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.
Similar content being viewed by others
References
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
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
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
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
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
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
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
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
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
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
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
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
Darling ACE, Mau B, Blattner FR, Perna NT (2004) Mauve: Multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772
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
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
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
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
Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52:696–704
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
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
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 30:3059
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 28:1647
Kelchner SA (2000) The evolution of non-coding chloroplast DNA and its application in plant systematics. Ann Missouri Bot Gard 87:482–498
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
Knoop V (2012) Seed plant mitochondrial genomes: complexity evolving. In: Bock R, Knoop V (eds) Genomics of chloroplasts and mitochondria. Springer, New York, pp 175–200
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
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 32:11–16
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 17:4089–4099
Lewis PO, Holder MT, Holsinger KE (2005) Polytomies and bayesian phylogenetic inference. Syst Biol 54:241–253. https://doi.org/10.1080/10635150590924208
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
Lira-Saade R (1995) Estudios taxonómicos y ecogeográficos de las Cucurbitaceae latinoamericanas de importancia económica. International Plant Genetic Resources Institute, Rome
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
Lynch M, Koskella B, Schaack S (2006) Mutation pressure and the evolution of organelle genomic architecture. Science 80-(311):1727–1731
Müller K (2005) SeqState—primer design and sequence statistics for phylogenetic DNA data sets. Appl Bioinform 4:65–69
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
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
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
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 36–39
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
Rice DW, Alverson AJ, Richardson AO et al (2013) Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm. Science 80-(342):1468–1473
Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
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
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
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
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
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
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
Scott I, Logan DC (2011) Mitochondrial dynamics. In: Kempken F (ed) Plant mitochondria. Springer, New York, pp 31–63
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 92:142–166
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
Shimodaira H (2002) An Approximately Unbiased test of phylogenetic tree selection. Syst Biol 51:492–508. https://doi.org/10.1080/10635150290069913
Shimodaira H, Hasegawa M (2001) CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17:1246–1247
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
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
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
Stern DB (1987) DNA transposition between plant organellar genomes. J Cell Sci. https://doi.org/10.1242/jcs.1987.Supplement_7.11
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
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:1105–1109
Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105:437–460
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
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
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
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
Yang Z (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591
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
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
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
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
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.
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.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors state they have no competing interests to declare.
Additional information
Handling Editor: Rafael Zardoya.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Aguirre-Dugua, X., Castellanos-Morales, G., Paredes-Torres, L.M. et al. Evolutionary Dynamics of Transferred Sequences Between Organellar Genomes in Cucurbita. J Mol Evol 87, 327–342 (2019). https://doi.org/10.1007/s00239-019-09916-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00239-019-09916-1