Skip to main content
Log in

Retroelements and DNA Methylation Could Contribute to Diversity of 5S rDNA in Agave L.

  • Original Article
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

Agave L. is a genus of economic importance, and many of the 166 species in the American plant genus Agave L. inhabit high-stress environments, which makes the genus promising for facing global climate change. However, sustainable use of economically important species without interfering with their ecology and evolution requires generating knowledge about the factors responsible for their genetic variation and diversity and, on this basis, their adaptation and speciation. Few genetic studies exploring the evolutionary relationships, speciation processes, genetic variability and diversity within species of Agave are currently available. Analyses of rDNA loci have been performed with the purpose of determining the genetic variability and diversity of the genus Agave, and these loci have been used as genetic markers of ploidy. However, the factors involved in the diversity of 5S rDNA regions in Agave have not yet been studied in depth. Our study explored the possible mechanisms of genetic (retroelements) and epigenetic (DNA methylation) diversity in 5S rDNA regions in Agave. We characterized the 5S rDNA gene tandem in species of the genus with different ploidy numbers and determined the levels of methylation in 13 haplotypes of 5S rDNA and in four non-transcribed spacers (NTS). Our results showed highly dynamic methylation with a high percentage in haplotypes and NTS of 5S rDNA regions in Agave. The characterization of the 5S rDNA tandem array in Agave revealed vestigial remains of the Cassandra terminal-repeat retrotransposon in miniature (TRIM). Our analysis supported previous results suggesting that in species of Agave L., regulation and diversity of 5S rDNA regions are controlled by coordinated genetic and epigenetic events, which will vary according to the species and the level of ploidy. The artificial pressure to which some agave crops are subjected may affect the mechanisms of evolution of gene 5S rDNA.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Adams KL, Cronn R, Percifield R, Wendel JF (2003) Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc Natl Acad Sci USA 100(8):4649–4654

    Article  CAS  Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16(1):37–48

    Article  Google Scholar 

  • Baneerjee S, Sharma AK (1987) Cytophotometric estimation of nuclear DNA in different species and varieties of Agave. Cytologia 52:85–90

    Google Scholar 

  • Bautista R, Villalobos DP, Diaz-Moreno S, Cantun FR, Canovas FM, Gonzalo Claros M (2008) Nueva estrategia para la construcción de una genoteca genómica de Pinus pinaster en cromosomas artificiales de bacterias. Sistemas y Recursos Forestales 3:238–249

    Google Scholar 

  • Bennetzen JL (2002) Mechanisms and rates of genome expansion and contraction in flowering plants. Genetic 115(1):29–36

    Google Scholar 

  • Bimboim HC, Doly J (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7(6):1513–1523

    Article  Google Scholar 

  • Castorena-Sánchez I, Escóbedo RM, Quiroz A (1991) New cytotaxonomical determinants recognized in six taxa of Agave in the sections Rigidae and Sisalanae. Can J Bot 69(6):1257–1264

    Article  Google Scholar 

  • Cavallini A, Natali L, Cionini G, Castorena-Sanchez I (1995) Cytophotometric and biochemical analyses of DNA in pentaploid and diploid Agave species. Genome 39(2):266–271

    Google Scholar 

  • Chacón J, Sousa A, Baeza CM, Renner SS (2012) Ribosomal DNA distribution and a genus-wide phylogeny reveal patterns of chromosomal evolution in Alstroemeria (Alstroemeriaceae). Am J Bot 99(9):1501–1512

    Article  Google Scholar 

  • Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Ann Rev Plant Biol 58:377–406

    Article  CAS  Google Scholar 

  • Chen ZJ (2010) Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci 15(2):57–71

    Article  CAS  Google Scholar 

  • Cioffi MB, Martins C, Bertollo LA (2010) Chromosome spreading of associated transposable elements and ribosomal DNA in the fish Erythrinus erythrinus. Implications for genome change and karyoevolution in fish. BMC Evol Biol 10(1):271

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cloix C, Tutois S, Mathieu O, Cuvillier C, Espagnol MC, Picard G, Tourmente S (2000) Analysis of 5S rDNA arrays in Arabidopsis thaliana: physical mapping and chromosome-specific polymorphisms. Genome Res 10(5):679–690

    Article  Google Scholar 

  • Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452(7184):215–219

    Article  CAS  Google Scholar 

  • De-la-Peña C, Nic-Can G, Ojeda G, Herrera-Herrera JL, López-Torres A, Wrobel K, Robert-Díaz ML (2012) KNOX1 is expressed and epigenetically regulated during in vitro conditions in Agave spp. BMC Plant Biol 12(1):203

