Evolution of Parallel Spindles Like genes in plants and highlight of unique domain architecture#
© Cigliano et al; licensee BioMed Central Ltd. 2011
Received: 26 November 2010
Accepted: 24 March 2011
Published: 24 March 2011
Polyploidy has long been recognized as playing an important role in plant evolution. In flowering plants, the major route of polyploidization is suggested to be sexual through gametes with somatic chromosome number (2n). Parallel Spindle1 gene in Arabidopsis thaliana (AtPS1) was recently demonstrated to control spindle orientation in the 2nd division of meiosis and, when mutated, to induce 2n pollen. Interestingly, AtPS1 encodes a protein with a FHA domain and PINc domain putatively involved in RNA decay (i.e. Nonsense Mediated mRNA Decay). In potato, 2n pollen depending on parallel spindles was described long time ago but the responsible gene has never been isolated. The knowledge derived from AtPS1 as well as the availability of genome sequences makes it possible to isolate potato PSLike (PSL) and to highlight the evolution of PSL family in plants.
Our work leading to the first characterization of PSLs in potato showed a greater PSL complexity in this species respect to Arabidopsis thaliana. Indeed, a genomic PSL locus and seven cDNAs affected by alternative splicing have been cloned. In addition, the occurrence of at least two other PSL loci in potato was suggested by the sequence comparison of alternatively spliced transcripts.
Phylogenetic analysis on 20 Viridaeplantae showed the wide distribution of PSLs throughout the species and the occurrence of multiple copies only in potato and soybean.
The analysis of PSLFHA and PSLPINc domains evidenced that, in terms of secondary structure, a major degree of variability occurred in PINc domain respect to FHA. In terms of specific active sites, both domains showed diversification among plant species that could be related to a functional diversification among PSL genes. In addition, some specific active sites were strongly conserved among plants as supported by sequence alignment and by evidence of negative selection evaluated as difference between non-synonymous and synonymous mutations.
In this study, we highlight the existence of PSLs throughout Viridaeplantae, from mosses to higher plants. We provide evidence that PSLs occur mostly as singleton in the analyzed genomes except in soybean and potato both characterized by a recent whole genome duplication event. In potato, we suggest the candidate PSL gene having a role in 2n pollen that should be deeply investigated.
We provide useful insight into evolutionary conservation of FHA and PINc domains throughout plant PSLs which suggest a fundamental role of these domains for PSL function.
Polyploidy represents the occurrence of more than two complete sets of chromosomes in an organism and has long been recognized as playing an especially important role in plant evolution . In flowering plants, polyploidy extent has been largely underestimated in terms of its commonality. Indeed, major recent advances in genomic analysis has revealed that almost all angiosperms have experienced at least one round of whole genome duplication during their evolution.
The wide spreading of polyploidy throughout the angiosperms can be related to their highly plastic genome structure, as inferred from their tolerance to changes in chromosome number, genome size and epigenome . Although information with regard to the modes of polyploidization is limited, the major route of polyploidization seems to be sexual through the functioning of gametes with somatic chromosome number (2n gametes) . Indeed, sexual polyploidization as compared to asexual would explain better the success of polyploid species in terms of higher fitness and more genetic flexibility. The control of 2n gamete formation has been generally attributed to the action of single recessive genes. These genes exhibit incomplete penetrance and variable expression that is significantly influenced by genetic, environmental and developmental factors . The molecular mechanisms leading to 2n gametes have only recently begun to be uncovered [5, 6]. In particular, d'Erfurth and colleagues  isolated and characterized Parallel Spindle1 gene in Arabidopsis thaliana (AtPS1) that controls diploid pollen formation through spindle orientation in the second division of meiosis. The occurrence of parallel spindles at meiosis II is a frequently found mechanism for 2n pollen formation that was described in potato many decades ago [8, 9]. In potato, ps mutants have been used for breeding purposes in order to introgress beneficial traits from diploid (2n = 2x = 24) relatives into cultivated strains . However, the gene ps leading to 2n pollen via parallel spindles was not isolated, so far.
