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Evolutionary Dynamics of Transferred Sequences Between Organellar Genomes in Cucurbita

  • Xitlali Aguirre-DuguaEmail author
  • Gabriela Castellanos-Morales
  • Leslie M. Paredes-Torres
  • Helena S. Hernández-Rosales
  • Josué Barrera-Redondo
  • Guillermo Sánchez-de la Vega
  • Fernando Tapia-Aguirre
  • Karen Y. Ruiz-Mondragón
  • Enrique Scheinvar
  • Paulina Hernández
  • Erika Aguirre-Planter
  • Salvador Montes-Hernández
  • Rafael Lira-SaadeEmail author
  • Luis E. EguiarteEmail author
Original Article

Abstract

Twenty-nine DNA regions of plastid origin have been previously identified in the mitochondrial genome of Cucurbita pepo (pumpkin; Cucurbitaceae). Four of these regions harbor homolog sequences of rbcL, matK, rpl20–rps12 and trnL–trnF, which are widely used as molecular markers for phylogenetic and phylogeographic studies. We extracted the mitochondrial copies of these regions based on the mitochondrial genome of C. pepo and, along with published sequences for these plastome markers from 13 Cucurbita taxa, we performed phylogenetic molecular analyses to identify inter-organellar transfer events in the Cucurbita phylogeny and changes in their nucleotide substitution rates. Phylogenetic reconstruction and tree selection tests suggest that rpl20 and rbcL mitochondrial paralogs arose before Cucurbita diversification whereas the mitochondrial matK and trnL–trnF paralogs emerged most probably later, in the mesophytic Cucurbita clade. Nucleotide substitution rates increased one order of magnitude in all the mitochondrial paralogs compared to their original plastid sequences. Additionally, mitochondrial trnL–trnF sequences obtained by PCR from nine Cucurbita taxa revealed higher nucleotide diversity in the mitochondrial than in the plastid copies, likely related to the higher nucleotide substitution rates in the mitochondrial region and loss of functional constraints in its tRNA genes.

Keywords

Gene duplication Inter-organellar DNA transfer Molecular evolution Paralogy Nucleotide substitution rate tRNA 

Notes

Acknowledgements

This manuscript includes in part the results of the Bachelor’s degree thesis of FTA, LMPT, PH, and KYRM, and postdoctoral work of XAD at Facultad de Estudios Superiores Iztacala, Universidad Nacional Autónoma de México. We are grateful to D. Piñero and V. Souza for supporting the project, and Laura Espinosa-Asuar for her help in laboratory work. Funds were provided by Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (Conabio) Project KE004 “Diversidad genética de las especies de Cucurbita en México e hibridación entre plantas genéticamente modificadas y especies silvestres de Cucurbita” and Project Conabio PE001 “Diversidad genética de las especies de Cucurbita en México. Fase II. Genómica evolutiva y de poblaciones, recursos genéticos y domesticación”, as well as Consejo Nacional de Ciencia y Tecnología (CONACyT) Problemas Nacionales grant number 247730 to Daniel Piñero (Instituto de Ecología, UNAM). XAD had a fellowship from Programa de Becas Posdoctorales de la Dirección General de Asuntos del Personal Académico (DGAPA), Universidad Nacional Autónoma de México.

Compliance with Ethical Standards

Conflict of interest

The authors state they have no competing interests to declare.

Supplementary material

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Electronic supplementary material 1 (DOCX 3448 kb)

