Plant Signaling & Behavior 6:1, 120-122; January 2011; © 2011 Landes Bioscience
Understanding DNA repair and recombination in higher plant genome Information from genome-wide screens in Arabidopsis and rice Sanjay Kumar Singh,1 Swarup Roy Choudhury,1,† Sujit Roy2,* and Dibyendu N. Sengupta1 Division of Plant Biology; 2Protein Chemistry Laboratory; Department of Chemistry; Bose Institute; Kolkata, West Bengal, India Present Address: Donald Danforth Plant Science Center; St. Louis, MO USA
1 †
Key words: arabidopsis, DNA repair, gene duplication, recombination, rice Abbreviations: DRR, DNA repair and recombination; NER, nucleotide excision repair; MMR, mis-match repair; NHEJ, non-homologous end joining; BER, base excision repair Submitted: 11/17/10 Accepted: 11/17/10 DOI: 10.4161/psb.6.1.14215 *Correspondence to: Sujit Roy; Email:
[email protected] Addendum to: Singh S, Roy S, Roy Choudhury S, Sengupta DN. DNA repair and recombination in higher plants: insights from comparative genomics of arabidopsis and rice. BMC Genomics 2010; 11:443; PMID: 20646326; DOI: 10.1186/1471-2164-11-443.
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Recently we have reported the in silico identification and in depth analysis of genes potentially involve in DNA repair and recombination (DRR) in two fully sequenced higher plant genomes, Arabidopsis and rice.1 In spite of strong conservation of DRR gene along with all three domain of life, we found some peculiar difference in presence and function of DRR genes in plants. Beside the eukaryotic homologs, several prokaryote-specific genes were also found to be well conserved in both plant genomes. Several functionally important DRR gene duplications were found in Arabidopsis that do not occur in rice. In spite of the fact that same DRR protein functions in different DNA repair pathways, we found that proteins belonging to the nucleotide excision repair (NER) pathway were relatively more conserved than proteins needed for the other DRR pathways. Identified DRR gene were found to reside in nucleus mainly while gene drain in between nucleus and cell organelles were also found in some cases. Here, we have discussed the peculiar features of DRR genes in higher plant genomes. Plant Genome and Maintenance of the Genome Integrity DNA is the repository of hereditary information and the blueprint for operation of individual cells and, probably, this is the reason that DNA is the only biomolecule that is specifically repaired while all others are replaced. Despite stable genomes of all living organisms, they are subject to damage by exogenous environmental agents
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(e.g. UV and ionizing radiations, chemical mutagens, fungal and bacterial toxins etc.) and endogenous agents (e.g. free radicals or alkylating agents generated in metabolism and replication errors).2 The DNA lesions could be altered base, missing base, mismatch base, deletion or insertion, linked pyrimidines, strand breaks, intraand inter-strand cross-links and these lesions can be removed by repair, replaced by recombination or retained, leading to genome instability or mutations or carcinogenesis or cell death (Fig. 1). Plants, because of their as sessile and phototrophic nature of lifestyle, are bound to expose to different environmental agents and endogenous processes that impose damage to DNA and cause genotoxic stress, which can lessen genome stability. DNA damage results in various physiological effects, such as reduced protein synthesis, cell membrane destruction and damage to photosynthetic proteins, which affects growth and development of the whole organism.3 Like any other organisms, plants employ a wide variety of strategies to cope with these genotoxic hazards.4 In recent years, there has been increased interest in plant DRR mechanism and in using plants as model for understanding these processes5,6 but plant DRR genes are still not explored as much as human, rodents, yeast or microorganism counterpart. Plants as a Model System for Study of DRR With the availability of complete plant genome sequences, the focus has shifted
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article addendum
Figure 1. Arabidopsis mutants of DNA repair and recombination genes.