Interestingly, AtPS1 is a protein which contains contemporarily a ForkHead Associated domain (FHA), and a C-terminal PilT N-terminus domain (PINc). So far, the FHA domain has been found in more than 5600 different proteins from prokaryotes to higher eukaryotes involved in several processes including cell cycle control, DNA repair, protein degradation, transcription and pre-mRNA splicing . FHA domain was shown to recognize phosphothreonine-containing epitopes . PINc domain has been found in more than 3600 proteins in all life kingdoms. PINc domain has RNA nuclease activity . In eukaryotes, PINc-containing proteins, such as human SMG6 and SMG5, were linked to Nonsense-Mediated mRNA Decay (NMD), that recognizes and rapidly degrades mRNAs containing Premature translation Termination Codons (PTCs).
In this study, a sequence-homology-based strategy was carried out to isolate PS gene from a diploid potato. Through this approach, a genomic locus PS-Like (PSL) and seven cDNAs affected by alternative splicing have been cloned. The occurrence of at least two other PSL loci is suggested in potato. In order to shed light on the evolution and function of PSL genes in plants, a phylogenetic analysis of PSL genes was performed and FHA/PINc domains were compared. As far as we know, this is the first report about the isolation and characterization of PSL in a crop. We also demonstrate the conservation of this gene family throughout plants.
Cloning and characterization of PSLgenes in potato
Given the meiotic function of AtPS1, potato PSL1 cDNA was isolated from pre-bolting buds. Seven different cDNAs ranging from 2.3 to 2.7 Kbp were isolated including PSL1a of 2.4 Kbp corresponding to PSL1_pred. The sequence alignment between cDNAs and the genomic PSL1 indicated the presence of different groups of related PSL sequences encoded by more than one locus (Figure 1A). In order to investigate the relationship between the different PSL cDNAs, we conducted a phylogenetic analysis that suggested the existence of three different loci named PSL1, PSL2 and PSL3 (Figure 1B). On the basis of sequence similarity, we assigned PSL1a, PSL1b and PSL1c cDNAs [GenBank:HQ418835, GenBank:HQ418836 and GenBank:HQ418837] to genomic PSL1, PSL3a, PSL3b and PSL3c cDNAs [GenBank:HQ418839, GenBank:HQ418840 and GenBank:HQ418841] to PSL3 and the last cDNA to PSL2 [GenBank:HQ418838]. Moreover, the distance measured as the number of different nucleotides among the seven cDNAs showed that PSL2 was more similar to PSL3 than to PSL1 (Figure 1C). The nucleotide comparison between the predicted phuPSL cDNA and PSL1a, PSL2 and PSL3c cDNAs showing a similarity of 98.5%, 99.1% and 99.6%, respectively, suggested that phuPSL locus corresponds to PSL3 being the differences explained by the different genetic background.
Based on the sequences of cloned PSL cDNAs, PSL1b and PSL1c, PSL3a and PSL3b are alternative splicing forms of PSL1 and PSL3 since they retained complete or partial introns causing the formation of premature stop codons (PTCs) (Figure 1A). Moreover, the cloned PSL2 cDNA showed a PTC caused by the retention of the second intron. As a consequence, all the predicted PSL proteins, except pPSL1a and pPSL3c, had truncated or lacking PINc domain (Figure 1D).
In order to evaluate whether the alternative splicing PSL variants were possible target of degradation through NMD we calculated the distance between PTCs and the successive exon-exon junction. Being this distance more than 50-55 nt according to Nagi and Maquat  we could consider PSL1b, PSL1c, PSL2, PSL3a and PSL3b as target of NMD.
Phylogenetic analysis of PSL genes in sequenced Viridaeplantae
In order to investigate the evolution of PSL family, a phylogenetic analysis was performed by a search on Interpro (http://www.ebi.ac.uk/interpro) for proteins with both FHA and PINc domains. Interestingly, these domains were contemporary present only in plants, except for the multidrug-efflux transporter NAEGRDRAFT_78193 from the amoeboid Naegleria gruberi.