References

  1. Adams KL, Qiu Y-L, Stoutemyer M, Palmer JD (2002) Punctuated evolution of mitochondrial gene content: High and variable rates of mitochondrial gene loss and transfer to the nucleus during angiosperm evolution. Proc Natl Acad Sci USA 99:9905–9912.  https://doi.org/10.1073/pnas.042694899 CrossRefPubMedGoogle Scholar
  2. Alverson AJ, Wei X, Rice DW et al (2010) Insights into the evolution of mitochondrial genome size from complete sequences of Citrullus lanatus and Cucurbita pepo (Cucurbitaceae). Mol Biol Evol 27:1436–1448.  https://doi.org/10.1093/molbev/msq029 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Alverson AJ, Rice DW, Dickinson S et al (2011) Origins and recombination of the bacterial-sized multichromosomal mitochondrial genome of cucumber. Plant Cell 23:2499–2513.  https://doi.org/10.1105/tpc.111.087189 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ara N, Nakkanong K, Lv W et al (2013) Antioxidant enzymatic activities and gene expression associated with heat tolerance in the stems and roots of two cucurbit species (“Cucurbita maxima” and “Cucurbita moschata”) and their interspecific inbred line “Maxchata”. Int J Mol Sci 14:24008–24028.  https://doi.org/10.3390/ijms141224008 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bailey CD, Carr TG, Harris SA, Hughes CE (2003) Characterization of angiosperm nrDNA polymorphism, paralogy, and pseudogenes. Mol Phylogenet Evol 29:435–455.  https://doi.org/10.1016/j.ympev.2003.08.021 CrossRefPubMedGoogle Scholar
  6. Barrera-Redondo J, Ibarra-Laclette E, Vázquez-Lobo A et al (2019) The genome of Cucurbita argyrosperma (silver-seed gourd) reveals faster rates of protein-coding gene and long noncoding RNA turnover and neofunctionalization within Cucurbita. Mol Plant 12:506–520.  https://doi.org/10.1016/j.molp.2018.12.023 CrossRefPubMedGoogle Scholar
  7. Bartoszewski G, Malepszy S, Havey MJ (2004) Mosaic (MSC) cucumbers regenerated from independent cell cultures possess different mitochondrial rearrangements. Curr Genet 45:45–53.  https://doi.org/10.1007/s00294-003-0456-6 CrossRefPubMedGoogle Scholar
  8. Borsch T, Quandt D (2009) Mutational dynamics and phylogenetic utility of noncoding chloroplast DNA. Plant Syst Evol 282:169–199.  https://doi.org/10.1007/s00606-009-0210-8 CrossRefGoogle Scholar
  9. Castellanos-Morales G, Paredes-Torres LM, Gámez N et al (2018) Historical biogeography and phylogeny of Cucurbita: Insights from ancestral area reconstruction and niche evolution. Mol Phylogenet Evol 128:38–54.  https://doi.org/10.1016/j.ympev.2018.07.016 CrossRefPubMedGoogle Scholar
  10. Chaw S-M, Wu C-S, Sudianto E (2018) Evolution of gymnosperm plastid genomes. Adv Bot Res 85:195–222.  https://doi.org/10.1016/bs.abr.2017.11.018 CrossRefGoogle Scholar
  11. Christensen AC (2013) Plant mitochondrial genome evolution can be explained by DNA repair mechanisms. Genome Biol Evol 5:1079–1086.  https://doi.org/10.1093/gbe/evt069 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cummings MP, Nugent JM, Olmstead RG, Palmer JD (2003) Phylogenetic analysis reveals five independent transfers of the chloroplast gene rbcL to the mitochondrial genome in angiosperms. Curr Genet 43:131–138.  https://doi.org/10.1007/s00294-003-0378-3 CrossRefPubMedGoogle Scholar
  13. Darling ACE, Mau B, Blattner FR, Perna NT (2004) Mauve: Multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403CrossRefGoogle Scholar
  14. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefGoogle Scholar
  15. Dietrich A, Small I, Cosset A et al (1996) Editing and import: Strategies for providing plant mitochondria with a complete set of functional transfer RNAs. Biochimie 78:518–529.  https://doi.org/10.1016/0300-9084(96)84758-4 CrossRefPubMedGoogle Scholar
  16. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:699–710.  https://doi.org/10.1371/journal.pbio.0040088 CrossRefGoogle Scholar
