) UV-B (290 to 320 nm) and UV-C (280 to 100 nm)light UV-C is filtered out in the atmosphere and UV-B andUV-A can reach earthrsquos surface effectively [3] Among UVradiation types UV-A radiation has been shown to haveless DNA damaging effect because it cannot be absorbed bynative DNA whereas UV-A and visible light energy (up to670ndash700 nm) can damage DNA via indirect photosensitizingreactions-mediated ROS generation especially singlet oxygen(1O2

) [9] UV-C radiation does not show much harmfuleffects on the biota since it is quantitatively absorbed byoxygen and ozone in the Earthrsquos atmosphere In the past 50years the concentration of ozone has decreased by about5 (hence significant depletion in stratospheric ozone)mainly due to the release of anthropogenic pollutants such aschlorofluorocarbons [10] Consequently a larger proportionof theUV-B spectrum reaches the Earthrsquos surface with seriousimplications on all living organisms [11ndash17]

UV-B radiation reaching the earthrsquos surface is highlyvariable and influenced by many factors including strato-spheric ozone layer and geographical area Though most ofthe extraterrestrial UV-B is absorbed by the stratosphericozone remaining UV-B can produce adverse effects ondiverse habitats [18] Anthropogenically released chlorineand fluorine-containing compounds (eg CFCs) mediatesignificant depletion of stratospheric ozone which is basicallyresponsible for increased UV-B radiation in the past decadesin particular in the Antarctic zone [11 12 16 17] AlthoughUV-B radiation has less than 1 of total solar energy it isa highly active component of the solar radiation that bringschemicalmodification inDNA[19 20]UV radiation is one ofthe most damaging agents for DNA and other biomoleculessuch as proteins and lipids [21 22] Moreover cellular DNAhas been considered an obvious key target for UV inducedgenetic damage in a variety of organisms including plants[1 23] Mechanism of DNA damage and repair in responseto UVIR radiation has been shown in Figure 1

On the perspective of IRmediatedDNAdamage in plantsit causes water radiolysis which generates highly reactiveOH∙ radicals OH∙ radicals are the most reactive among allROS and known to react with all biological molecules likeDNA proteins lipids and almost any constituent of cells Inthe absence of any enzymatic mechanism for the removal ofOH∙ excess OH∙ accumulation ultimately leads to cell deathDNA is the most preferred biomolecule being attacked byboth the OH∙ and the UV radiations (ie there is both directand indirect effect) [24] A number of alterations like SSBsand DSBs may take place in the IR and free radicals targetedDNA [24] Plants may recruit a wide variety of strategies toeither reverse excise or tolerate the presence ofDNAdamage

products [5] In this perspective though mechanisms under-lying UV and ionizing radiations-mediated DNA damageand repair have been thoroughly described in bacteria yeastand mammalian systems information on these processesin plants is scanty and unsubstantiated However the DNAdamage under UV radiation and DNA repair associatedenzymes have been shown to greatly modulate the mutationrate chromosome aberration frequencies and viability inseeds and seedlings [25]

The following sections and subsections present anoverview on UVionizing radiation-mediated DNA dam-age products and critically discuss potential biochemicaland genetic mechanisms underlying UVionizing radiationaccrued DNA damage and repair pathways

3 UV-B Radiation Accrued DNA Damage

UV-B radiation can penetrate and damage plant genome byinducing oxidative damage (pyrimidine hydrates) and cross-links (bothDNAprotein andDNA-DNA) that are responsiblefor retarding the growth and development of plants [1 6 2627] UV-B radiation damages nuclear chloroplast and mito-chondrial DNA by inducing various DNA lesions includingthe generation of cyclobutane pyrimidine dimers (CPDs) (asthe primaryUV-B-inducedDNA lesions accounting approxi-mately 75 of UV-B-mediated total DNA damage) and otherphotoproducts pyrimidine (6-4) pyrimidone dimers as themajor lesions while the minor includes oxidized or hydratedbases single-strand breaks and others [28 29]

On the perspective of the production of different types ofstructural distortions within DNA due to CPDs and 6-4PPsthe induction of a slight bending on the DNA helix has beenevidenced due to CPDs whereas 6-4PPs can produce muchmore bending and also unwinding on the DNA [1] TheseDNA lesions together can act as the principal cause of UV-B-induced growth inhibition in plants Additionally theseproducts can be lethal ormutagenic to organisms and can alsoimpede transcriptional processes and result in error-pronereplication [30ndash33] Indirect generation of reactive oxygenspecies (ROS) due to solar UV light has also been evidencedin the nucleus [34] Nevertheless ROS-accrued base andnucleotide modifications especially in sequences with highguanosine content and also strand breaks have been widelyreported and reviewed [6 30 35 36]

31 Cyclobutane Pyrimidine Dimer Cyclobutane pyrimidinedimer (CPD) is a major type of DNA damage induced byUV-B radiation CPDs constitute themajority of these lesions(approximately 75) Herein any of the diastereoisomerssuch as cistrans (relative position of pyrimidine rings) andsyn-anti (relative orientation ofC5ndashC6bonds) can be formedMoreover though cis-syn forms of CPDs are of commonoccurrence trans-syn forms are present exclusively withinsingle-strandedDNA [1 37]No or very low amounts ofCPDshave been evidenced due to lowUV-B rates (lt1 120583molmminus2 sminus1)which though below the limit of detection stimulate protec-tive and photomorphogenetic responses [38 39] eventuallyaffecting the plantrsquos resistance to UV-B stress [15 28 38]

The Scientific World Journal 3

Majorlesions

Single strand breaks (SSBs) double strand breaks (DSBs)hydrolytic depurination apyrimidinic sites

DNA damage

Cyclobutane pyrimidinedimers (CPDs) pyrimidone dimers

Pyrimidine (6-4)

IonizationUV-B

radiation

Repairpathways

Homologous recombination

Light-dependent repair(photoreactivationphotorepair)

Light-independent repair(dark repair)

Dire

ct an

dor

via

reac

tive o

xyge

n sp

ecie

s

(Chloroplast nuclear mitochondrial DNA)

Nonhomologousrecombination

Maintenance of the genomeintegrity and viability of plants

Figure 1 Mechanism of DNA damage and repair in plants


32 Pyrimidine (6-4) Pyrimidone Dimers Pyrimidine (6-4)pyrimidone dimers (6-4PPs dimers) are other major lesionscaused by UV-B radiation However the occurrence of 6-4PPs dimers is much less frequent than CPDs [6 40]TheUVradiation wavelength and sequence dependent formation ofthe 6-4PPs at adjacent TT TC and CC nucleotides has alsobeen evidenced [1] To this end in addition to being impactedby UV-B 6-4PP dimers are photoisomerized by UV-A lightresulting in the Dewar isomer [37 40]

33 Ionizing Radiation and DNA Damage A number ofalterations may take place in the IR and free radicals targetedDNA like single-strand breaks and double-strand breaks andhydrolytic depurination apyrimidinic sites and oxidativedamage to the bases and the phosphodiester backbone ofDNA are common [24 41] Gamma irradiation with differentdose rates induces different DNA damage responses inPetunia times hybrida cells [42] Double-strand breaks (DSBs)are a strikingly genotoxic form of DNA damage henceDSBs present a unique challenge to the cell The failure torepair a break in DNA has been widely evidenced to causeloss of a chromosome arm where misrepair can producetranslocations deletions and other chromosomal abnormal-ities [43 44] In addition unrepaired breaks in dividingcells can initiate cell cycle checkpoints halting divisionand consequently slowing the growth of the organism [45]However the production of aneuploid daughter cells (thatare often not viable) has been reported as nondividing cellswith DSBs [46 47] The developmental regulation of DSBrepair mechanisms in plants has also been evidenced [48]The occurrence of multiple pathways for the repair of DSBshas been reported in plants [49] Some of the major pathwaysfor DSB-repair in plants will be overviewed in the followingsections