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Echevarría-Machado I, Sánchez-Cach LA, Hernández-Zepeda C, Rivera-Madrid R, Moreno-Valenzuela OA (2005) A simple and efficient method for isolation of DNA in high mucilaginous plant tissues. Mol Biotechnol 31(2):129–135

    Article  Google Scholar 

  • Eickbush TH, Eickbush DG (2007) Review. Finely orchestrated movements: evolution of the ribosomal RNA genes. Genetics 175:477–485

    Article  CAS  Google Scholar 

  • Foerster AM, Hetzl J, Müllner C, Scheid OM (2010) Analysis of bisulfite sequencing data from plant DNA using CyMATE. Plant Epigenet: Methods Protoc 631:13–22

    Google Scholar 

  • Fu Y, Dominissini D, Rechavi G, He C (2014) Gene expression regulation mediated through reversible m6A RNA methylation. ‎Nat Rev Genet 15(5):293–306

    Google Scholar 

  • Garcia S, Kovařík A (2013) Dancing together and separate again: gymnosperms exhibit frequent changes of fundamental 5S and 35S rRNA gene (rDNA) organisation. Heredity 111(1):23–33

    Article  CAS  Google Scholar 

  • Garcia S, Panero JL, Siroky J, Kovarik A (2010) Repeated reunions and splits feature the highly dynamic evolution of 5S and 35S ribosomal RNA genes (rDNA) in the Asteraceae family. BMC Plant Biol 10(1):176

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Garcia S, Khaitová CL, Kovařík A (2012) Expression of 5S rRNA genes linked to 35S rDNA in plants, their epigenetic modification and regulatory element divergence. BMC Plant Biol 12(1):95

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gómez-Rodríguez VM, Rodríguez-Garay B, Palomino G, Martínez J, Barba-Gonzalez R (2013) Physical mapping of 5S and 18S ribosomal DNA in three species of Agave (Asparagales, Asparagaceae). Comp Cytogenet 7(3):191–203

    Google Scholar 

  • Good-Avila SV, Souza V, Gaut BS, Eguiarte LE (2006) Timing and rate of speciation in Agave (Agavaceae). Proc Natl Acad Sci USA 103(24):9124–9129

    Article  CAS  Google Scholar 

  • Granneman S, Baserga SJ (2005) Crosstalk in gene expression: coupling and co-regulation of rDNA transcription, pre-ribosome assembly and pre-rRNA processing. Curr Opin Cell Biol 17(3):281–286

    Article  CAS  Google Scholar 

  • Gruber AR, Neuböck R, Hofacker IL, Washietl S (2007) The RNAz web server: prediction of thermodynamically stable and evolutionarily conserved RNA structures. Nucleic Acids Res 35(2):W335–W338

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids 41(41):95–98

    Google Scholar 

  • Hawkins JS, Hu G, Rapp RA, Grafenberg JL, Wendel JF (2007) Phylogenetic determination of the pace of transposable element proliferation in plants: copia and LINE-like elements in Gossypium. Genome 51(1):11–18

    Google Scholar 

  • Henderson IR, Chan SR, Cao X, Johnson L, Jacobsen SE (2010) Accurate sodium bisulfite sequencing in plants. Epigenetics 5(1):47–49

    Article  Google Scholar 

  • Hertweck KL (2013) Assembly and comparative analysis of transposable elements from low coverage genomic sequence data in Asparagales 1. Genome 56(9):487–494

    Article  CAS  Google Scholar 

  • Hetzl J, Foerster AM, Raidl G, Mittelsten-Scheid O (2007) CyMATE: a new tool for methylation analysis of plant genomic DNA after bisulphite sequencing. Plant J 51(3):526–536

    Article  CAS  Google Scholar 

  • Hill P, Burford D, Martin DM, Flavell AJ (2005) Retrotransposon populations of Vicia species with varying genome size. Mol Genet Genom 273(5):371–381

    Article  CAS  Google Scholar 

  • Kalendar R, Tanskanen J, Chang W, Antonius K, Sela H, Peleg O, Schulman AH (2008) Cassandra retrotransposons carry independently transcribed 5S RNA. Proc Natl Acad Sci USA 105(15):5833–5838

    Article  CAS  Google Scholar 

  • Khaliq I, Awais-Khan M, Pearce S (2012) Ty1-Copia retrotransposons are heterogeneous, extremely high copy number and are major players in the genome organization and evolution of Agave tequilana. Genet Resour Crop Evol 59(4):575–587

