DNA repair and recombination in higher plants: insights from comparative genomics of arabidopsis and rice
© Singh et al; licensee BioMed Central Ltd. 2010
Received: 12 March 2010
Accepted: 21 July 2010
Published: 21 July 2010
The DNA repair and recombination (DRR) proteins protect organisms against genetic damage, caused by environmental agents and other genotoxic agents, by removal of DNA lesions or helping to abide them.
We identified genes potentially involved in DRR mechanisms in Arabidopsis and rice using similarity searches and conserved domain analysis against proteins known to be involved in DRR in human, yeast and E. coli. As expected, many of DRR genes are very similar to those found in other eukaryotes. Beside these eukaryotes specific genes, several prokaryotes specific genes were also found to be well conserved in plants. In Arabidopsis, several functionally important DRR gene duplications are present, which do not occur in rice. Among DRR proteins, we found that proteins belonging to the nucleotide excision repair pathway were relatively more conserved than proteins needed for the other DRR pathways. Sub-cellular localization studies of DRR gene suggests that these proteins are mostly reside in nucleus while gene drain in between nucleus and cell organelles were also found in some cases.
The similarities and dissimilarities in between plants and other organisms' DRR pathways are discussed. The observed differences broaden our knowledge about DRR in the plants world, and raises the potential question of whether differentiated functions have evolved in some cases. These results, altogether, provide a useful framework for further experimental studies in these organisms.
The integrity of genomes of all living organisms is continuously being challenged by different environmental agents and metabolic by-products. Consequently, evolution has provided organisms with several DNA repair and recombination (DRR) pathways to remove or to tolerate lesions in their genetic material and maintain the integrity of genome. Thus DRR is not only a fundamental cellular process for protecting cells against the damage, but is also indispensable to ensure faithful transmission of genetic information from one generation to the next. In fact, these partly redundant machineries have at least two important contrasting roles in evolution, escorting the genome, and allowing for a certain level of mutations during evolution. The decisive balance of these two activities is perhaps the best reason for the high levels of conservation observed in DRR related proteins, even across the three domains, Bacteria, Archaea and Eukarya [1–3].
The effect of environmental change on ecosystem scales responses and on the life processes of individual organisms has been a major environmental issue for the last three decades. Understanding of how species may evolve in response to environmental changes remains relatively unclear, particularly for plants. Plants, because of their intrinsic immobility, are constantly exposed to various environmental agents and endogenous processes that impose damage to DNA and cause genotoxic stress, which can reduce plant genome stability, growth and productivity. Like any other organisms plants employ a wide variety of strategies to either reverse, excise, or tolerate the presence of DNA damage products. Although repair and damage tolerance mechanisms have been thoroughly described in E. coli, Saccharomyces cerevisiae, rodents and human, surprisingly little is known about these processes in plants. However, in recent years, there has been increased interest in plant DRR and in using plants as models for understanding the under lying mechanism of DRR .
Our research interest lies mainly with understanding the coordination between replication and repair machinery in higher plant genome with special emphasis on the role of single subunit, short gap- filling family-X DNA polymerase orthologues in plant DNA replication and repair (DNA polymerase λ) [5–9]. Previously few attempts have been made to study the different repair pathway in plants at genome level but they were limited to either gene identification or single pathway only [10, 11]. Recent study has reported in detail about the core DNA replication machinery in rice and Arabidopsis. Previously, we carried out an in silico analysis to study the sequential, structural and phylogenetic features of BRCT (breast cancer susceptibility C-terminus) domain in higher plant genome and investigated the distribution of this module in various proteins in higher plants in relation to the functional significance of these proteins in plant DNA damage and repair . However detailed knowledge about the sequential, structural and evolutionary properties of the genes involved in plant DRR events is still very limited.
In this article, we have made an attempt to systemically analyze the genomes of the two fully sequenced and well explored plants, Arabidopsis (a dicot) and rice (a monocot), to investigate the presence and evolution of genes known to be involved in DRR in other organisms. We have found that some repair machinery is very well conserved in plant genomes whereas others have diverged more rapidly. In addition, several genes involved in different repair pathways are found to be duplicated in both the genomes. To further gain insight into plant DRR components, we have combined published experimental information with our own bioinformatics analysis of genomic sequence data. We observed that the genes involved in DRR are, in general, part of the cell core metabolic pathways and showed significant similarity in different genomes while intriguing differences indicating biological diversity in plant responses to DNA damage. Overall this in silico study provides important information regarding DRR pathways in plants and represents a useful starting place for further research on the functional characterization of the proteins involved in plant DNA metabolism and the evolution of DRR genes in higher plant genomes.