4 DNA Damage-Repair Pathways

The repair of DNA damage is essential for the survival oforganisms while if repair does not take place genomicintegrity will not be maintained [50] To this end coor-dination between DNA replication and repair has beenconsidered essential for the maintenance of the genome [51]The UV radiation induced DNA damage and repair has beenwell studied but concrete information on the underlyingmechanisms in plant system is still lacking [51]

Information pertaining to the dynamics of DNA dam-age accumulation and molecular mechanisms that regulaterecovery from radiation injury as a function of dose rate isunsubstantiated and poorly explored [24 42] Neverthelessthe information to date available in the current contextindicates that amechanism ofDNAdamage repair in plants isvery complex which actually involvesmultiple loci Addition-ally involvement of mechanismsmdasheither similar or identicalto those regulating the integrity of foreign sequences in theplant genomesmdashhas been reported [24] In addition plantresponse to IR may also involve the activation of cell cyclecheck-points which subsequentlymay lead to theDNA repairresponse [52] The studies on 120574-rays on Populus nigra var

italica revealed that the modulation of repair mechanismsis essential for the adaptive response to IR [53] Chronicor acute irradiation exposed Arabidopsis thaliana plantsexhibited differential regulation of gene expression of DNArepair machinery [54] It is to be underlined here that theDNA damage contributed by either UV andor IR can becorrected employing a number of pathways such as directrepair photorepair (photoreactivation) base excision repair(BER) nucleotide excision repair (NER) or mismatch repair(MMR) in plants where abovementioned lesion-specificrepair pathways can reverse UVIR-induced DNA damageto preserve the genomic integrity [55ndash58] The significanceof the replicative arrest avoidance has also been evidentin plants as a potential mechanism for UV photoproducts-tolerance Moreover implication of genes isolated from themodel plant A thaliana in nucleotide excision repair ortolerance of UV-induced DNA damage was a possible resultof phenotypic characterization of plant mutants functionalcomplementation studies and cDNA analysis [57]

Major mechanisms underlying coping strategies for UV-BIR-induced DNA damage are being overviewed hereunder

41 Light-Dependent Repair (PhotoreactivationPhotorepair)The photorepair (photoreactivation) is the major pathway inplants for repairing UV-B induced low frequencies of DNAdamage (especially of UV-B induced CPDs) where the pho-tolyase mediates the major processes by absorbing blueUV-A (320ndash400 nm) light and uses the energy to monomerizedimers [1 59ndash62] There exist similar reaction mechanismsunderlying both CPD photolyases and 6-4 photolyases-mediated repair of the respective pyrimidine dimers [40 63]The occurrence of the reduced pterin MTHF in plant-CPDphotolyase activity as the second chromophore has beenevidenced [64] Photolyases bind specifically to DNA lesionsand efficiently and quickly remove the bulk of UV-inducedCPDs and (6-4)-photoproducts directly by absorbing light inthe 300ndash600 nm range [27 65 66] A number of cofactorsincluding the quality timing and quantity of photoreacti-vating light and damage levels largely modulate this repair[60 65 67] Different genotypes exhibiting sensitivity to UV-B were reported to exhibit differential ability to repair UV-B-mediated DNA damage types (such as CPDs) where UV-B =sensitive cultivars were less able to repair CPDs throughphotoreactivation than UV-B resistant cultivars [68]

To date photoreactivation and photolyases have beenextensively reported in several plant species [65ndash77] How-ever credible work has been performed on Oryza sativacultivars where photolyase has been evidenced as a majorfactor modulatingO sativa cultivar capability to repair DNAdamage types [68 76ndash79] Earlier also the sensitivity ofO sativa to UV-B radiation was reported to vary amongcultivars [78] Based on the exhibition of O sativa cultivarspotential for the level of CPD photolyase activity O sativacultivars were clearly classified into three groups which inturn depended on amino acid residues at positions 126 (UV-B resistant O sativa glutamine UV-B sensitive and UV-Bhypersensitive O sativa arginine) and 296 (UV-B resistant


and UV-B sensitive O sativa glutamine UV-B hypersensi-tive histidine) [68] It was also postulated that increasingthe activity of the photolyase enzyme in O sativa mayincrease their resistance to UV-B radiation [68 77 79] Insome recent reports UV-B sensitive O sativa cultivars wereevidenced to exhibit less capability to repair CPDs throughphotoreactivation than UV-B resistant cultivars where theauthors considered an alteration of CPD photolyase activityresulting from spontaneously occurring mutations in theCPD photolyase gene [68 76 77 79] Transgenic O sativaplants have also been successfully generated bearing theCPD photolyase gene from UV-B resistant O sativa cultivars[68 80] Overexpression of CPD photolyase in O sativaresults in higher CPD photolyase activity which resulted insignificant more resistance to UV-B induced growth damagethan wild-type plants In contrast plants with the genetransferred in the antisense orientation had significantlylower CPD photolyase activity and showed less resistanceto UV-B radiation Recently Teranishi et al [68] developedCPD photolyase overexpressing transgenic O sativa plantswith higher CPD photolyase activity using UV-B sensitiveO sativa Norin 1 (japonica) and UV-B hypersensitive Osativa Surjamkhi (indica) as parental line (PL) plants Theseresults emphasized that CPD photolyase is a crucial factorfor determining UV-B sensitivity in O sativa [68 80] Inaddition to the studies on O sativa the overexpression ofCPD photolyase in A thaliana also resulted in a moderateincrease in biomass production under conditions of elevatedUV-B radiation [17] Moreover an ecotype-specific geneticvariability in the UV-B response in A thaliana has also beenevidenced [81]

42 Light-Independent Repair (Dark Repair) The dark repairincludes nucleotide excision repair (NER) base excisionrepair (BER) mismatch repair (MMR) and other DNArepair pathways Excision repair (NER and BER) is veryimportant for maintaining genome stability and essentialfor the survival of organisms The potential mechanismsunderlying dark repair reactions have been discussed earlierextensively [40 82 83] The occurrence of light-independentrepair pathway has been evidenced in a number of plantspecies including carrot protoplasts [84 85]A thaliana [86]alfalfa seedlings [59 65] soybean chloroplasts and leaves [6087]O sativa cultivars [61] and Triticum aestivum leaf tissues[88] (reviewed by Britt et al [71] amp Tuteja et al [6]) Despitethe availability of biochemical and genetic data in favor ofsome sort of NER in plants limited information is availableconcerning the molecular characterization of plant geneproducts actively involved in dark repair [62] Compared tothe light-dependent repair (photoreactivationphotorepair)more general and flexible feature has been evidenced by thelight-independent repair (dark repair) where the recognitionand targeting of the damaged strand and subsequent removalof a 24ndash32 base oligonucleotide containing the damagedproduct and filling the gap through DNA synthesis andligation of the nicks have been reported [89 90] In contextwith NER this system has been considered the most versatilesystem for dealing with the DNA damage [91] Since NER

recognizes conformational changes in theDNAduplex ratherthan a specific type of DNA damage this system can alsorepair different types of damage [25] Moreover NER com-prises the two subpathways namely global genomic repair(GGR) and transcription-coupled repair (TCR) where GGRrepairs the DNA damage over the entire genome and TCRis selective for the transcribed DNA strand in expressedgenes [51] The wide class of helix-distorting lesions such asCPDs and (6-4) photoproducts are repaired by NER [6 27]The sequential involvement of NER-mediated recognitionof DNA damage incision on damaged strand excision ofdamage containing oligonucleotides DNA synthesis andligation has been reported [51] The conserved nature of theNER repair pathway has been proved by revealingmost of thegenes involved in NER in A thaliana [92]