  17. Goremykin VV, Salamini F, Velasco R, Viola R (2009) Mitochondrial DNA of Vitis vinifera and the issue of rampant horizontal gene transfer. Mol Biol Evol 26:99–110.  https://doi.org/10.1093/molbev/msn226 CrossRefPubMedGoogle Scholar
  18. Goremykin VV, Lockhart PJ, Viola R, Velasco R (2012) The mitochondrial genome of Malus domestica and the import-driven hypothesis of mitochondrial genome expansion in seed plants. Plant J 71:615–626.  https://doi.org/10.1111/j.1365-313X.2012.05014.x CrossRefPubMedGoogle Scholar
  19. Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52:696–704CrossRefGoogle Scholar
  20. Havey MJ (1997) Predominant paternal transmission of the mitochondrial genome in cucumber. J Hered 88:232–235.  https://doi.org/10.1055/s-0031-1299652 CrossRefGoogle Scholar
  21. Kates HR, Soltis PS, Soltis DE (2017) Evolutionary and domestication history of Cucurbita (pumpkin and squash) species inferred from 44 nuclear loci. Mol Phylogenet Evol 111:98–109.  https://doi.org/10.1016/j.ympev.2017.03.002 CrossRefPubMedGoogle Scholar
  22. Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059PubMedPubMedCentralGoogle Scholar
  23. Kearse M, Moir R, Wilson A et al (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647CrossRefGoogle Scholar
  24. Kelchner SA (2000) The evolution of non-coding chloroplast DNA and its application in plant systematics. Ann Missouri Bot Gard 87:482–498CrossRefGoogle Scholar
  25. Kistler L, Newsom LA, Ryan TM et al (2015) Gourds and squashes (Cucurbita spp.) adapted to megafaunal extinction and ecological anachronism through domestication. Proc Natl Acad Sci USA 112:15107–15112.  https://doi.org/10.1073/pnas.1516109112 CrossRefPubMedGoogle Scholar
  26. Knoop V (2012) Seed plant mitochondrial genomes: complexity evolving. In: Bock R, Knoop V (eds) Genomics of chloroplasts and mitochondria. Springer, New York, pp 175–200CrossRefGoogle Scholar
  27. Kocyan A, Zhang LB, Schaefer H, Renner SS (2007) A multi-locus chloroplast phylogeny for the Cucurbitaceae and its implications for character evolution and classification. Mol Phylogenet Evol 44:553–577.  https://doi.org/10.1016/j.ympev.2006.12.022 CrossRefPubMedGoogle Scholar
  28. Laslett D, Canback B (2004) ARAGORN, a program for the detection of transfer RNA and transfer-messenger RNA genes in nucleotide sequences. Nucleic Acids Res 32:11–16CrossRefGoogle Scholar
  29. Leon P, Walbot V, Bedinger P (1989) Molecular analysis of the linear 2.3 kb plasmid of maize mitochondria: apparent capture of tRNA genes. Nucleic Acids Res 17:4089–4099CrossRefGoogle Scholar
  30. Lewis PO, Holder MT, Holsinger KE (2005) Polytomies and bayesian phylogenetic inference. Syst Biol 54:241–253.  https://doi.org/10.1080/10635150590924208 CrossRefPubMedGoogle Scholar
  31. Librado P, Rozas J (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452.  https://doi.org/10.1093/bioinformatics/btp187 CrossRefPubMedGoogle Scholar
  32. Lira-Saade R (1995) Estudios taxonómicos y ecogeográficos de las Cucurbitaceae latinoamericanas de importancia económica. International Plant Genetic Resources Institute, RomeGoogle Scholar
  33. Lowe TM, Chan PP (2016) tRNAscan-SE On-line: integrating search and context analysis of transfer RNA Genes. Nucleic Acids Res 44:W54–57.  https://doi.org/10.1093/nar/gkw413 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Lynch M, Koskella B, Schaack S (2006) Mutation pressure and the evolution of organelle genomic architecture. Science 80-(311):1727–1731CrossRefGoogle Scholar
  35. Müller K (2005) SeqState—primer design and sequence statistics for phylogenetic DNA data sets. Appl Bioinform 4:65–69CrossRefGoogle Scholar
  36. Müller K (2006) Incorporating information from length-mutational events into phylogenetic analysis. Mol Phylogenet Evol 38:667–676.  https://doi.org/10.1016/j.ympev.2005.07.011 CrossRefPubMedGoogle Scholar
  37. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkCrossRefGoogle Scholar