Analysis of FHA and PINc secondary structure and active sites in PSL proteins
Selective pressure among amino acid sites in the PSLfamily
In this work, we isolated PSL genes in a diploid potato (2n = 2x = 24) and through in silico analysis we identified PSL in other plant species. The function of PSL in plants can be inferred from Arabidopsis study on AtPS1 gene that appears responsible for the spindle orientation at meiosis II playing a regulatory function, likely via RNA decay .
In all the analysed species, except soybean and potato, PSL loci appear as singleton behaving as resistant to duplication. It is known that angiosperms are mostly paleopolyploids , many having survived multiple duplication events . Analysis of genome sequences shows that some genes duplicate and persist as multiple copies after whole genome duplication (WGD) while other genes are iteratively returned to singleton status. Moreover, it seems that the singleton status is consistently restored for some functional gene groups like those involved in DNA repair or signal transduction . The evolutive history of potato and soybean could explain the expansion of PSL genes occurring in these species that have experienced recent WGD. In cultivated potato (2n = 4x = 48), WGD is reported to have occurred about 10 million of years ago (mya) after the divergence from Solanum lycopersicum . In soybean (2n = 2x = 40), which seems to be an ancient allopolyploid on the basis of two different centromeric repeat classes , two rounds of WGD happened the latter aging 10-15 mya [24, 25]. In addition, the location of the four soybean PSLs on different chromosomes reinforce their origin from WGD rather than tandem duplications.
The evident feature of PSL proteins is the contemporary presence of FHA and PINc domains. FHA is reported as a phosphothreonine (pT) binding domain showing a 11 beta-sandwich secondary structure, also containing small helical insertions between the beta-strands . The FHA active sites are usually located in the loops connecting b3/b4, b4/b5 and b6/b7 strands. RAD53pFHA arginine-70, serine-85 and asparagine-107 (corresponding to arginine-6, serine-21 and asparagine-60 in Figure 5) are involved in the interaction with the phosphopeptide backbone. Arginine-83 (corresponding to arginine-19 in Figure 5) is the most important aminoacid for FHA binding specificity. Indeed, its conversion to glycine shifts the binding from pTXXD to pTXXI peptides in RAD53pFHA interaction experiments using surface plasmon resonance . Glycine-69 and histidine-88 (corresponding to glycine-5 and histidine-24 in Figure 5) stabilize the architecture of the binding site. The remaining conserved residue, asparagine-112 (corresponding to asparagine-65 in Figure 5), is remote from the peptide binding site and serves to tether the beta turn between b7/8 to b10 [12, 15]. The comparison of predicted secondary structure in our dataset showed a wide conservation among plant species regarding the number and the position of the beta-sheets and the presence of an helical insertion between the second and the third beta-sheet as a characteristic feature of monocot PSL proteins. The comparison of active sites showed that two PSLFHA residues involved in pT binding as well those involved in stabilisation of the architecture of the binding site are fully conserved except for asparagine-65 that is replaced with a different polarity residue (arginine) in AlPSL1, AtPS1, GmPSL3 and GmPSL4 with unknown possible effect on domain architecture. Moreover, as compared to RAD53pFHA, a conserved substitution in plants is a histidine instead of asparagine-60, known to be important for the selectivity of binding of phosphothreonine upon phosphoserine. The different polarity between these two residues might suggest a functional diversification of this active site. However, the consequences of this substitution in PSLFHA domain in terms of ligand binding cannot be easily predicted and should be assessed by protein:protein interaction analysis. It is also intriguing the lack of arginine-19 in plants raising the question of binding selectivity for plant PSLFHA.
As regards PINc domain, we made reference to human SMG6PINc which has RNAse activity and it is composed of alternating beta-sheets and alpha-helices. It is reported that hSMG6 is involved in NMD together with hSMG5 and hSMG7 . In Arabidopsis, AtSMG7 was proved to be involved in NMD and to be required for meiotic spindle organization in meiosis II . As reported by Glavan and colleagues , hSMG6 and other PINc domains show three conserved aspartic residues at positions 1251, 1353 and 1392 (corresponding to aspartate-6, -194 and -233 in Additional File 2) involved in Mg2+ binding. Threonine or serine embedded in the motif (T/S) XD is proposed to be the catalytic site on the basis of sequence alignment of PIN domains and it is located at residue-1390 (corresponding to threonine-231 in Figure 7) in hSMG6PINc.