BER also comprises the two subpathways namely theshort-patch BER and long-patch BER where the former isDNA polymerase (beta-dependent) and the latter is DNApolymerase (deltaepsilon-dependent) BER repairs the oxi-dized or hydrated bases and SSB Herein DNA glycosylasesinitiate this process by releasing the damaged base withcleavage of the sugar phosphate chain excision of a basicresidue or of a basic residue containing oligonucleotidesand DNA synthesis and ligation [6 27] Short-patch BERis initiated by removal of the damaged base by a DNAglycosylase enzyme that is specific for the particular baseadduct [93 94] whereas in the long-patch BER the repairis a result of nick translation reaction accompanied by stranddisplacement in the 51015840ndash31015840 direction thereby generating a flaptype of structure [95 96] The homologues of componentsinvolved in BER in O sativa and A thaliana have also beenreported [51 97ndash99]

Insertions or deletions of nucleotides (potential frameshift mutations) may be more frequent where nucleotide-repeat sequences can give rise to slip-mispairing [100]Additionally the mismatched bases also arise during recom-binationHowever themismatch repair (MMR) systems havebeen evolved to correct a large portion of these errors furtherreducing the error rate 10minus9 to 10minus10 [101] The promotion ofgenomic stability by highly conserved MMR systems via thecorrection of DNA replication errors antagonizing homeolo-gous recombination and responding to various DNA lesionshas been widely evidenced [101] MMR mechanism is highlyconserved between specieswhere it removesmajority (999)of the errors remaining after polymerase proofreading toreduce the error rate to onemisincorporated base per 109-1010nucleotides in the nascent DNA chain Moreover MMRmayalso recognize mismatches at sites of recombination betweenDNA sequences thereby it can reduce the rate of occurrenceof recombination events [101 102] Encoding a suite of MMRprotein orthologs including MSH2 the constant componentof various specialized eukaryotic mismatch recognition het-erodimers has been reported in A thaliana and other plants[101]

43 Double-Strand Breaks Repair Double-strand breaks(DSBs) have to be eliminated before genomes can be repli-cated hence genomic DSBs have been regarded as key


intermediates in recombination reactions of living organismsNevertheless the efficient repair of genomic DNA-DSBs isimportant for the survival of all organisms [103 104]Thoughthe studies on DSBs repair in animals and yeast have beencredibly performed this aspect in plants lags behind [44] Inrecent years basicmechanisms ofDSB repair in somatic plantcells have been elucidated In addition homologous recombi-nation (HR) and the nonhomologous system (NHR) are thetwo general classes of recombination to performDSBs-repairThe availability of complete sequences of A thaliana and Osativa has intensified efforts to characterize endogenous reg-ulatory components of HR and nonhomologous end joining(NHEJ) [92] HR and NHR-assisted repair of double-strandDNA breaks has been reported to control the viability underirradiation [104 105] Both HR and NHRNHEJ pathwaysare responsible for balancing genome stability against thegeneration of genetic diversity Additionally the essentialroles of HR and NHEJ have been considered vital for geneticengineering [44] Moreover there are credible reports onthe (a) isolation of radiation-sensitive plant mutants [2740 106 107] and (b) successful cloning of many plantgenes from different repair pathways involved in repair ofradiation-induced damage [108ndash111] but to date the efficiencyof NER and DSB repair and the stabilitymodification ofthese systems under chronic irradiation conditions have notbeen reported [25] Some of the specific features and overallsignificance of these two DSB-repair pathways (ie HR andNHEJ) are highlighted hereunder

44 Homologous Recombination HR has been considered asthe major pathway for maintaining the genome integrity andviability of plants where it performs mainly the error-freeDSB-repair HR uses a homologous chromosome or chro-matid as a template to recover information [43] Moreoverin HR the double-stranded gap generated by a frayed DSBis filled by copying or in some cases splicing homologoussequences from elsewhere in the genome [44] A crediblework in yeast has led to the categorization of modelspertaining to HR into three models DNA double-strandbreak repair (DSBR) model synthesis-dependent strandannealing (SDSA) and single-strand annealing (SSA) [40112 113] In brief both DSBR and SDSA are initiated by a31015840 resection forming a long single-stranded DNA tail thatinvades a homologous duplex and primes DNA synthesisbut in SDSA the newly synthesized DNA then reannealswith the other side of the DSB repairing the break andavoiding the formation of the joint molecule [40] SSA mayoccur between tandemly repeated sequences and annealhomologous regions exposed during resection A number ofplant species have been evidenced to possess DSBR SDSAand SSA HR pathways exhibiting much of the commonmolecular machineries where recombination frequencieswere reported to greatly vary from the origin of the donorand recipient sequences [40 104 114] Very rare (around 1 in10000 repair events) occurrence of HR-mediated DSB repairhas been reported in plant somatic cells via allelic sequences[115]

On the perspective of molecular mechanism of HRa number of researchers including [40 114 116] reportedor reviewed sharing of similarities in meiotic and somaticrecombination pathways at the molecular level Central tothe process of homologous recombination are the RAD52epistasis group genes (RAD50 RAD51 RAD52 RAD54RDH54TID1 RAD55 RAD57 RAD59 MRE11 and XRS2)most of which were identified by their requirement for therepair of IR-induced DNA damage in yeastThe contributionof mutations in these genes was evidenced to cause defects inmeiotic andor mitotic recombination and thus has providedevidence for a link between DSB repair (DSBR) and HR[117] Among these genes owing to severe meiotic defects Athaliana HR null mutants such as AtRAD51 AtRAD50 andAtMRE11 were reported to be completely sterile [108 118]In addition meiocytes of these mutant lines were evidencedto show extensive chromosome fragmentation leading ulti-mately to nonviable gametes because of the incapability ofthese mutants to align homologous chromosomes (synapsis)during the early stages of meiosis [108 118] Rad54 hasbeen isolated and characterized from A thaliana where itssignificance in HR was advocated [119] A weaker expres-sion of Rad54 has been evidenced earlier in irradiated Athaliana when compared to nonirradiated plants A planthomolog of Nijmegen breakage syndrome-1 gene from Ara-bidopsis (AtNbs1) and O sativa (OsNbs1) has been identifiedand their involvement in DNADSB repair was evidenced[120ndash122]

45 Nonhomologous Recombination The nonhomologousrecombination system or nonhomologous end-joining(NHRNHEJ) system also termed as ldquoillegitimate recombi-nationrdquo does not require homologous sequences rather itacts to rejoin the two end breaks and often results in deletionsor mistakes and thus mutations Although NHR is obviouslyerror prone and degraded or even inappropriate ends maybe rejoined this repair system appears to be crucial inradio-induced DSB repair in plants [40 43 44] Eventhough HR has been evidenced less efficient in DSB repair inplants the information on NHR (or NHEJ) in plants islacking [123] thus it is important to have insight into NHRpathway since genomic alterations in meristematic cells canbe transferred to the offspring [104] In somatic tissue NHEJhas been evidenced as a major pathway for DSB repair SinceNHEJ-mediated rejoining of the broken ends is associatedwith deletions of various sizes and also with insertions ofsequences (filler DNA) (that are often copied from sites closeto the DSB) and sequence similarities are not required inNHEJ for the incorporation of filler DNA into the breakNHEJ does not preserve genetic information and genomicintegrity at the break site [124] NHEJ may also differ amongspecies where an inverse correlation of deletion size togenome size has been postulated thus NHEJ significance inthe genome size evolution has been advocated [125] Detailsabout the molecular-genetics of NHEJ in eukaryotes can befound elsewhere [126]