    Article  CAS  Google Scholar 

  • Kinoshita T, Seki M (2014) Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiol 55(11):1859–1863

    Article  Google Scholar 

  • Kobayashi T (2006) Strategies to maintain the stability of the ribosomal RNA gene repeats. Genes Genet Syst 81(3):155–161

    Article  Google Scholar 

  • Kobayashi T (2011) Regulation of ribosomal RNA gene copy number and its role in modulating genome integrity and evolutionary adaptability in yeast. Cell Mol Life Sci 68(8):1395–1403

    Article  CAS  Google Scholar 

  • Kovarik A, Dadejova M, Lim YK, Chase MW, Clarkson JJ, Knapp S, Leitch AR (2008) Evolution of rDNA in Nicotiana allopolyploids: a potential link between rDNA homogenization and epigenetics. Ann Bot 101(6):815–823

    Article  CAS  Google Scholar 

  • Lawrence RJ, Earley K, Pontes O, Silva M, Chen ZJ, Neves N, Viegas W, Pikaard CS (2004) A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. Mol Cell 13(4):599–609

    Article  Google Scholar 

  • Layat E, Sáez-Vásquez J, Tourmente S (2012) Regulation of Pol I-transcribed 45S rDNA and Pol III-transcribed 5S rDNA in Arabidopsis. Plant Cell Physiol 53(2):267–276

    Article  CAS  Google Scholar 

  • Lemon B, Tjian R (2000) Orchestrated response: a symphony of transcription factors for gene control. Genes Dev 14(20):2551–2569

    Article  Google Scholar 

  • Martinez G, Castellano M, Tortosa M, Pallas V, Gomez G (2013) A pathogenic non-coding RNA induces changes in dynamic DNA methylation of ribosomal RNA genes in host plants. Nucleic Acids Res 42(3):1553–1562

    Google Scholar 

  • Mathieu O, Yukawa Y, Sugiura M, Picard G, Tourmente S (2002) 5S rRNA genes expression is not inhibited by DNA methylation in Arabidopsis. Plant J 29(3):313–323

    Article  Google Scholar 

  • Mathieu O, Probst AV, Paszkowski J (2005) Distinct regulation of histone H3 methylation at lysines 27 and 9 by CpG methylation in Arabidopsis. EMBO J 24(15):2783–2791

    Article  CAS  Google Scholar 

  • Mayer C, Schmitz KM, Li J, Grummt I, Santoro R (2006) Intergenic transcripts regulate the epigenetic state of rRNA genes. Mol Cell 22(3):351–361

    Article  CAS  Google Scholar 

  • McKain MR, Wickett N, Zhang Y, Ayyampalayam S, McCombie WR, Chase MW, Pires JC, de Pamphilis CW, Leebens-Mack J (2012) Phylogenomic analysis of transcriptome data elucidates co-occurrence of a paleopolyploid event and the origin of bimodal karyotypes in Agavoideae (Asparagaceae). Am J Bot 99(2):397–406

    Article  Google Scholar 

  • McStay B, Grummt I (2008) The epigenetics of rRNA genes: from molecular to chromosome biology. Annu Rev Cell Dev Biol 24:131–157

    Article  CAS  Google Scholar 

  • Mittelsten-Scheid O, Probst AV, Afsar K, Paszkowski J (2002) Two regulatory levels of transcriptional gene silencing in Arabidopsis. Proc Natl Acad Sci USA 99(21):13659–13662

    Google Scholar 

  • Moreno-Salazar SF, Esqueda MA, Martínez J, Palomino G (2007) Nuclear genome size and karyotipe of Agave angustifolia and A. rhodacantha from Sonora, México. Rev Fitotec Mex 30(1):13–23

    Google Scholar 

  • Morse AM, Peterson DG, Islam-Faridi MN, Smith KE, Magbanua Z, Garcia SA, Kubisiak TL, Amerson HV, Carlson JE, Nelson CD, Davis JM (2009) Evolution of genome size and complexity in Pinus. PLoS ONE 4(2):e4332

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nic-Can GI, López-Torres A, Barredo-Pool F, Wrobel K, Loyola-Vargas VM, Rojas-Herrera R, De-la-Peña C (2013) New insights into somatic embryogenesis: LEAFY COTYLEDON1, BABY BOOM1 and WUSCHEL-RELATED HOMEOBOX4 are epigenetically regulated in Coffea canephora. PLoS ONE 8(8):e72160

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Okonechnikov K, Golosova O, Fursov M (2012) The UGENE team. Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics 28:1166–1167