Our results showed differences of secondary structures in PSLPINc domains even between phylogenetically close organisms. Moreover, the typical alternation between beta-sheets and alpha-helices does not seem to be respected. In spite of these differences, the active sites showed a wide conservation among plants. The aspartate-6 is conserved in all proteins except for SbPSL1 and SiPSL1 where an asparagine is present. This substitution maybe occurred after the divergence of BEP from PACCAD clades among Poaceae given its absence in Oryza sativa, Brachypodium distachyon and Selaginella moellendorffii. The residue-194 showed the major degree of variation among the species mostly characterized by glutamate instead of aspartate. This substitution is not related to phylogenesis, being glutamate present in both monocots and dicots while aspartate-194 is shared by the Brassicaceae BrPSL1, the Selaginellaceae SmPSL1 and the Solanaceae PSL3c. In Carica papaya, Mimulus guttatus and Medicago truncatula the change involved aminoacids with a different polarity such as lysine, alanine, and asparagine. The aspartate-233 is widely conserved among PSL proteins, except those of Poaceae OsPSL1, SiPSL1 and BdPSL1 showing a serine-233, likely a substitution occurred after the separation of monocots from dicots. GmPSL3 and SbPSL1 lack this residue due to PINc domain truncation at leucine-203 and lysine-227, respectively. As compared to hSMG6, the majority of plants showed a serine instead of threonine-231 that is present only in PtPSL1, SiPSL1, SmPSL1 and VvPSL1. This substitution should not compromise the PINc activity since serine and threonine are the most represented residues at this position in PINc domains of different organisms . Based on the evidence that the three aspartate residues of PINc domain are crucial for RNase activity, we can argue that PSLs lacking one of these residues or showing aminoacid with different polarity (BdPSL1, CpPSL1, CsPSL1, GmPSL3, MgPSL1, MtPSL1, SbPSL1, SiPSL1, OsPSL1) have no enzymatic activity. However, we cannot exclude that they are partners of other proteins retaining RNAse activity. Indeed, in human, it is known that hSMG5 lacking two aspartate residues respect to hSMG6 has no enzymatic activity but the interaction between hSMG5 and hSMG7 led to a functional nuclease activity of SMG7-SMG5 complex .
Functional analysis of Arabidopsis PS1 reinforced the evidence that the defects in meiotic spindle orientation in meiosis II led to the formation of diplopollen. Among the analysed species, Manihot esculenta (2n = 2x = 36) was reported to produce 2n pollen but the cytological mechanisms underlying its formation were not deeply investigated . Since the predicted MePSL protein has FHA and PINc active sites similar to those of other species, it is likely that the mechanism leading to 2n pollen in Manihot esculenta does not involve parallel spindles.
In the potato genotype analysed in this study, neither spindle defects nor 2n pollen have been reported . In this genotype, we identified three PSL loci and seven transcripts. Based on AtPS1 characterized by FHA and PINc domains we can suspect that PSL1a and PSL3c, carrying both domains, are functional proteins. In addition, it can be speculated that PSL1a that evidences the same PINc active residues of AtPS1 is the strongest candidate for the regulation of spindle orientation in meiosis II. The landscape of alternative splicing in potato PSL is not surprising since it has been already observed for genes involved in Arabidopsis meiosis. For instance, AtSPO11-1, involved in double strand breaks (DSBs) required for meiotic recombination, exhibits up to ten splicing forms showing PTCs . As inferred for AtSPO11-1, PSLs are possible target of NMD that could act as a post-transcriptional regulatory pathway for the proper expression of PSL. Alternative splicing was observed also in Glycine max but the lack of PTCs exclude NMD regulation of PSL transcripts. Defining the ligands of FHA and PINc domains and proving PSL as a component in NMD are essential to link PSLs to plant evolution by polyploidization via 2n gametes.