5 Conclusion and Future Perspectives

Plant nuclear DNA is an inherently unstable molecule andcan be damaged spontaneouslymetabolically or by a numberof stress factors Though sunlight is obligatory for photosyn-thesis and survival of plants it also represents one of themajor threats to their genomic integrity Sunlight containsenergy rich UV-A (320ndash400 nm) UV-B (290ndash320 nm) andUV-C (280ndash100 nm) light While UV-C is filtered out in theatmosphere UV-B and UV-A can reach earthrsquos surface Onthe other hand IR causes water radiolysis which generateshighly reactive hydroxyl radicals DNA is the object of anattack by both UV and IR radiations leading to a numberof alterations including SSBs and DSBs The accumulationof such damages and unrecognized and unrepaired DNAdamage may cause fatal mutations which in turn can reduceplant genome stability growth and productivity and alsothreaten the organismrsquos immediate survival Plants employvarious strategies to either reverse excise or tolerate thepresence of DNA damage products The literature reviewedhere reflected the paucity of information on the basic mech-anisms underlying UV or IR mediated DNA damage andrepair compared to bacteria yeast and mammalian systemsBoth HR and NHR pathways-mediated facilitation of theprogrammed repair of DSBs have been evidenced Thusplants have become an ideal system for the identification ofgenes which are not accessible to classical genetic analysis inother systems (including mammalian model systems) Iden-tification and characterization of UVIR-sensitive mutants indifferent plant species are expected to achieve more insightsinto genetic recombinationmanipulation in plants

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

Sarvajeet S Gill and Ritu Gill would like to acknowledge thereceipt of funds from DST CSIR and UGC Government ofIndia New Delhi Narendra Tuteja acknowledges partialsupport from DST and DBT Naser A Anjum (SFRHBPD846712012) is grateful to the Portuguese Foundation forScience and Technology (FCT) and the Aveiro UniversityResearch InstituteCentre for Environmental and MarineStudies (CESAM) for partial financial supports Authorsapologize if some references related to the main theme of thecurrent review could not be cited due to space constraint

References

[1] N Tuteja P Ahmad B B Panda and R Tuteja ldquoGenotoxicstress in plants shedding light on DNA damage repair andDNA repair helicasesrdquoMutation Research Reviews in MutationResearch vol 681 no 2-3 pp 134ndash149 2009

[2] S S Gill and N Tuteja ldquoReactive oxygen species and antioxi-dant machinery in abiotic stress tolerance in crop plantsrdquo PlantPhysiology and Biochemistry vol 48 no 12 pp 909ndash930 2010

[3] S Biedermann SMooney andH Hellmann ldquoRecognition andrepair pathways of damaged DNA in higher plantsrdquo in SelectedTopics in DNA Repair C Chen Ed pp 201ndash236 InTech 2011

[4] E J Vonarx The repair and tolerance of DNA damage inhigher plants [PhD thesis] School of Biological and ChemicalSciences Deakin University Geelong Australia 2000

[5] S K Singh S Roy S R Choudhury and D N SenguptaldquoDNA repair and recombination in higher plants insights fromcomparative genomics of arabidopsis and ricerdquo BMCGenomicsvol 11 no 1 article 443 2010

[6] N Tuteja M B Singh M K Misra P L Bhalla and R TutejaldquoMolecularmechanisms ofDNAdamage and repair progress inplantsrdquo Critical Reviews in Biochemistry and Molecular Biologyvol 36 no 4 pp 337ndash397 2001

[7] W M Waterworth G E Drury C M Bray and C E WestldquoRepairing breaks in the plant genome the importance ofkeeping it togetherrdquo New Phytologist vol 192 no 4 pp 805ndash822 2011

[8] S Roy S K Singh S R Choudhury and D N SenguptaldquoAn insight into the biological functions of family X-DNApolymerase in DNA replication and repair of plant genomerdquoPlant Signaling and Behavior vol 4 no 7 pp 678ndash681 2009

[9] R G Alscher J L Donahue and C L Cramer ldquoReactiveoxygen species and antioxidants relationships in green cellsrdquoPhysiologia Plantarum vol 100 no 2 pp 224ndash233 1997

[10] J A Pyle ldquoGlobal ozone depletion observation and theoryrdquoin Plants and UV-B Responses to Environmental Change P JLumbsden Ed pp 3ndash12 Cambridge University Press Cam-bridge UK 1996

[11] J G Anderson D W Toohey and W H Brune ldquoFree radicalswithin the Antarctic vortex the role of CFCs in Antarctic ozonelossrdquo Science vol 251 no 4989 pp 39ndash46 1991

[12] R McKenzie B Connor and G Bodeker ldquoIncreased summer-time UV radiation in New Zealand in response to ozone lossrdquoScience vol 285 no 5434 pp 1709ndash1711 1999

[13] F S Xiong and T A Day ldquoEffect of solar ultraviolet-Bradiation during springtime ozone depletion on photosynthesisand biomass production of Antarctic vascular plantsrdquo PlantPhysiology vol 125 no 2 pp 738ndash751 2001

[14] G C Cannon L A Hedrick and S Heinhorst ldquoRepair mech-anisms of UV-induced DNA damage in soybean chloroplastsrdquoPlant Molecular Biology vol 29 no 6 pp 1267ndash1277 1995

[15] H Frohnmeyer and D Staiger ldquoUltraviolet-B radiation-mediated responses in plants Balancing damage and protec-tionrdquo Plant Physiology vol 133 no 4 pp 1420ndash1428 2003

[16] S Solomon D Qin M Manning et al IPCC 2007 ClimateChange 2007 The Physical Science Basis Contribution of Work-ing Group I to the Fourth Assessment Report of the Intergovern-mental Panel on Climate Change Cambridge University PressCambridge UK 2007

[17] G Kaiser O Kleiner C Beisswenger and A Batschauer ldquoIn-creased DNA repair in Arabidopsis plants overexpressing CPDphotolyaserdquo Planta vol 230 no 3 pp 505ndash515 2009

[18] R L McKenzie L O Bjorn A Bais and M Ilyasd ldquoChangesin biologically active ultraviolet radiation reaching the Earthrsquossurfacerdquo Photochemical and Photobiological Sciences vol 2 no1 pp 5ndash15 2003


[19] R P Sinha and D-P Hader ldquoUV-induced DNA damage andrepair a reviewrdquo Photochemical amp Photobiological Sciences vol1 no 4 pp 225ndash236 2002

[20] R P Rastogi A KumarM B Tyagi and R P Sinha ldquoMolecularmechanisms of ultraviolet radiation-induced DNA damage andrepairrdquo Journal of Nucleic Acids vol 2010 Article ID 592980 32pages 2010

[21] C Prinsze T M A R Dubbelman and J van Steveninck ldquoPro-tein damage induced by small amounts of photodynamicallygenerated singlet oxygen or hydroxyl radicalsrdquo Biochimica etBiophysica Acta vol 1038 no 2 pp 152ndash157 1990

[22] N Smirnoff ldquoAntioxidant systems and plant response to theenvironmentrdquo in Environment and Plant Metabolism Flexibilityand Acclimation N Smirnoff Ed pp 217ndash243 Bios ScientificPublishers Oxford UK 1995

[23] F E Quaite B M Sutherland and J C Sutherland ldquoQuan-titation of pyrimidine dimers in DNA from UVB-irradiatedalfalfa (Medicago sativa L) seedlingsrdquo Applied and TheoreticalElectrophoresis vol 2 no 6 pp 171ndash175 1992

[24] M-A Esnault F Legue andCChenal ldquoMolecularmechanismsof ultraviolet radiation-induced DNA damage and repairrdquoEnvironmental and Experimental Botany vol 68 no 3 pp 231ndash32 2010

[25] I I Boubriak D M Grodzinsky V P Polischuk et al ldquoAdap-tation and impairment of DNA repair function in pollen ofBetula verrucosa and seeds ofOenothera biennis fromdifferentlyradionuclide- contaminated sites of Chernobylrdquo Annals ofBotany vol 101 no 2 pp 267ndash276 2008