Results and discussion
Identification of DRR genes in rice and Arabidopsis
In order to study the conservation and evolution of DRR pathways in rice (Oryza sativa) and Arabidopsis (Arabidopsis thaliana) genomes, we examined the conservation of 229 and 223 gene models in Arabidopsis and rice respectively. Detail about every gene and number of paralogs present in Arabidopsis and rice genomes are tabulated in additional file 1 while the locus IDs and relevant plant literature (if available) is listed in additional file 2. The genomes of Arabidopsis and rice were searched for the presence of genes known to act in the metabolism of DNA lesions, mostly in human, Saccharomyces cerevisiae and E. coli. When a gene was not found, it indicates either that the gene was absent in the considered organism or that the sequence was too varied to be recognized using our criteria. Later on, genes of rice and Arabidopsis were also queried against each genome to check the consistency of the genes. Sequences were also manually checked for the presence of any wrong annotations. Few probable wrong annotations were found. For example, BLAST analysis revealed three loci, LOC_Os02g54280, LOC_Os02g54170 and LOC_Os02g54290, with significant hits for AtBRU1 in rice, a gene acts as a link between responses to DNA damage and epigenetic gene silencing in Arabidopsis. We discarded LOC_Os02g54290 because it did not contain the BRU1 specific domain. LOC_Os02g54170 was annotated as BRUSHY 1 while LOC_Os02g54280 was annotated as retrotransposon protein. CDD analysis has shown that LOC_Os02g54280 contain the BRU1 specific conserved domains, tetratricopeptide repeats (TPRs) and leucine-rich repeats (LRRs), with few additional domains like RnaseH (cd06222). LOC_Os02g54170 has shown to contain only LRRs and lack TPRs. Thus the possibility of wrong annotation for LOC_Os02g54280, as like LOC_Os02g54290, was high as it was highly similar to AtBRU1 (1.1e-140, 41.0% identity and 67.3% similar) and also contained all conserved domains. The identified DRR genes were found to be distributed on all the rice (3 to 17%) and Arabidopsis (12 to 30%) chromosomes. In rice, the highest number of DRR genes (17.48%) was predicted on chromosome 1, the longest chromosome in the rice genome. Similarly in Arabidopsis, the longest chromosomes 1 and 5 of Arabidopsis have been found to harbour the highest number of genes involved in DRR (29.91% and 23.21% respectively) (Additional file 3). Apparently, the distribution of DRR genes in terms of their involvement in different pathway seems uniform, however a strong bias towards clustering of genes involved in same pathway on different chromosome deserve special mention (Additional file 4).
In order to facilitate understanding of the major similarities and differences between two genomes, genes have been classified as: 1-Excision repair [base excision repair (BER), nucleotide excision repair (NER) and mismatch repair (MMR)]; 2- Double-Strand Break Repair [homologous recombination (HR) and non-homologous end joining (NHEJ)] and 3- Other DNA repair related genes. In the third category, we have assigned all those genes which are not catalogued in KEGG pathway database as the part of main DRR pathways.
Conservation of pathway
In terms of absence or presence of a particular protein involved in a given pathway, NER and MMR were found to be most conserved pathways where merely all components were present while NHEJ and BER were least conserved pathways of genome maintenance. All components of both sub-pathways of NER, transcription-coupled repair (TCR) and global genome repair (GGR) pathways were well conserved in both genomes except the xeroderma pigmentosum complementation group A (XPA) gene which is involved in the damage-recognition step of the NER processes, while all genes which are reported to be involved in eukaryotic MMR pathway are present in plants. Difference in term of copy number of genes as seen in BER and NER pathway was not found in MMR specific proteins may suggest the universal and utmost functional importance of this pathway. It was also found that all subunit of a multimeric protein were not conserved with similar rate during evolution. For example, POLD1 subunit of Delta-type DNA polymerase holoenzymes (pold) was always more conserved (At-Hs -54.1%, Os-Hs-55.4%) than the other subunits while POLD3 subunit was always least conserved (At-Hs -25.1%, Os-Hs -21.4%) (Figure 1). Rbx1, an ubiquitin ligase, was the most conserved gene in plant DRR pathways. Plants Rbx1 genes showed more than 80% identity to its human homolog. PCNA, DMC and RAD51A were the other much conserved proteins which showed more than 60% identity at amino acid level in plant-human pair. POLD3, PRKDC, RPA3, XRCC4 and NBS1 proteins were the least conserved genes in plant-human pair which shared less than 25% amino acid. In terms of difference in number of paralogs, MMR and NHEJ were much conserved. In both pathways, similar number of paralogs was found in Arabidopsis and rice genomes except few exceptions like MRE11 and FEN1. This result may suggest that MMR and NHEJ pathway have been naturally preserved as such through out plant genome evolution. Our analysis suggested that plant DRR machinery is more closely related to human as compared to yeast because plants retain more mammalian homologs than the yeast counterparts.