In this study, we show that PSLs are common genes across Viridaeplantae. We provide evidence that PSLs occur mostly as singleton in the analyzed genomes except in soybean and potato both characterized by a recent event of whole genome duplication. We provide useful insight into evolutionary preservation of FHA and PINc domains throughout plant PSL genes, suggesting a fundamental role of these domains for PSL function. FHA appeared to be highly conserved, while PINc secondary structure and specific active sites showed a less conserved landscape, suggesting a functional diversification among PSL genes.
A previously described  diploid clone of potato (named T710) coming from hybridization between Solanum tuberosum haploid USW3304 (2n = 2x = 24) and S. chacoense (2n = 2x = 24) has been used to isolate PSL genes.
Potato PSLcloning and sequence analysis
Plant genomic DNA was isolated from leaves using the DNeasy Plant Mini Kit (QIAGEN http://www1.qiagen.com). Bacterial plasmid DNA was isolated using QIAprep Spin Miniprep Kit (QIAGEN). Total RNA from prebolting buds was extracted using the RNeasy Plant Mini Kit (QIAGEN) and then treated with DNase I (Invitrogen, http://www.invitrogen.com) to remove residual genomic DNA. Primer pairs for cloning designed with PRIMER3 (http://frodo.wi.mit.edu/cgi-bin/primer3/primer3.cgi) are listed in Additional file 3: Primers used in this study.
PSL1 genomic fragment was amplified by PCR with primers PS_F1 and PS_R1 and full sequence with primers PS_F2 and PS_R2. The coding region of PSL transcripts was amplified by RT-PCR by using SuperScriptTM III Reverse Transcriptase (Invitrogen) with an oligo- dT12-18 (Invitrogen). The cDNA was subjected to PCR with PS_CF and PS_CR primers (Additional File 3). PCR products have been cloned into PCR2.1 with T/A Cloning kit (Invitrogen). Nucleotide sequencing was carried out by Eurofins MWG Operon sequencing service (Germany).
PSL1 gene structure and cDNA predictions were carried out using FGENESH online tool (http://linux1.softberry.com/berry.phtml?topic=fgenesh&group=programs&subgroup=gfind) selecting Tomato as organism. In silico translation of cDNA sequences was carried out using the Expasy Translation tool (http://www.expasy.ch/tools/dna.html).
Identification of unannotated PSLgenes
The PSL protein sequences were identified and collected by TBLASTN  search against the Phytozome v6 database (http://www.phytozome.net/), SGN (SOL Genomic Network, http://sgn.cornell.edu/) and Potato Genome Sequencing Consortium (PGSC, http://potatogenomics.plantbiology.msu.edu/index.php?p=blast).
Molecular Phylogenetic analysis by Maximum Likelihood method
The PSL protein sequences were firstly aligned by MUSCLE  using the default settings of MEGA5 . The best model for Maximum Likelihood phylogeny analysis was chosen testing all the available models in ProtTest version 2.4  with slow optimization strategy and selecting the one with highest AICc value. The evolutionary history was then inferred by using the Maximum Likelihood method according to Jones et al. w/freq. model . The bootstrap consensus tree was inferred from 100 replicates . Initial tree(s) for the heuristic search were obtained automatically as following. When the number of common sites is <100 or less than one fourth of the total number of sites, the maximum parsimony method was used, otherwise BIONJ method with MCL distance matrix was used. A discrete Gamma distribution was used to model evolutionary rate differences among sites (4 categories, +G, parameter = 1.3900). The rate variation model allowed for some sites to be evolutionarily invariable ([+I], 9.0566% sites). All ambiguous positions were removed for each sequence pair. Evolutionary analyses were conducted in MEGA5.