[26] A E Stapleton ldquoUltraviolet radiation and plants burningquestionsrdquoThe Plant Cell vol 4 no 11 pp 1353ndash1358 1992

[27] A B Britt ldquoMolecular genetics of DNA repair in higher plantsrdquoTrends in Plant Science vol 4 no 1 pp 20ndash25 1999

[28] C L Ballare M C Rousseaux P S Searles et al ldquoImpactsof solar ultraviolet-B radiation on terrestrial ecosystems ofTierra del Fuego (southern Argentina)mdashan overview of recentprogressrdquo Journal of Photochemistry and Photobiology B Biol-ogy vol 62 no 1-2 pp 67ndash77 2001

[29] M Takahashi M Teranishi H Ishida et al ldquoCyclobutanepyrimidine dimer (CPD) photolyase repairs ultraviolet-B-induced CPDs in rice chloroplast andmitochondrial DNArdquoThePlant Journal vol 66 no 3 pp 433ndash442 2011

[30] B Demple and L Harrison ldquoRepair of oxidative damage toDNA enzymology and biologyrdquoAnnual Review of Biochemistryvol 63 pp 915ndash948 1994

[31] J H Hoeijmakers ldquoGenome maintenance mechanisms forpreventing cancerrdquoNature vol 411 no 6835 pp 366ndash374 2001

[32] A Sancar L A Lindsey-Boltz K Unsal-Kacmaz and S LinnldquoMolecular mechanisms of mammalian DNA repair and theDNA damage checkpointsrdquoAnnual Review of Biochemistry vol73 pp 39ndash85 2004

[33] E C Friedberg G C Walker W Siede R D Wood RA Schultz and T Ellenberger DNA Repair and MutagenesisAmerican Society of Microbiology Press Washington DCUSA 2nd edition 2006

[34] B Iovine M Nino C Irace M A Bevilacqua and G Mon-frecola ldquoUltraviolet B and A irradiation induces fibromodulinexpression in human fibroblasts in vitrordquo Biochimie vol 91 no3 pp 364ndash372 2009

[35] H Wiseman and B Halliwell ldquoDamage to DNA by reactiveoxygen and nitrogen species role in inflammatory disease andprogression to cancerrdquo Biochemical Journal vol 313 no 1 pp17ndash29 1996

[36] N Tuteja and R Tuteja ldquoUnraveling DNA repair in humanmolecular mechanisms and consequences of repair defectrdquoCritical Reviews in Biochemistry and Molecular Biology vol 36no 3 pp 261ndash290 2001

[37] S Mouret C Baudouin M Charveron A Favier J Cadet andT Douki ldquoCyclobutane pyrimidine dimers are predominantDNA lesions in whole human skin exposed to UVA radiationrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 103 no 37 pp 13765ndash13770 2006

[38] B C Kim D J Tennessen and R L Last ldquoUV-B-induced pho-tomorphogenesis in Arabidopsis thalianardquo The Plant Journalvol 15 no 5 pp 667ndash674 1998

[39] H Frohnmeyer L Loyall M R Blatt and A Grabov ldquoMillisec-ond UV-B irradiation evokes prolonged elevation of cytosolic-free Ca2+ and stimulates gene expression in transgenic parsleycell culturesrdquo Plant Journal vol 20 no 1 pp 109ndash117 1999

[40] C M Bray and C E West ldquoDNA repair mechanisms in plantscrucial sensors and effectors for the maintenance of genomeintegrityrdquo New Phytologist vol 168 no 3 pp 511ndash528 2005

[41] G Slupphaug B Kavli and H E Krokan ldquoThe interactingpathways for prevention and repair of oxidative DNA damagerdquoMutation Research vol 531 no 1-2 pp 231ndash251 2003

[42] M Dona L Ventura A Macovei et al ldquoGamma irradia-tion with different dose rates induces different DNA damageresponses in Petunia x hybrida cellsrdquo Journal of Plant Physiologyvol 170 no 8 pp 780ndash787 2013

[43] J Friesner and A B Britt ldquoKu80- and DNA ligase IV-deficientplants are sensitive to ionizing radiation and defective in T-DNA integrationrdquo Plant Journal vol 34 no 4 pp 427ndash4402003

[44] E Hefner S B Preuss and A B Britt ldquoArabidopsis mutantssensitive to gamma radiation include the homologue of thehuman repair gene ERCC1rdquo Journal of Experimental Botany vol54 pp 669ndash680 2003

[45] D Lydall and T Weinert ldquoYeast checkpoint genes in DNAdamage processing implications for repair and arrestrdquo Sciencevol 270 no 5241 pp 1488ndash1491 1995

[46] O V Belyakov K M Prise K R Trott and B D MichaelldquoDelayed lethality apoptosis and micronucleus formation inhuman fibroblasts irradiated with X-rays or 120572-particlesrdquo Inter-national Journal of Radiation Biology vol 75 no 8 pp 985ndash9931999

[47] W F Morgan J P Day M I Kaplan E M McGhee and CL Limoli ldquoGenomic instability induced by ionizing radiationrdquoRadiation Research vol 146 no 3 pp 247ndash258 1996

[48] A Boyko F Zemp J Filkowski and I Kovalchuk ldquoDouble-strand break repair in plants is developmentally regulatedrdquoPlant Physiology vol 141 no 2 pp 488ndash497 2006

[49] E C Friedberg G C Walker and W Siede DNA Repair andMutagenesis American Society for Microbiology WashingtonDC USA 1995

[50] G Ries W Heller H Puchta H Sandermann H K Seldlitzand B Hohn ldquoElevated UV-B radiation reduces genome stabil-ity in plantsrdquo Nature vol 406 no 6791 pp 98ndash101 2000


[51] S Kimura Y Tahira T Ishibashi et al ldquoDNA repair in higherplants photoreactivation is the major DNA repair pathwayin non-proliferating cells while excision repair (nucleotideexcision repair and base excision repair) is active in proliferatingcellsrdquoNucleic Acids Research vol 32 no 9 pp 2760ndash2767 2004

[52] T Cools and L de Veylder ldquoDNA stress checkpoint control andplant developmentrdquo Current Opinion in Plant Biology vol 12no 1 pp 23ndash28 2009

[53] M Nishiguchi T Nanjo and K Yoshida ldquoThe effects of gammairradiation on growth and expression of genes encoding DNArepair-related proteins in Lombardy poplar (Populus nigra varitalica)rdquo Journal of Environmental Radioactivity vol 109 pp 19ndash28 2012

[54] I Kovalchuk J Molinier Y Yao A Arkhipov and OKovalchuk ldquoTranscriptome analysis reveals fundamental dif-ferences in plant response to acute and chronic exposure toionizing radiationrdquoMutation Research vol 624 no 1-2 pp 101ndash113 2007

[55] C J Norbury and I D Hickson ldquoCellular responses to DNAdamagerdquo Annual Review of Pharmacology and Toxicology vol41 pp 367ndash401 2001

[56] J Molinier M-E Stamm and B Hohn ldquoSNM-dependentrecombinational repair of oxidatively induced DNA damage inArabidopsis thalianardquoEMBOReports vol 5 no 10 pp 994ndash9992004

[57] B A Kunz H J Anderson M J Osmond and E J VonarxldquoComponents of nucleotide excision repair and DNA damagetolerance inArabidopsis thalianardquoEnvironmental andMolecularMutagenesis vol 45 no 2-3 pp 115ndash127 2005

[58] Y Zhang L H Rohde K Emami et al ldquoSuppressed expressionof non-DSB repair genes inhibits gamma-radiation-inducedcytogenetic repair and cell cycle arrestrdquo DNA Repair vol 7 no11 pp 1835ndash1845 2008