    Article  CAS  Google Scholar 

  • Orioli A, Pascali C, Pagano A, Teichmann M, Dieci G (2012) RNA polymerase III transcription control elements: themes and variations. Gene 493(2):185–194

    Article  CAS  Google Scholar 

  • Palomino G, Martínez J, Méndez I (2005) Citotipos en Agave angustifolia Haw. Determinados por citometría de flujo y análisis de sus cariotipos. Rev Int Contam Ambie 21(1):49–54

    Google Scholar 

  • Palomino G, Martínez J, Méndez I, Cepeda-Cornejo V, Barba-González R, Rodríguez-Garay B (2015) Nuclear genome size and cytotype analysis in Agave parviflora Torr. subsp. flexiflora Gentry (Asparagales, Asparagaceae). Caryologia 68(3):159–168

    Article  Google Scholar 

  • Paule MR, White RJ (2000) Transcription by RNA polymerases I and III. Nucleic Acids Res 28(6):1283–1298

    Article  Google Scholar 

  • Piegu B, Guyot R, Picault N, Roulin A, Saniyal A, Kim H, Collura K, Brar DS, Jackson S, Wing RA, Panaud O (2006) Doubling genome size without polyploidization: dynamics of retrotransposition-driven genomic expansions in Oryza australiensis, a wild relative of rice. Genome Res 16(10):1262–1269

    Article  CAS  Google Scholar 

  • Pikaard CS (2000) The epigenetics of nucleolar dominance. Trends Genet 16(11):495–500

    Article  Google Scholar 

  • Preuss S, Pikaard CS (2007) rRNA gene silence and nucleolar dominance: insights into a chromosome-scale epigenetic on/off switch. BBA-Gene Struct Expr 1769(5):383–392

    Google Scholar 

  • Probst AV, Fagard M, Proux F, Mourrain P, Boutet S, Earley K, Lawrence RJ, Pikaard CS, Murfett J, Furner I, Vaucheret H, Scheid OM (2004) Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell 16(4):1021–1034

    Article  CAS  Google Scholar 

  • Renny-Byfield S, Chester M, Kovařík A, Le Comber SC, Grandbastien MA, Deloger M, Nichols RA, Macas J, Novák P, Chase MW, Leitch AR (2011) Next generation sequencing reveals genome downsizing in allotetraploid Nicotiana tabacum, predominantly through the elimination of paternally derived repetitive DNAs. Mol Biol Evol 28(10):2843–2854

    Article  CAS  Google Scholar 

  • Reuter JS, Mathews DH (2010) RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinform 11(1):129

    Article  CAS  Google Scholar 

  • Robert ML, Lim KY, Hanson L, Sanchez-Teyer F, Bennett MD, Leitch AR, Leitch IJ (2008) Wild and agronomically important Agave species (Asparagaceae) show proportional increases in chromosome number, genome size, and genetic markers with increasing ploidy. Bot J Linn Soc 158(2):215–222

    Article  Google Scholar 

  • Sampath P, Yang TJ (2014) Comparative analysis of Cassandra TRIMs in three Brassicaceae genomes. Plant Genet Resour 12(S1):S146–S150

    Article  CAS  Google Scholar 

  • Sanmiguel P, Bennetzen JL (1998) Evidence that a recent increase in maize genome size was caused by the massive amplification of intergene retrotransposons. Ann Bot 82(1):37–44

    Google Scholar 

  • Secco D, Wang C, Shou H, Schultz MD, Chiarenza S, Nussaume L, Lister R (2015) Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. Elife 4:e09343

    Article  PubMed Central  Google Scholar 

  • Song Q, Chen ZJ (2015) Epigenetic and developmental regulation in plant polyploids. Curr Opin Plant Biol 24:101–109

    Article  CAS  Google Scholar 

  • Szymanski M, Barciszewska MZ, Erdmann VA, Barciszewski J (2002) 5S ribosomal RNA database. Nucleic Acids Res 30(1):176–178

    Article  Google Scholar 

  • Szymanski M, Miroslawa B, Volker EA, Barciszewski J (2003) 5S rRNA: structure and interactions. Biochem J 371(3):641–651

    Article  Google Scholar 

  • Tamayo-Ordoñez M, Rodríguez-Zapata LC, Sánchez-Teyer LF (2012) Construction and characterization of a partial binary bacterial artificial chromosome (BIBAC) of Agave tequilana var. azul (2X) and its application for gene identification. Afr J Biotechnol 11(93):15950–15958