PSL domain analysis
The locations of FHA and PINc domains within PSL genes were detected using SMART . Secondary structure prediction was performed using domains from PSL sequences as input into the PSIPRED secondary structure prediction server . The program MUSCLE  was used to do multiple sequence alignments of FHA and PINc domains in PSL proteins, yRAD53p [NCBI:6325104] and hSMG6 [UniProt:Q86US8]. Conservation of phosphothreonine-binding residues in FHA and of RNAse activity residues in PINc were determined by alignment with yRAD53p and hSMG6, respectively.
Comparison of dN-dS values between PSLsequences
The coding sequences of PSLs were obtained from the databases reported in Additional File 1. The terminal codon was manually removed, then the codon alignment was performed by MUSCLE  using the default settings of MEGA5  (Tamura et al., personal communication). To select the best substitution model we used JmodelTest 0.1.1 [39, 40] with default settings. The GTR  model was selected as the best fitting as evidenced by AICc values.
The codon alignment was then uploaded on DataMonkey 2010 server [18, 42] and dN-dS evaluated using GTR as substitution model, and SLAC (default settings except for Global dN/dS value = estimated with CI), FEL and REL  alghoritms. Codons subjected to evolutive pressure were identified with Integrative Selection Analysis selecting significance levels for SLAC p < 0.1, FEL p < 0.1 and REL Bayes Factor < 50. Only codons with a significant dN-dS value according to all the three methods were reported.
#Contribution n 358 from CNR - National Research Council of Italy, Institute of Plant Genetics, Research Division Portici.
We wish to thank Ms. Rosa Paparo for helpful technical assistance, Prof. Domenico Carputo and Dr. Raphael Mercier for useful comments on the manuscript. This work was partially funded by Galileo Grant from University Italy-France.
- Tate JA, Soltis DE, Soltis PS: Polyploidy in Plants. The Evolution of the Genome. Edited by: Gregory T. 2005, Elsevier Inc, 371-414. full_text.View ArticleGoogle Scholar
- Leitch AR, Leitch IJ: Genomic plasticity and the diversity of polyploid plants. Science. 2008, 320: 481-483. 10.1126/science.1153585.View ArticlePubMedGoogle Scholar
- Bretagnolle F, Thompson J: Tansley Review No-78 - Gametes with the somatix chromosome-number - mechanisms of their formation and rolein the evolution of autopolyploid plants. New Phytol. 1995, 129 (1): 1-22. 10.1111/j.1469-8137.1995.tb03005.x.View ArticleGoogle Scholar
- Consiglio F, Carputo D, Frusciante L, Monti LM, Conicella C: Meiotic mutations and crop improvement. Plant Breeding reviews. Edited by: Janick J. 2007, Purdue University, John Wiley & Sons, Inc, 28: 163-203. full_text.View ArticleGoogle Scholar
- Mercier R, Vezon D, Bullier E, Motamayor J, Sellier A, Lefevre F, Pelletier G, Horlow C: SWITCH1 (SWI1): a novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis. Gene Dev. 2001, 15 (14): 1859-1871. 10.1101/gad.203201.View ArticlePubMedPubMed CentralGoogle Scholar
- Ravi M, Marimuthu MPA, Siddiqi I: Gamete formation without meiosis in Arabidopsis. Nature. 2008, 451: 1121-1124. 10.1038/nature06557.View ArticlePubMedGoogle Scholar
- d'Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Simon M, Jenczewski E, Mercier R: Mutations in AtPS1 (Arabidopsis thaliana parallel spindle 1) lead to the production of diploid pollen grains. PLoS Genet. 2008, 4: e1000274-View ArticlePubMedPubMed CentralGoogle Scholar