[59] F E Quaite S Takayanagi J Ruffini J C Sutherland andB M Sutherland ldquoDNA damage levels determine cyclobutylpyrimidine dimer repair mechanisms in alfalfa seedlingsrdquo PlantCell vol 6 no 11 pp 1635ndash1641 1994

[60] B M Sutherland S Takayanagi J H Sullivan and J CSutherland ldquoPlant responses to changing environmental stresscyclobutyl pyrimidine dimer repair in soybean leavesrdquo Photo-chemistry and Photobiology vol 64 no 3 pp 464ndash468 1996

[61] J Hidema T Kumagai J C Sutherland and B M SutherlandldquoUltraviolet B-sensitive rice cultivar deficient in cyclobutylpyrimidine dimer repairrdquo Plant Physiology vol 113 no 1 pp39ndash44 1997

[62] F Gallego O Fleck A Li J Wyrzykowska and B TinlandldquoAtRAD1 a plant homologue of human and yeast nucleotideexcision repair endonucleases is involved in dark repair of UVdamages and recombinationrdquo Plant Journal vol 21 no 6 pp507ndash518 2000

[63] A Sancar ldquoStructure and function of DNA photolyase andcryptochrome blue-light photoreceptorsrdquo Chemical Reviewsvol 103 no 6 pp 2203ndash2237 2003

[64] W M Waterworth Q Jiang C E West M Nikaido and C MBray ldquoCharacterization of Arabidopsis photolyase enzymes andanalysis of their role in protection from ultraviolet-B radiationrdquoThe Journal of Experimental Botany vol 53 no 371 pp 1005ndash1015 2002

[65] Q Pang and J B Hays ldquoUV-B-inducible and temperature-sensitive photoreactivation of cyclobutane pyrimidine dimersinArabidopsis thalianardquo Plant Physiology vol 95 no 2 pp 536ndash543 1991

[66] Y TakeuchiMMurakami N Nakajima N Kondo O Nikaidoand Y Takeuchi ldquoThe photorepair of photoisomerization ofDNA lesions in etiolated cucumber cotyledons after irradiationby UV-B depends on wavelengthrdquo Plant Cell Physiology vol 39pp 745ndash750 1996

[67] A E Stapleton C S Thornber and V Walbot ldquoUV-B com-ponent of sunlight causes measurable damage in field-grownmaize (Zea mays L) developmental and cellular heterogeneityof damage and repairrdquo Plant Cell amp Environment vol 20 no 3pp 279ndash290 1997

[68] M Teranishi T Taguchi T Ono and J Hidema ldquoAugmentationof CPD photolyase activity in japonica and indica rice increasestheir UVB resistance but still leaves the difference in theirsensitivitiesrdquoPhotochemical and Photobiological Sciences vol 11no 5 pp 812ndash820 2012

[69] J Hidema and T Kumagai ldquoUVB-induced cyclobutyl pyrimi-dine dimer and photorepair with progress of growth and leafage in ricerdquo Journal of Photochemistry and Photobiology B vol43 no 2 pp 121ndash127 1998

[70] T Kumagai J Hidema H-S Kang and T Sato ldquoEffects ofsupplemental UV-B radiation on the growth and yield of twocultivars of Japanese lowland rice (Oryza sativa L) underthe field in a cool rice-growing region of Japanrdquo AgricultureEcosystems amp Environment vol 83 no 1-2 pp 201ndash208 2001

[71] A B Britt J-J Chen D Wykoff and D Mitchell ldquoA UV-sensitive mutant of Arabidopsis defective in the repair ofpyrimidine-pyrimidinone(6ndash4) dimersrdquo Science vol 261 no5128 pp 1571ndash1574 1993

[72] J Hidema T Kumagai and B M Sutherland ldquoUV radiation-sensitiveNorin 1 rice contains defective cyclobutane pyrimidinedimer photolyaserdquo Plant Cell vol 12 no 9 pp 1569ndash1578 2000

[73] A-L Dany T Douki C Triantaphylides and J Cadet ldquoRepairof the main UV-induced thymine dimeric lesions within Ara-bidopsis thaliana DNA evidence for the major involvementof photoreactivation pathwaysrdquo Journal of Photochemistry andPhotobiology B Biology vol 65 no 2-3 pp 127ndash135 2001

[74] S Takahashi N Nakajima H Saji and N Kondo ldquoDiurnalchange of cucumber CPD photolyase gene (CsPHR) expressionand its physiological role in growth under UV-B irradiationrdquoPlant and Cell Physiology vol 43 no 3 pp 342ndash349 2002

[75] A Tanaka A Sakamoto Y Ishigaki et al ldquoAn ultraviolet-B-resistant mutant with enhanced DNA repair in arabidopsisrdquoPlant Physiology vol 129 no 1 pp 64ndash71 2002

[76] M Teranishi Y Iwamatsu J Hidema and T KumagaildquoUltraviolet-B sensitivities in Japanese lowland rice cultivarscyclobutane pyrimidine dimer photolyase activity and genemutationrdquo Plant and Cell Physiology vol 45 no 12 pp 1848ndash1856 2004

[77] A Yamamoto T Hirouchi T Mori et al ldquoBiochemical and bio-logical properties of DNA photolyases derived from utraviolet-sensitive rice cultivarsrdquo Genes amp Genetic Systems vol 82 no 4pp 311ndash319 2007

[78] T Kumagai and T Sato ldquoInhibitory effects of increase in near-UV radiation on the growth of Japanese rice cultivars (Oryzasativa L) in a phytotron and recovery by exposure to visibleradiationrdquo Japan Journal of Breeding vol 42 pp 545ndash552 1992


[79] J Hidema M Teranishi Y Iwamatsu et al ldquoSpontaneouslyoccurring mutations in the cyclobutane pyrimidine dimerphotolyase gene cause different sensitivities to ultraviolet-B inricerdquo Plant Journal vol 43 no 1 pp 57ndash67 2005

[80] J Hidema T Taguchi T Ono M Teranishi K Yamamotoand T Kumagai ldquoIncrease in CPD photolyase activity functionseffectively to prevent growth inhibition caused by UVB radia-tionrdquo Plant Journal vol 50 no 1 pp 70ndash79 2007

[81] I Kalbina and A Strid ldquoSupplementary ultraviolet-B irradia-tion reveals differences in stress responses between Arabidopsisthaliana ecotypesrdquo Plant Cell and Environment vol 29 no 5pp 754ndash763 2006

[82] B J V Berg andG B Sancar ldquoEvidence for dinucleotide flippingby DNA photolyaserdquo The Journal of Biological Chemistry vol273 no 32 pp 20276ndash20284 1998

[83] T Carell L T Burgdorf L M Kundu and M Cichon ldquoThemechanism of action of DNA photolyasesrdquo Current Opinion inChemical Biology vol 5 no 5 pp 491ndash498 2001

[84] G P Howland ldquoDark repair of ultraviolet induced pyrimidinedimers in the DNA of wild carrot protoplastsrdquo Nature vol 254no 5496 pp 160ndash161 1975

[85] A C Eastwood and A G McLennan ldquoRepair replicationin ultraviolet light-irradiated protoplasts of Daucus carotardquoBiochimica et Biophysica Acta Gene Structure and Expressionvol 826 no 1 pp 13ndash19 1985

[86] J B Hays ldquoArabidopsis thaliana a versatile model systemfor study of eukaryotic genome-maintenance functionsrdquo DNARepair vol 1 no 8 pp 579ndash600 2002


[88] R M Taylor O Nikaido B R Jordan J Rosamond C M Brayand A K Tobin ldquoUltraviolet-B-induced DNA lesions and theirremoval in wheat (Triticum aestivum L) leavesrdquo Plant Cell andEnvironment vol 19 no 2 pp 171ndash181 1996

[89] D P Batty and R D Wood ldquoDamage recognition in nucleotideexcision repair of DNArdquoGene vol 241 no 2 pp 193ndash204 2000