Plants homologs of bacterial DRR gene have very low sequence similarity but retention of conserved domain probably suggested the functional conservation of those proteins. Bacterial homologs were found in all pathways except NHEJ. These prokaryotic and yeast specific genes are not well explored in plant genomes except the bacterial RecA gene. RecA, a gene central to general DNA repair and recombination in bacteria, was found to be most conserved bacterial homolog in plant which showed more than 40% amino acid identity in both genomes in comparison to RecA of E. coli. Arabidopsis encodes orthologs of bacterial RecA proteins which are targeted to chloroplasts [14, 15] and mitochondria  and reported to be associated with DNA repair [16, 17]. Complexes of different proteins plays pivotal role in DNA repair processes. We found that plants appeared to retain a partner of bacterial protein complexes while loose other partners. So, in the absence of partner how these bacterial proteins work would be an important question for further investigation.
Specificities of plant DRR machinery
Functional studies of different genes involved in core DRR pathways in plants, especially Arabidopsis, underline the particular and novel behaviour of DRR in plants, amongst the higher eukaryotes. The function of different DRR pathways in plants has been more difficult to demonstrate. For instance, first step in BER is the removal of a base by a glycosylase. 8-oxo-G is the most widespread type of damage repaired by the BER pathway in DNA  and plants possess both animal (OGG1) and bacterial (FPG) homolog that remove 8-oxo-G from DNA. The reason why plants have retained these apparently redundant enzymes is not known. Several novel genes, for instance MSH7, BRU1 and RecQsim which are not present in other eukaryotes, are found to be well conserved in plants. Presence of these plant specific genes may lead to a unique DNA repair processes in plants. For instance, MSH7, a bacterial MutS homolog, has been found to be exclusive to plants. It interacts with AtMSH2, as do AtMSH3 and AtMSH6 proteins (other plant homologs of bacterial MutS). Thus it may have a role in maintaining genomic stability which is exclusive to plants .
Several mutations which are reported to be lethal in animals have been found to be non-lethal in Arabidopsis. For example, homozygous mouse knockouts for ERCC1 died before weaning  while atercc1 plants were found to be phenotypically normal in absence of exogenous DNA damaging agents . Same was true for RAD50, MRE11, RAD51, MUS81, BRCA1 and BARD1 also. CRY proteins, members of flavoproteins superfamily, are reported to be ubiquitous in all kingdoms of life. All members of this superfamily possess the characteristics of an N-terminal photolyase homology (PHR) domain. In bacteria, these enzymes mediate photoreactivation but the homologs of CRY protein, CRY1 and CRY2, in insects, animals and plants play a role in blue-light perception and circadian rhythm entrainment instead of DNA repair .
Differences in DRR machinery among plants
Despite of strong conservation of DRR proteins, we have observed intriguing difference in DRR genes in plant genomes also. This difference ranges from difference in number of homlogs to the absence or presence of a particular protein (Additional file 1). For example Arabidopsis have been found to contain two paralogous copies of xeroderma pigmentosum complementation group B (XPB), a component of the transcription factor IIH (TFIIH), gene. Analysis of the presence of XPB gene in different plant genomes including rice, Medicago trunculata, Carica papaya, Vitis venifera, Zea mays, Glycine max, sorghum and populus have indicated that beside Glycine max none of the analyzed plant genome has two paralogs for XPB genes. Both genes (Joint Genome Institute accession number-Glyma08g01970 and Glyma05g37610) of Glycine max were found to be originated from intergenomic duplication from Arabidopsis. These results indicated towards genus specific expansion of XPB and worth further investigation. FEN1, a nuclease, show an interesting pattern of evolution. All monocotyledonous genomes we analyzed, rice, Zea mays, sorghum and Brachypodium, were found to contain two copies of FEN1 and these copies were not the products of intragenomic duplication. On the other hand, all the dicotyledonous genomes that we have studied, Arbidopsis, Medicago trunculata, Vitis venifera, Glycine max and populous, have single copy of FEN1 except Glycine max. These copies of FEN1 in Glycine max were the product of intragenomic duplication and, unlike monocotyledonous FEN1 genes, acquire same node on phylogenetic tree (our unpublished data). Thus, FEN1 shows lineage specific evolution. Significant difference has also been observed in the duplication level in DRR genes of Arabidopsis and rice. Taken together, these results possibly reflecting some differences in the mechanisms and pathways by which damaged DNA are repaired by Arabidopsis and rice genomes.