- Fukuda Y: Cytological studies on the development of pollen grains in different races of solanum. Bot Mag Tokyo. 1927, 41: 459-474.View ArticleGoogle Scholar
- Mok D, Peloquin J: The inheritance of three mechanisms of diplandroid (2n pollen) formation in diploid potatoes. Heredity. 1975, 35: 1-8. 10.1038/hdy.1975.100.View ArticleGoogle Scholar
- Peloquin SJ, Boiteux LS, Carputo D: Meiotic mutants in potato. Valuable variants. Genetics. 1999, 153: 1493-1499.PubMedPubMed CentralGoogle Scholar
- Li J, Lee GI, Van Doren SR, Walker JC: The FHA domain mediates phosphoprotein interactions. J Cell Sci. 2000, 113: 4143-4149.PubMedGoogle Scholar
- Durocher D, Jackson SP: The FHA domain. FEBS Lett. 2002, 513: 58-66. 10.1016/S0014-5793(01)03294-X.View ArticlePubMedGoogle Scholar
- Lareau LF, Brooks AN, Soergel DAW, Meng Q, Brenner SE: The coupling of alternative splicing and nonsense-mediated mRNA decay. Adv Exp Med Biol. 2007, 623: 190-211. full_text.View ArticlePubMedGoogle Scholar
- Nagy E, Maquat LE: A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem Sci. 1998, 23 (6): 198-199. 10.1016/S0968-0004(98)01208-0.View ArticlePubMedGoogle Scholar
- Durocher D, Taylor IA, Sarbassova D, Haire LF, Westcott SL, Jackson SP, Smerdon SJ, Yaffe MB: The molecular basis of FHA domain:phosphopeptide binding specificity and implications for phospho-dependent signaling mechanisms. Mol Cell. 2000, 6 (5): 1169-1182. 10.1016/S1097-2765(00)00114-3.View ArticlePubMedGoogle Scholar
- Arcus VL, Bäckbro K, Roos A, Daniel EL, Baker EN: Distant structural homology leads to the functional characterization of an archaeal PIN domain as an exonuclease. J Biol Chem. 2004, 279 (16): 16471-16478. 10.1074/jbc.M313833200.View ArticlePubMedGoogle Scholar
- Glavan F, Behm-Ansmant I, Izaurralde E, Conti E: Structures of the PIN domains of SMG6 and SMG5 reveal a nuclease within the mRNA surveillance complex. The EMBO Journal. 2006, 25 (21): 5117-5125. 10.1038/sj.emboj.7601377.View ArticlePubMedPubMed CentralGoogle Scholar
- Pond SLK, Frost SDW: Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics. 2005, 21 (10): 2531-2533. 10.1093/bioinformatics/bti320.View ArticlePubMedGoogle Scholar
- Bowers JE, Chapman BA, Rong J, Paterson AH: Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature. 2003, 422 (6930): 433-438. 10.1038/nature01521.View ArticlePubMedGoogle Scholar
- Paterson AH, Bowers JE, Chapman BA: Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci USA. 2004, 101 (26): 9903-9908. 10.1073/pnas.0307901101.View ArticlePubMedPubMed CentralGoogle Scholar
- Doyle JJ, Flagel LE, Paterson AH, Rapp RA, Soltis DE, Soltis PS, Wendel JF: Evolutionary genetics of genome merger and doubling in plants. Annu Rev Genet. 2008, 42: 443-461. 10.1146/annurev.genet.42.110807.091524.View ArticlePubMedGoogle Scholar
- Fawcett JA, Maere S, Van de Peer Y: Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proc Natl Acad Sci USA. 2009, 106 (14): 5737-5742. 10.1073/pnas.0900906106.View ArticlePubMedPubMed CentralGoogle Scholar
- Gill N, Findley S, Walling JG, Hans C, Ma J, Doyle J, Stacey G, Jackson SA: Molecular and chromosomal evidence for allopolyploidy in soybean. Plant Physiol. 2009, 151 (3): 1167-1174. 10.1104/pp.109.137935.View ArticlePubMedPubMed CentralGoogle Scholar
- Shoemaker RC, Schlueter J, Doyle JJ: Paleopolyploidy and gene duplication in soybean and other legumes. Curr Opin Plant Biol. 2006, 9 (2): 104-109. 10.1016/j.pbi.2006.01.007.View ArticlePubMedGoogle Scholar