[90] O Maillard U Camenisch K B Blagoev and H NaegelildquoVersatile protection from mutagenic DNA lesions conferredby bipartite recognition in nucleotide excision repairrdquoMutationResearch vol 658 no 3 pp 271ndash286 2008

[91] I Boubriak H Kargiolaki L Lyne and D J Osborne ldquoTherequirement for DNA repair in desiccation tolerance of germi-nating embryosrdquo Seed Science Research vol 7 no 2 pp 97ndash1051997

[92] The Arabidopsis Genome Initiative (TAGI) ldquoAnalysis of thegenome sequence of the flowering plant Arabidopsis thalianardquoNature vol 408 pp 796ndash815 2000

[93] K W Caldecott ldquoMammalian DNA single-strand break repairan X-ra(y)ted affairrdquo BioEssays vol 23 no 5 pp 447ndash455 2001

[94] J C Fromme A Banerjee andG L Verdine ldquoDNA glycosylaserecognition and catalysisrdquo Current Opinion in Structural Biol-ogy vol 14 no 1 pp 43ndash49 2004

[95] J J Harrington and M R Lieber ldquoFunctional domains withinFEN-1 and RAD2 define a family of structure-specific endonu-cleases implications for nucleotide excision repairrdquo Genes ampDevelopment vol 8 no 11 pp 1344ndash1355 1994

[96] XWu J Li X Li C-L Hsieh PM J Burgers andM R LieberldquoProcessing of branched DNA intermediates by a complex ofhuman FEN-1 and PCNArdquo Nucleic Acids Research vol 24 no11 pp 2036ndash2043 1996

[97] A Klungland and T Lindahl ldquoSecond pathway for completionof human DNA base excision-repair reconstitution with puri-fied proteins and requirement forDNase IV (FEN1)rdquoTheEMBOJournal vol 16 no 11 pp 3341ndash3348 1997

[98] M-V Garcıa-Ortiz R R Ariza and T Roldan-Arjona ldquoAnOGG1 orthologue encoding a functional 8-oxoguanine DNAglycosylaselyase in Arabidopsis thalianardquo Plant Molecular Biol-ogy vol 47 no 6 pp 795ndash804 2001

[99] S Kimura and K Sakaguchi ldquoDNA repair in plantsrdquo ChemicalReviews vol 106 no 2 pp 753ndash766 2006

[100] T A Kunkel andK Bebenek ldquoDNA replication fidelityrdquoAnnualReview of Biochemistry vol 69 pp 497ndash529 2000

[101] J M Leonard S R Bollmann and J B Hays ldquoReductionof stability of Arabidopsis genomic and transgenic DNA-repeat sequences (microsatellites) by inactivation of AtMSH2mismatch-repair functionrdquo Plant Physiology vol 133 no 1 pp328ndash338 2003

[102] S-Y Wu K Culligan M Lamers and J Hays ldquoDissimilarmispair-recognition spectra of Arabidopsis DNA-mismatch-repair proteins MSH2sdotMSH6 (MutS120572) and MSH2sdotMSH7(MutS120574)rdquoNucleic Acids Research vol 31 no 20 pp 6027ndash60342003

[103] H Puchta B Dujon and B Hohn ldquoTwo different but relatedmechanisms are used in plants for the repair of genomic double-strand breaks by homologous recombinationrdquoProceedings of theNational Academy of Sciences of theUnited States of America vol93 no 10 pp 5055ndash5060 1996

[104] H Puchta ldquoThe repair of double-strand breaks in plantsmechanisms and consequences for genome evolutionrdquo TheJournal of Experimental Botany vol 56 no 409 pp 1ndash14 2005

[105] C E West W M Waterworth P A Sunderland and C MBray ldquoArabidopsis DNA double-strand break repair pathwaysrdquoBiochemical Society Transactions vol 32 no 6 pp 964ndash9662004

[106] C-Z Jiang J Yee D L Mitchell and A B Britt ldquoPhotorepairmutants of arabidopsisrdquo Proceedings of the National Academy ofSciences of the United States of America vol 94 no 14 pp 7441ndash7445 1997

[107] Z Liu J D Hall and D W Mount ldquoArabidopsis UVH3 geneis a homolog of the Saccharomyces cerevisiae RAD2 and humanXPG DNA repair genesrdquo Plant Journal vol 26 no 3 pp 329ndash338 2001

[108] J-Y Bleuyard M E Gallego F Savigny and C I WhiteldquoDiffering requirements for the Arabidopsis Rad51 paralogs inmeiosis and DNA repairrdquo The Plant Journal vol 41 no 4 pp533ndash545 2005

[109] P G Morgante C M Berra M Nakabashi R M ACosta C F M Menck and M-A van Sluys ldquoFunctionalXPBRAD25 redundancy in Arabidopsis genome characteriza-tion of AtXPB2 and expression analysisrdquoGene vol 344 pp 93ndash103 2005

[110] L Liang S Flury V Kalck B Hohn and J Molinier ldquoCEN-TRIN2 interacts with the arabidopsis homolog of the humanXPC protein (AtRAD4) and contributes to efficient synthesis-dependent repair of bulky DNA lesionsrdquo Plant MolecularBiology vol 61 no 1-2 pp 345ndash356 2006


[111] E J Vonarx E K Tabone M J Osmond H J Anderson andB A Kunz ldquoArabidopsis homologue of human transcriptionfactor IIHnucleotide excision repair factor p44 can function intranscription and DNA repair and interacts with AtXPDrdquo ThePlant Journal vol 46 no 3 pp 512ndash521 2006

[112] Y Aylon andM Kupiec ldquoDSB repair the yeast paradigmrdquoDNARepair vol 3 no 8-9 pp 797ndash815 2004

[113] B O Krogh and L S Symington ldquoRecombination proteins inyeastrdquo Annual Review of Genetics vol 38 pp 233ndash271 2004

[114] D Schuermann J Molinier O Fritsch and B Hohn ldquoThedual nature of homologous recombination in plantsrdquo Trends inGenetics vol 21 no 3 pp 172ndash181 2005

[115] B Gisler S Salomon andH Puchta ldquoThe role of double-strandbreak-induced allelic homologous recombination in somaticplant cellsrdquo Plant Journal vol 32 no 3 pp 277ndash284 2002

[116] A P Caryl G H Jones and F C H Franklin ldquoDissectingplant meiosis using Arabidopsis thaliana mutantsrdquo Journal ofExperimental Botany vol 54 no 380 pp 25ndash38 2003

[117] L S Symington ldquoRole of RAD52 epistasis group genes inhomologous recombination and double-strand break repairrdquoMicrobiology and Molecular Biology Reviews vol 66 no 4 pp630ndash670 2002

[118] J Puizina J Siroky P Mokros D Schweizer and K RihaldquoMre11 deficiency in Arabidopsis is associated with chromoso-mal instability in somatic cells and Spo11-dependent genomefragmentation during meiosisrdquo Plant Cell vol 16 no 8 pp1968ndash1978 2004

[119] K Osakabe K Abe T Yoshioka et al ldquoIsolation and characteri-zation of the RAD54 gene from Arabidopsis thalianardquoThe PlantJournal vol 48 no 6 pp 827ndash842 2006

[120] I Kovalchuk V Abramov I Pogribny and O KovalchukldquoMolecular aspects of plant adaptation to life in the Chernobylzonerdquo Plant Physiology vol 135 no 1 pp 357ndash363 2004

[121] N Akutsu K Iijima T Hinata and H Tauchi ldquoCharacteriza-tion of the plant homolog of Nijmegen breakage syndrome 1involvement in DNA repair and recombinationrdquo Biochemicaland Biophysical Research Communications vol 353 no 2 pp394ndash398 2007