  38. Notsu Y, Masood S, Nishikawa T et al (2002) The complete sequence of the rice (Oryza sativa L.) mitochondrial genome: Frequent DNA sequence acquisition and loss during the evolution of flowering plants. Mol Genet Genomics 268:434–445.  https://doi.org/10.1007/s00438-002-0767-1 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Palmer JD (1992) Mitochondrial DNA in plant systematics: applications and limitations. In: Soltis PS, Soltis DE, Doyle JJ (eds) Molecular systematics of plants. Chapman and Hall, London, pp 36–39CrossRefGoogle Scholar
  40. Pirie MD, Vargas MPB, Botermans M et al (2007) Ancient paralogy in the cpDNA trnL-F region in Annonaceae: Implications for plant molecular systematics. Am J Bot 94:1003–1016.  https://doi.org/10.3732/ajb.94.6.1003 CrossRefPubMedGoogle Scholar
  41. Rice DW, Alverson AJ, Richardson AO et al (2013) Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm. Science 80-(342):1468–1473CrossRefGoogle Scholar
  42. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefGoogle Scholar
  43. Rouphael Y, Cardarelli M, Rea E, Colla G (2012) Improving melon and cucumber photosynthetic activity, mineral composition, and growth performance under salinity stress by grafting onto Cucurbita hybrid rootstocks. Photosynthetica 50:180–188.  https://doi.org/10.1007/s11099-012-0002-1 CrossRefGoogle Scholar
  44. Sanchez-Puerta MV, Zubko M, Palmer JD (2015) Homologous recombination and retention of a single form of most genes shape the highly chimeric mitochondrial genome of a cybrid plant. Genome Res 206:381–396.  https://doi.org/10.1111/nph.13188 CrossRefGoogle Scholar
  45. Sanchez-Puerta MV, Edera A, Gandini CL et al (2019) Genome-scale transfer of mitochondrial DNA from legume hosts to the holoparasite Lophophytum mirabile (Balanophoraceae). Mol Phylogenet Evol 132:243–250.  https://doi.org/10.1016/j.ympev.2018.12.006 CrossRefPubMedGoogle Scholar
  46. Sanderson MJ, Copetti D, Búrquez A et al (2015) Exceptional reduction of the plastid genome of saguaro cactus (Carnegiea gigantea): loss of the ndh gene suite and inverted repeat 1. Am J Bot 102:1115–1127.  https://doi.org/10.3732/ajb.1500184 CrossRefPubMedGoogle Scholar
  47. Sanjur OI, Piperno DR, Andres TC, Wessel-Beaver L (2002) Phylogenetic relationships among domesticated and wild species of Cucurbita (Cucurbitaceae) inferred from a mitochondrial gene: Implications for crop plant evolution and areas of origin. Proc Natl Acad Sci USA 99:535–540.  https://doi.org/10.1073/pnas.012577299 CrossRefPubMedGoogle Scholar
  48. Schaefer H, Heibl C, Renner SS (2009) Gourds afloat: a dated phylogeny reveals an Asian origin of the gourd family (Cucurbitaceae) and numerous oversea dispersal events. Proc R Soc B 276:843–851.  https://doi.org/10.1098/rspb.2008.1447 CrossRefPubMedGoogle Scholar
  49. Scott I, Logan DC (2011) Mitochondrial dynamics. In: Kempken F (ed) Plant mitochondria. Springer, New York, pp 31–63CrossRefGoogle Scholar
  50. Shaw J, Lickey EB, Beck JT et al (2005) The tortoise and the hare II; relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot 92:142–166CrossRefGoogle Scholar
  51. Shen J, Kere MG, Chen JF (2013) Mitochondrial genome is paternally inherited in Cucumis allotetraploid (C.×hytivus) derived by interspecific hybridization. Sci Hortic (Amsterdam) 155:39–42.  https://doi.org/10.1016/j.scienta.2013.03.009 CrossRefGoogle Scholar
  52. Shimodaira H (2002) An Approximately Unbiased test of phylogenetic tree selection. Syst Biol 51:492–508.  https://doi.org/10.1080/10635150290069913 CrossRefPubMedGoogle Scholar
  53. Shimodaira H, Hasegawa M (2001) CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17:1246–1247CrossRefGoogle Scholar