Functional diversity of DRR genes
Gene duplicates and their evolution in DRR genes
In the sense of duplication, we found NER as a unique pathway where eight genes, CDK7, PCNA, RPA1, RBX, RAD23, LIG1 and DDB1, were found to be duplicated in Arabidopsis while RAD23 and DMC1 were duplicated in rice genome. CDK7, RBX1 and RAD23 paralogs were duplicated many times in course of Arabidopsis evolution. DDB1 (Ks value 0.57) and RPA1 (Ks value 0.79) duplicated quite recently than PCNA (Ks value 1.13) but the all three genes pairs retained same gene structure (Additional file 5). LIG1 duplication (Ks value 0.39) was quite newer but locus AT1G49250 showed an intron gain in comparison to locus AT1G08130. CDK7 duplicated three times. Among three gene pairs, locus AT1G18040-AT1G73690 pair appears to duplicated very recently and locus AT1G73690 maintained same gene structure as AT1G18040. On the other hand, other two pairs AT1G18040- AT1G67580 and AT1G18040-AT3G48750, ancient duplicates, showed intron loss and intron gain events during evolution. RBX1 and RAD23 showed relatively complex trend of evolution. Four paralogs of RAD23 are present in Arabidopsis which appear to be originated in different duplication events. Gene pair, locus AT1G16190-AT1G79650 (RAD23A-RAD23B) duplicated recently (Ks value 0.6) and retained the similar gene structure. Locus AT3G02540, RAD23C, was involved in two different duplication events with AT5G16090, RAD23A, (Ks value 0.63) and AT5G38470, RAD23 D, (Ks value 1.49) at two different times. It was worth notice that RAD23C - RAD23 D pair, an ancient duplication event, retained the same gene structure but RAD23C - RAD23A differ in their gene structure. Among rice RAD23 paralogs, loci LOC_Os08g33340 and LOC_Os09g24200 were found to be duplicated to each other and maintained the similar gene structure (Figure 4b, Additional file 5).
Beside the above discussed genes, Muts like protein (in MMR), RAD21 (in NHEJ), RecQl4 and RecA (in HR) UBC1, UBE2N and MMS2 (in RAD6 pathway), CHEK1, CHEK2, CLK2A, PR19A/PUB60-1, AXR1, SMC2 and SMC3 (in other conserved DNA damage response genes) were found to be duplicated in Arabidopsis at different time during evolution (Additional file 5). Among these genes, RecQl4, SMC2 and MMS2 of Arabidopsis deserve special description because of their complex mode of evolution. Two loci, AT1G10930 and AT1G60930, were predicted as putative candidates for RecQl4 in Arabidopsis. Both loci appear to be duplicated recently while the locus AT1G10930 was duplicated from locus AT3G05740, candidate gene for RecQI1, very earlier and acquire many introns and different function also (Figure 5b). Functional diversion of these two loci, AT1G10930 and AT1G60930, has been discussed in great detail else where . The similar kind of evolution pattern was also found in SMC2 and SMC3 where both candidate gene for SMC2, AT3G47460 and AT5G62410, were duplicated recently while locus AT5G62410 itself duplicated from locus AT2G27170, SMC3, (Figure 4c and Figure 5c). MMS2 (UEV1) gene family has four members and all of them were duplicated in pair-wise manner to each other. This assumption was also supported by the phylogenetic analysis data where duplicated pair acquires the nearest nodes of its duplicated partners (Figure 4d). In Rice, UBC, SSPR1 and CHEK1 genes were found to be duplicated and surprisingly most of the genes maintained the same gene structure.