    Google Scholar 

  • Tamayo-Ordóñez YJ, Narvaez-Zapata JA, Sánchez-Teyer LF (2015) Comparative characterization of ribosomal DNA regions in different Agave accessions with economical importance. Plant Mol Biol Rep 33(6):2014–2029

    Article  CAS  Google Scholar 

  • Tamayo-Ordóñez MC, Espinosa-Barrera LA, Tamayo-Ordóñez YJ, Ayil-Gutiérrez B, Sánchez-Teyer LF (2016a) Advances and perspectives in the generation of polyploid plant species. Euphytica 209(1):1–22

    Article  Google Scholar 

  • Tamayo-Ordóñez MC, Rodriguez-Zapata LC, Narváez-Zapata JA, Tamayo-Ordóñez YJ, Ayil-Gutiérrez BA, Barredo-Pool F, Sánchez-Teyer LF (2016b) Morphological features of different polyploids for adaptation and molecular characterization of CC-NBS-LRR and LEA gene families in Agave L. J Plant Physiol 195:80–94

    Article  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739

    Article  CAS  Google Scholar 

  • Terol J, Naranjo MA, Ollitrault P, Talon M (2008) Development of genomic resources for Citrus clementina: Characterization of three deep-coverage BAC libraries and analysis of 46 000 BAC-end sequences. BMC Genom 9:423

    Article  CAS  Google Scholar 

  • Tynkevich YO, Volkov RA (2014) Structural organization of 5S ribosomal DNA in Rosa rugosa. Cytol Genet 48(1):1–6

    Article  Google Scholar 

  • Vaillant I, Tutois S, Cuvillier C, Schubert I, Tourmente S (2007) Regulation of Arabidopsis thaliana 5S rRNA genes. Plant Cell Physiol 48(5):745–752

    Article  CAS  Google Scholar 

  • Vaillant I, Tutois S, Jasencakova Z, Douet J, Schubert I, Tourmente S (2008) Hypomethylation and hypermethylation of the tandem repetitive 5S rRNA genes in Arabidopsis. Plant J 54(2):299–309

    Article  CAS  Google Scholar 

  • Vanyushin BF (2006) DNA methylation: basic mechanisms. In: Doerfler W, Böhm P (eds) Current topics in microbiology and immunology. Springer, Berlin, pp 67–122

    Google Scholar 

  • Wang W, Ma L, Becher H, Garcia S, Kovarikova A, Leitch IJ, Leitch AR, Kovarik A (2016) Astonishing 35S rDNA diversity in the gymnosperm species Cycas revoluta Thunb. Chromosoma 125(4):683–699

    Article  CAS  Google Scholar 

  • Wicke S, Costa A, Muñoz J, Quandt D (2011) Restless 5S: the re-arrangement (s) and evolution of the nuclear ribosomal DNA in land plants. Mol Phylogenet Evol 61(2):321–332

    Article  CAS  Google Scholar 

  • Xue S, Barna M (2012) Specialized ribosomes: a new frontier in gene regulation and organismal biology. Nat Rev Mol Cell Biol 13(6):355–369

    Article  CAS  Google Scholar 

  • Yang J, Sharma S, Kötter P, Entian KD (2015) Identification of a new ribose methylation in the 18S rRNA of S. cerevisiae. Nucleic Acids Res 43(4):2342–2352

    Google Scholar 

  • Zuccolo A, Sebastian A, Talag J, Yu Y, Kim H, Collura K, Kudrna D, Wing RA (2007) Transposable element distribution, abundance and role in genome size variation in the genus Oryza. BMC Evol Biol 7(1):152

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

The authors wish to express their gratitude to M.C. Miriam Monforte González for her contribution and orientation to the sequencing services for clones from the BIBAC genomic library of A. tequilana. Thanks are also given to Dr. Benjamin Abraham Ayil Gutierrez for his contribution in the figures and to M.C. Erika A. De la Cruz-Arguijo for her technical assistance in the sequencing of the clones using the ABI PRISM model 377 sequencer.

Funding

This work was supported by projects 50268 and 180757 of the Center of Scientific Research of Yucatán and the Genomic Biotechnology Center of the National Polytechnic Institute.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to L. F. Sánchez-Teyer.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Additional file 1 (DOC 459 KB)

Supplementary material 2 (DOCX 35 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tamayo-Ordóñez, Y.J., Narváez-Zapata, J.A., Tamayo-Ordóñez, M.C. et al. Retroelements and DNA Methylation Could Contribute to Diversity of 5S rDNA in Agave L.. J Mol Evol 86, 404–423 (2018). https://doi.org/10.1007/s00239-018-9856-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-018-9856-6

Keywords

Navigation