to plant functional genomics.7,8 Ingenious use of a variety of techniques has led to the identification of several genes and regulatory elements in plants especially in rice and Arabidopsis. Recent functional studies have begun to shed light on how plants cope with DNA damage caused by exoand/or endogenous factors. The genome of the plant encodes orthologs of most proteins used by eukaryotes to maintain genomic integrity.1 Beside the conservation of mammalian orthologs of genomemaintenance proteins, plant DNA repair and mutation-antagonism functions match considerably with their mammalian
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counterparts.9 Several DRR genes mutant line which leads to embryonic lethality or infertility in mammals have proved to be tolerated by plants1 (Fig. 1). Considering these facts, plants can be superb model to study the DRR because of their high tolerance to DRR gene mutations and considerable homology with mammalian DRR proteins. Lessons from Arabidopsis and Rice Genome Our recent observations involving in silico analysis of genome of two well explored
plant models, Oryza sativa and Arabidopsis thaliana, have shown that both genomes retain most of the eukaryotic DRR genes.1 Several prokaryotic DRR genes were also identified in both genomes. In addition to interconnectedness in DRR pathways, NER pathway was more conserved than others in terms of amino acid identity. All genes of NER pathway showed a high degree of sequence similarity with their counterparts present in other genomes. In terms of absence or presence of a particular protein involved in a given pathway, NER and mis-match repair (MMR) pathways were found to be most preserved
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where merely all components were present while non-homologous end joining (NHEJ) and base excision repair (BER) pathways were least conserved. Plant DRR machinery was found to be more closely related to human as compared to yeast because both plant genomes were found to retain more mammalian homologs than the yeast counterparts. Although plants genomes have several homologs of bacterial DRR gene but they show very little sequence similarity with bacterial DRR genes. Bacterial homologs were found in all pathways except NHEJ. Despite of strong conservation of DRR proteins, intriguing difference in DRR genes in plant genomes were also observed. These differences include extensive duplication and lineage specific expansion of a particular DRR gene e.g. FEN1. Many DRR proteins were predicted to function in a number of diverse activities unrelated to their DRR processes which suggests their probable role in normal plant growth and development. Sub-cellular prediction studies suggested that 17% and 10% of all DRR genes in Arabidopsis were of chloroplast and mitochondrial origin respectively while 19% and 17% of rice
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DRR genes were of chloroplast and mitochondrial origin respectively. Four and eight genes among identified prokaryotic specific genes were predicted to be localize outside the nucleus. Conclusions and Perspective In spite of increasing interest in plant DRR machinery, there is still limited knowledge about plant DRR. The datasets provided in our study can serve as valuable source for further comparative, evolutionary and functional studies. A detailed understanding of the core DRR machinery in plants provide researchers with an important tool for understanding what makes plants unique with respect to repair and developmental competence and for investigating how plant genome maintenance strategies differ from the mechanisms employed by animals. Significant difference in the duplication level in DRR genes of Arabidopsis and rice and lineage specific evolution of some DRR genes can be an interesting subject of study for the evolutionary biologists. The presence of prokaryotic specific genes in nuclear genome is another interesting point raised
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in this study. Intriguing differences in Arabidopsis and rice DRR genes can also raise a question that whether both genomes implement some specific mechanism to cope with DNA damages and needs further detail studies. References 1. Singh S, Roy S, Roy Choudhury S, Sengupta D. DNA repair and recombination in higher plants: insights from comparative genomics of Arabidopsis and rice. BMC Genomics 2010; 11:443. 2. Hoeijmakers J. Genome maintenance mechanisms for preventing cancer. Nature 2001; 411:366-74. 3. Britt A. Molecular genetics of DNA repair in higher plants. Trends Plant Sci 1999; 4:20-5. 4. Kimura S, Sakaguchi K. DNA repair in plants. Chem Rev 2006; 106:753-66. 5. Tuteja N, Ahmad P, Panda B, Tuteja R. Genotoxic stress in plants: Shedding light on DNA damage, repair and DNA repair helicases. Mutat Res Rev Mut Res 2009; 681:134-49. 6. Kunz B, Anderson H, Osmond M, Vonarx E. Components of nucleotide excision repair and DNA damage tolerance in Arabidopsis thaliana. Environ Mol Mutagen 2005; 45:115-27. 7. Langridge P, Fleury D. Making the most of ‘omics’ for crop breeding. Trends Biotechnol 2010; In Press. 8. Holtorf H, Guitton MC, Reski R. Plant functional genomics. Naturwissenschaften 2002; 89:235-49. 9. Hays JB. Arabidopsis thaliana, a versatile model system for study of eukaryotic genome-maintenance functions. DNA Repair 2002; 1:579-600.
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