[122] W M Waterworth C Altun S J Armstrong et al ldquoNBS1 isinvolved inDNA repair and plays a synergistic role withATM inmediating meiotic homologous recombination in plantsrdquo PlantJournal vol 52 no 1 pp 41ndash52 2007

[123] V Gorbunova and A A Levy ldquoNon-homologous DNA endjoining in plant cells is associated with deletions and filler DNAinsertionsrdquo Nucleic Acids Research vol 25 no 22 pp 4650ndash4657 1997

[124] W Goettel and J Messing ldquoChange of gene structure andfunction by non-homologous end-joining homologous recom-bination and transposition of DNArdquo PLoS Genetics vol 5 no6 Article ID e1000516 2009

[125] A Kirik S Salomon and H Puchta ldquoSpecies-specific double-strand break repair and genome evolution in plantsrdquoTheEMBOJournal vol 19 no 20 pp 5562ndash5566 2000

[126] E Weterings and D J Chen ldquoNon-homologous end joiningin eukaryotesrdquo in Encyclopedia of Biological Chemistry J LWilliam and M D Lane Eds pp 269ndash274 Academic PressWaltham Mass USA 2013

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of


Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology


Molecular Biology International

GenomicsInternational Journal of


The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014


BioinformaticsAdvances in

Marine BiologyJournal of



Signal TransductionJournal of


BioMed Research International

Evolutionary BiologyInternational Journal of



Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014


Genetics Research International


Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational



Enzyme Research



Microbiology


2 Ultraviolet (UV) Ionizing Radiations (IR)and Cellular DNA

Plants because of their sessile nature are especially suscep-tible to damage caused by environmental factors Thoughsunlight is obligatory for photosynthesis and survival ofplants it also represents one of the major threats to theirgenomic integrity Sunlight contains energy rich UV-A (320ndash400 nm) UV-B (290 to 320 nm) and UV-C (280 to 100 nm)light UV-C is filtered out in the atmosphere and UV-B andUV-A can reach earthrsquos surface effectively [3] Among UVradiation types UV-A radiation has been shown to haveless DNA damaging effect because it cannot be absorbed bynative DNA whereas UV-A and visible light energy (up to670ndash700 nm) can damage DNA via indirect photosensitizingreactions-mediated ROS generation especially singlet oxygen(1O2

) [9] UV-C radiation does not show much harmfuleffects on the biota since it is quantitatively absorbed byoxygen and ozone in the Earthrsquos atmosphere In the past 50years the concentration of ozone has decreased by about5 (hence significant depletion in stratospheric ozone)mainly due to the release of anthropogenic pollutants such aschlorofluorocarbons [10] Consequently a larger proportionof theUV-B spectrum reaches the Earthrsquos surface with seriousimplications on all living organisms [11ndash17]

UV-B radiation reaching the earthrsquos surface is highlyvariable and influenced by many factors including strato-spheric ozone layer and geographical area Though most ofthe extraterrestrial UV-B is absorbed by the stratosphericozone remaining UV-B can produce adverse effects ondiverse habitats [18] Anthropogenically released chlorineand fluorine-containing compounds (eg CFCs) mediatesignificant depletion of stratospheric ozone which is basicallyresponsible for increased UV-B radiation in the past decadesin particular in the Antarctic zone [11 12 16 17] AlthoughUV-B radiation has less than 1 of total solar energy it isa highly active component of the solar radiation that bringschemicalmodification inDNA[19 20]UV radiation is one ofthe most damaging agents for DNA and other biomoleculessuch as proteins and lipids [21 22] Moreover cellular DNAhas been considered an obvious key target for UV inducedgenetic damage in a variety of organisms including plants[1 23] Mechanism of DNA damage and repair in responseto UVIR radiation has been shown in Figure 1

On the perspective of IRmediatedDNAdamage in plantsit causes water radiolysis which generates highly reactiveOH∙ radicals OH∙ radicals are the most reactive among allROS and known to react with all biological molecules likeDNA proteins lipids and almost any constituent of cells Inthe absence of any enzymatic mechanism for the removal ofOH∙ excess OH∙ accumulation ultimately leads to cell deathDNA is the most preferred biomolecule being attacked byboth the OH∙ and the UV radiations (ie there is both directand indirect effect) [24] A number of alterations like SSBsand DSBs may take place in the IR and free radicals targetedDNA [24] Plants may recruit a wide variety of strategies toeither reverse excise or tolerate the presence ofDNAdamage

products [5] In this perspective though mechanisms under-lying UV and ionizing radiations-mediated DNA damageand repair have been thoroughly described in bacteria yeastand mammalian systems information on these processesin plants is scanty and unsubstantiated However the DNAdamage under UV radiation and DNA repair associatedenzymes have been shown to greatly modulate the mutationrate chromosome aberration frequencies and viability inseeds and seedlings [25]

The following sections and subsections present anoverview on UVionizing radiation-mediated DNA dam-age products and critically discuss potential biochemicaland genetic mechanisms underlying UVionizing radiationaccrued DNA damage and repair pathways

3 UV-B Radiation Accrued DNA Damage

UV-B radiation can penetrate and damage plant genome byinducing oxidative damage (pyrimidine hydrates) and cross-links (bothDNAprotein andDNA-DNA) that are responsiblefor retarding the growth and development of plants [1 6 2627] UV-B radiation damages nuclear chloroplast and mito-chondrial DNA by inducing various DNA lesions includingthe generation of cyclobutane pyrimidine dimers (CPDs) (asthe primaryUV-B-inducedDNA lesions accounting approxi-mately 75 of UV-B-mediated total DNA damage) and otherphotoproducts pyrimidine (6-4) pyrimidone dimers as themajor lesions while the minor includes oxidized or hydratedbases single-strand breaks and others [28 29]

On the perspective of the production of different types ofstructural distortions within DNA due to CPDs and 6-4PPsthe induction of a slight bending on the DNA helix has beenevidenced due to CPDs whereas 6-4PPs can produce muchmore bending and also unwinding on the DNA [1] TheseDNA lesions together can act as the principal cause of UV-B-induced growth inhibition in plants Additionally theseproducts can be lethal ormutagenic to organisms and can alsoimpede transcriptional processes and result in error-pronereplication [30ndash33] Indirect generation of reactive oxygenspecies (ROS) due to solar UV light has also been evidencedin the nucleus [34] Nevertheless ROS-accrued base andnucleotide modifications especially in sequences with highguanosine content and also strand breaks have been widelyreported and reviewed [6 30 35 36]

31 Cyclobutane Pyrimidine Dimer Cyclobutane pyrimidinedimer (CPD) is a major type of DNA damage induced byUV-B radiation CPDs constitute themajority of these lesions(approximately 75) Herein any of the diastereoisomerssuch as cistrans (relative position of pyrimidine rings) andsyn-anti (relative orientation ofC5ndashC6bonds) can be formedMoreover though cis-syn forms of CPDs are of commonoccurrence trans-syn forms are present exclusively withinsingle-strandedDNA [1 37]No or very low amounts ofCPDshave been evidenced due to lowUV-B rates (lt1 120583molmminus2 sminus1)which though below the limit of detection stimulate protec-tive and photomorphogenetic responses [38 39] eventuallyaffecting the plantrsquos resistance to UV-B stress [15 28 38]


Majorlesions


DNA damage


Pyrimidine (6-4)

IonizationUV-B

radiation

Repairpathways




Dire

ct an

dor

via

reac

tive o

xyge

n sp

ecie

s
































Acknowledgments


References










































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Majorlesions


DNA damage


Pyrimidine (6-4)

IonizationUV-B

radiation

Repairpathways




Dire

ct an

dor

via

reac

tive o

xyge

n sp

ecie

s
































Acknowledgments


References










































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology




























Acknowledgments


References










































































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology
























































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

review article dna damage and repair in plants under...

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