- Chang Y-F, Imam JS, Wilkinson MF: The nonsense-mediated decay RNA surveillance pathway. Annu Rev Biochem. 2007, 76: 51-74. 10.1146/annurev.biochem.76.050106.093909.View ArticlePubMedGoogle Scholar
- Riehs N, Akimcheva S, Puizina J, Bulankova P, Idol RA, Siroky J, Schleiffer A, Schweizer D, Shippen DE, Riha K: Arabidopsis SMG7 protein is required for exit from meiosis. J Cell Sci. 2008, 121: 2208-2216. 10.1242/jcs.027862.View ArticlePubMedGoogle Scholar
- Ogburia M, Yabuya T, Adachi T: A cytogenetic study of bilateral sexual polyploidization in cassava (Manihot esculenta Crantz). Plant Breeding. 2002, 121: 278-280. 10.1046/j.1439-0523.2002.00694.x.View ArticleGoogle Scholar
- Conicella C, Barone A, Giudice A, Frusciante L, Monti LM: Cytological evidences of SDR-FDR mixture in the formation of 2n eggs in a potato diploid clone. Theor Appl Genet. 1991, 81 (1): 59-63. 10.1007/BF00226112.View ArticlePubMedGoogle Scholar
- Hartung F, Puchta H: Molecular characterisation of two paralogous SPO11 homologues in Arabidopsis thaliana. Nucleic Acids Res. 2000, 28 (7): 1548-1554. 10.1093/nar/28.7.1548.View ArticlePubMedPubMed CentralGoogle Scholar
- Barone C, Frusciante : Selection of potato diploid hybrids for 2n gamete production. Journal of Genetics and Breeding. 1993, 47: 313-318.Google Scholar
- Altschul SF, Lipman DJ: Protein database searches for multiple alignments. Proc Natl Acad Sci USA. 1990, 87 (14): 5509-5513. 10.1073/pnas.87.14.5509.View ArticlePubMedPubMed CentralGoogle Scholar
- Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. NAR. 2004, 32 (5): 1792-1797. 10.1093/nar/gkh340.View ArticlePubMedPubMed CentralGoogle Scholar
- Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 2007, 24: 1596-1599. 10.1093/molbev/msm092.View ArticlePubMedGoogle Scholar
- Abascal F, Zardoya R, Posada D: ProtTest: Selection of best-fit models of protein evolution. Bioinformatics. 2005, 21: 2104-2105. 10.1093/bioinformatics/bti263.View ArticlePubMedGoogle Scholar
- Jones DT, Taylor WR, Thornton JM: The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 1992, 8 (3): 275-282.PubMedGoogle Scholar
- Felsenstein : Confidence limits on phylogenies: An approach using the bootstrap. Evolution. 1985, 39: 783-791. 10.2307/2408678.View ArticleGoogle Scholar
- Schultz J, Milpetz F, Bork P, Ponting CP: SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA. 1998, 95 (11): 5857-5864. 10.1073/pnas.95.11.5857.View ArticlePubMedPubMed CentralGoogle Scholar
- McGuffin LJ, Bryson K, Jones DT: The PSIPRED protein structure prediction server. Bioinformatics. 2000, 16 (4): 404-405. 10.1093/bioinformatics/16.4.404.View ArticlePubMedGoogle Scholar
- Posada D: jModelTest: Phylogenetic Model Averaging. Mol Biol Evol.
- Guindon S, Gascuel O: A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol. 2003, 52: 696-704. 10.1080/10635150390235520.View ArticlePubMedGoogle Scholar
- Tavaré S: Some Probabilistic and Statistical Problems in the Analysis of DNA Sequences. Lectures on Mathematics in the Life Sciences. Edited by: AMS. 1986, 17: 57-86.Google Scholar
- Pond SLK, Muse SV: HyPhy: hypothesis testing using phylogenies. Bioinformatics. 2005, 21 (5): 676-679. 10.1093/bioinformatics/bti079.View ArticlePubMedGoogle Scholar
- Pond SLK, Frost SDW: Not So Different After All: A Comparison of Methods for Detecting Amino Acid Sites Under Selection. Mol Biol Evol. 2005, 22 (5): 1208-1222. 10.1093/molbev/msi105.View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.