DRR in chloroplast and mitochondria
We have utilized the benefits of presence of whole genome sequence of rice and Arabidopsis to analyze the uniformity and ubiquity of DRR genes and pathways in higher plant genome. Additionally, extension of many previously reported components have facilitated comparison within plants and between plants and other eukaryotes. Through genome-wide bioinformatic analysis and a comprehensive review of the existing literature, we have described that the core DRR machinery is highly conserved across plant species and displays many features in regular with other eukaryotes and some characteristics that are unique to plants. The absence and the presence of certain genes are discussed and predictions are made considering the particular aspects of the human/Saccharomyces cerevisiae/E. coli. The detected similarity and differences broaden present information about what is known for DRR in the plants, and offer a constructive framework for further experimental studies in these organisms. Generalization to other plant species is affirmed by the inclusion of both a monocot and a dicot in this analysis. Finally, extensive comparison of rice and Arabidopsis genome in respect to presence and absence of DRR genes may help understanding the basic difference between monocots and dicots. Furthermore, the datasets provided can serve as valuable source for further comparative, evolutionary and functional studies. A detailed understanding of the core DRR machinery in plants will 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.
Identification of DRR genes
All the annotated gene and protein sequences of rice chromosomes (TIGR release 6) were downloaded from The Institute for Genomic Research (TIGR) Rice Genome Annotation website . For Arabidopsis, all the annotated gene and protein sequences (TAIR release 8) were downloaded from The Arabidopsis Information Resource (TAIR) database . The redundant and genes annotated as transposable elements were removed to get a final list of non-redundant genes in rice and Arabidopsis. To identify DRR genes we used two different criteria. To select the correct putative orthologue first, we performed global alignments using the FASTA BLAST suit  and rejected all alignments with less than 20% identity, unless a portion of the protein showed a very strong similarity. Secondly, a possible conserved motif was searched using the Conserved Domain Database (CDD) . When none of these two approaches produced significant result, the corresponding gene was discarded. Primarily, Potential DRR genes in rice and Arabidopsis genome were identified by sequence similarity searches using the DNA repair genes of human, Saccharomyces cerevisiae and E. coli as seed sequences orthologs and keyword searches. Secondly Arabidopsis DRR genes were used to identify the putative DNA repair genes in rice genome. We, next, we searched the primary literature, and when presented, included experimental results that concerned to plant systems to authenticate the annotation. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway database  was used as guide for the gene involve in main repair and recombination pathway while we follow the classification of Wood et al. for the DNA repair genes.
Analysis of DRR genes
The percentage of amino acid identity between a given human/Saccharomyces cerevisiae/E. coli gene and its corresponding orthologue in Arabidopsis and rice was obtained from the Smith-Waterman alignment between the two sequences. Means were calculated using these values.
Duplicated genes and their Ka, Ks and e-values in DRR proteins of rice, Arabidopsis, sorghum and populus were extracted out from the Plant Genome Duplication Database (PGDD) . PGDD is a public database to identify and catalogue plant genes in terms of intra or inter-genome syntenic relationships.
Phylogenetic trees were generated for a group of DNA repair protein homologs. Protein sequences were aligned using the Clustal W multiple sequence alignment program . Only unambiguously aligned positions (excluding poorly conserved and gap regions) were used in phylogenetic analysis, which was performed using the MEGA4 . Neighbor-Joining and Parsimony methods were used for phylogenetic tree searching and inference. The phylogenetic trees were tested by bootstrap analysis with 10000 replications and strict consensus trees were constructed. Similar topologies were found for both algorithms employed, and only Neighbor-Joining being displayed. We used PGDD naming convention for the populus and sorghum dataset in this analysis as the original naming style for predicted models were un-informative. The respective accession numbers used in this analysis and the original naming of predicted genes are given in Additional file 9.
Functional diversity of DRR proteins was carried out according to the GO rules using the gene ontology tools at http://www.agbase.msstate.edu. Only two independent sets of ontologies were used to describe a gene product: (1) the biological process in which the gene product participates and (2) the molecular function that describes the gene product activities.
Additional methods are given in Additional file 10.
SKS, SR and SRC thank UGC, DST and CSIR, Govt. of India respectively for providing the financial assistance. We are thankful to Dr. Shrihari Sonawane and Mr. Ranjan Das for critical discussion in different aspects of this work.
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