  54. Sloan DB, Alverson AJ, Chuckalovcak JP et al (2012a) Rapid evolution of enormous, multichromosomal genomes in flowering plant mitochondria with exceptionally high mutation rates. PLoS Biol 10:e1001241.  https://doi.org/10.1371/journal.pbio.1001241 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Sloan DB, Müller K, McCauley DE et al (2012b) Intraspecific variation in mitochondrial genome sequence, structure, and gene content in Silene vulgaris, an angiosperm with pervasive cytoplasmic male sterility. New Phytol 196:1228–1239.  https://doi.org/10.1111/j.1469-8137.2012.04340.x CrossRefPubMedGoogle Scholar
  56. Smith DR, Keeling PJ (2015) Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes. Proc Natl Acad Sci USA 112:10177–10184.  https://doi.org/10.1073/pnas.1422049112 CrossRefPubMedGoogle Scholar
  57. Stern DB (1987) DNA transposition between plant organellar genomes. J Cell Sci.  https://doi.org/10.1242/jcs.1987.Supplement_7.11 CrossRefGoogle Scholar
  58. Suchard M, Lemey P, Baele G et al (2018) Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol 4:vey016.  https://doi.org/10.1093/ve/vey016 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109CrossRefGoogle Scholar
  60. Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460PubMedPubMedCentralGoogle Scholar
  61. Untergasser A, Cutcutache I, Koressaar T et al (2012) Primer3-New capabilities and interfaces. Nucleic Acids Res 40:e115.  https://doi.org/10.1093/nar/gks596 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Wicke S, Schneeweiss GM, dePamphilis CW et al (2011) The evolution of the plastid chromosome in land plants: Gene content, gene order, gene function. Plant Mol Biol 76:273–297.  https://doi.org/10.1007/s11103-011-9762-4 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Wolfe AD, Randle CP (2004) Recombination, heteroplasmy, haplotype polymorphism, and paralogy in plastid genes: implications for plant molecular systematics. Syst Bot 29:1011–1020.  https://doi.org/10.1600/0363644042451008 CrossRefGoogle Scholar
  64. Wolfe KH, Li W-H, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84:9054–9058.  https://doi.org/10.1073/pnas.84.24.9054 CrossRefPubMedGoogle Scholar
  65. Yang Z (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591CrossRefGoogle Scholar
  66. Zhang LB, Simmons MP, Kocyan A, Renner SS (2006) Phylogeny of the Cucurbitales based on DNA sequences of nine loci from three genomes: implications for morphological and sexual system evolution. Mol Phylogenet Evol 39:305–322.  https://doi.org/10.1016/j.ympev.2005.10.002 CrossRefPubMedGoogle Scholar
  67. Zhang C, Zhu Q, Liu S et al (2018) The complete chloroplast genome sequence of the Cucurbita pepo L. (Cucurbitaceae). Mitochondrial DNA Part B 3:717–718.  https://doi.org/10.1080/23802359.2018.1483766 CrossRefGoogle Scholar
  68. Zheng YH, Alverson AJ, Wang QF, Palmer JD (2013) Chloroplast phylogeny of Cucurbita: Evolution of the domesticated and wild species. J Syst Evol 51:326–334.  https://doi.org/10.1111/jse.12006 CrossRefGoogle Scholar
  69. Zhu A, Guo W, Gupta S et al (2016) Evolutionary dynamics of the plastid inverted repeat: The effects of expansion, contraction, and loss on substitution rates. New Phytol 209:1747–1756.  https://doi.org/10.1111/nph.13743 CrossRefPubMedGoogle Scholar
  70. Zhu,Q., Gao,P., Liu,S., Wang, X., Qu,S. and Luan,F. (2017). The complete chloroplast genome sequence of the Cucurbita moschata Duch. Direct Submission (18-Dec-2017) National Center for Biotechnology Information. Reference Sequences NC_036506 and NC_036505.Google Scholar

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Authors and Affiliations

  1. 1.Unidad de Biotecnología Y Prototipos, Facultad de Estudios Superiores IztacalaUniversidad Nacional Autónoma de MéxicoTlalnepantlaMexico
  2. 2.Departamento de Conservación de La BiodiversidadEl Colegio de La Frontera Sur, Unidad VillahermosaVillahermosaMexico
  3. 3.Departamento de Ecología Evolutiva, Instituto de EcologíaUniversidad Nacional Autónoma de MéxicoCiudad de MéxicoMexico
  4. 4.Campo Experimental Bajío, Instituto Nacional de Investigaciones Forestales, Agrícolas Y Pecuarias (INIFAP)CelayaMexico

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