Structural, evolutionary and phylogenomic features of the plastid genome of Carya illinoinensis cv. Imperial

Authors

  • Jordana Caroline Nagel Federal University of the Pampa, Graduate Program in Biological Sciences, Campus São Gabriel, São Gabriel, RS, Brazil, Universidade Regional Integrada do Alto Uruguai e das Missões, Campus Santo Ângelo, Santo Ângelo, RS, Brazil
  • Lilian de Oliveira Machado Federal University of Santa Catarina, Graduate Program in Plant Genetic Resources, Florianópolis, SC, Brazil
  • Rafael Plá Matielo Lemos Federal University of the Pampa, Graduate Program in Biological Sciences, Campus São Gabriel, São Gabriel, RS, Brazil
  • Cristiane Barbosa D’Oliveira Matielo Federal University of the Pampa, Graduate Program in Biological Sciences, Campus São Gabriel, São Gabriel, RS, Brazil
  • Tales Poletto Federal University of Santa Maria, Graduate Program in Forest Engineering; Santa Maria, RS, Brazil
  • Igor Poletto Federal University of the Pampa, Graduate Program in Biological Sciences, Campus São Gabriel, São Gabriel, RS, Brazil
  • Valdir Marcos Stefenon Federal University of Santa Catarina, Graduate Program in Plant Genetic Resources, Florianópolis, SC, Brazil & Federal University of the Pampa, Graduate Program in Biological Sciences, Campus São Gabriel, São Gabriel, RS, Brazil

DOI:

https://doi.org/10.15287/afr.2019.1413

Keywords:

Pecan, chloroplast genome, phylogenomics, Juglandaceae

Abstract

The economically most important nut tree species in the world belong to family Juglandaceae, tribe Jungladeae. Evolutive investigations concerning species from this tribe are important for understanding the molecular basis driving the evolution and systematics of these species. In this study, we release the complete plastid genome of C. illinoinensis cv. Imperial. Using an IonTorrent NGS platform we generated 8.5´108 bp of raw sequences, enabling the assemblage of the complete plastid genome of this species. The plastid genome is 160,818 bp long, having a quadripartite structure with an LSC of 90,041 bp, an SSC of 18,791 bp and two IRs of 25,993 bp. A total of 78 protein-coding, 37 tRNA-coding, and 8 rRNA-coding regions were predicted. Bias in synonymous codon usage was detected in cultivar Imperial and three tRNA-coding regions were identified as hotspots of nucleotide divergence, with high estimations of dN/dS ratio. The high fraction of SSR loci prospected in non-coding regions may provide informative genetic markers, useful to a wide range of genetic researches. Despite the significant structural differences among plastid genomes, the phylogenetic relationships among species is supported by the whole plastid genome analysis,supporting the monophyly of subtribes Caryinae and Juglandinae within family Juglandaceae.

References

Amiryousefi A., Hyvönen J., Poczai P., 2018. IRscope: an online program to visualize the junction sites of chloroplast genomes. Bioinformatics 34:3030-3031. https://doi.org/10.1093/bioinformatics/bty220" target="_blank">DOI: 10.1093/bioinformatics/bty220 Beier S., Thiel T., Münch T., Scholz U., Mascher M., 2017. MISA-web: a web server for SSR prediction. Bioinformatics 33:2583-2585. https://doi.org/10.1093/bioinformatics/btx198" target="_blank">DOI: 10.1093/bioinformatics/btx198 Bock R., 2017. Witnessing genome evolution: experimental reconstruction of endosymbiotic and horizontal gene transfer. Annu Rev Genet. 51:1-22. https://doi.org/10.1146/annurev-genet-120215-035329" target="_blank">DOI: 10.1146/annurev-genet-120215-035329 Chan P.P., Lowe T.M., 2019. tRNAscan-SE: Searching for tRNA Genes in Genomic Sequences. Methods Mol Biol. 1962:1-14. https://doi.org/10.1007/978-1-4939-9173-0_1" target="_blank">DOI: 10.1007/978-1-4939-9173-0_1 Curtu A.L., Gailing O., Finkeldey R., 2007.Evidence for hybridization and introgression within a species-rich oak (Quercus spp.) community. BMC Evolutionary Biology 7:218. https://doi.org/10.1186/1471-2148-7-218" target="_blank">DOI: 10.1186/1471-2148-7-218 Darling, A.C.E., 2004. Mauve: Multiple Alignment of Conserved Genomic Sequence with Rearrangements. Genome Res 14:1394-1403. https://doi.org/10.1101/gr.2289704" target="_blank">DOI: 10.1101/gr.2289704 Dong W., Xu C., Li W., Xie X., Lu Y., Liu Y., Jin X., Suo Z., 2017. Phylogenetic Resolution in Juglans Based on Complete Chloroplast Genomes and Nuclear DNA Sequences. Front. Plant Sci. 8:1148. https://doi.org/10.3389/fpls.2017.01148" target="_blank">DOI: 10.3389/fpls.2017.01148 Doyle J.J., Doyle J.L., 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull Bot Soc Am. 19:11-15. Dugas D.V., Hernandez D., Koenen, et al., 2015.Mimosoid legume plastid genome evolution: IR expansion, tandem repeat expansions, and accelerated rate of evolution in clpP. Sci. Rep. 5:1-13. https://doi.org/10.1038/srep16958" target="_blank">DOI: 10.1038/srep16958 Edgar R.C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797. https://doi.org/10.1093/nar/gkh340" target="_blank">DOI: 10.1093/nar/gkh340 Hu Y., Chen X., Feng X., Woeste K.E., Zhao P., 2016. Characterization of the complete chloroplast genome of the endangered species Carya sinensis (Juglandaceae). Conservation Genet Resour 8:467-470. https://doi.org/10.1007/s12686-016-0601-4" target="_blank">DOI: 10.1007/s12686-016-0601-4 Hu Y., Woeste K.E., Zhao P., 2017.Completion of the Chloroplast Genomes of Five Chinese Juglans and Their Contribution to Chloroplast Phylogeny. Front. Plant Sci. 7:1955. https://doi.org/10.3389/fpls.2016.01955" target="_blank">DOI: 10.3389/fpls.2016.01955 Huang Y., Xiao L., Zhang Z. et al., 2019. The genomes of pecan and Chinese hickory provide insights into Carya evolution and nut nutrition. GigaScience, 8: 1-17. https://doi.org/10.1093/gigascience/giz036" target="_blank">DOI: 10.1093/gigascience/giz036 Katoh K., Rozewicki J., Yamada K.D., 2017. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics bbx108. https://doi.org/10.1093/bib/bbx108" target="_blank">DOI: 10.1093/bib/bbx108 Laslett D., Canback B., 2004. ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 32:11-16. https://doi.org/10.1093/nar/gkh152" target="_blank">DOI: 10.1093/nar/gkh152 Lemos R.P.M., Matielo C.B.D'O., Beise D.C., Rosa V.G., Sarzi D.S., Roesch L.F.W., Stefenon V.M., 2018. Characterization of Plastidial and Nuclear SSR Markers for Understanding Invasion Histories and Genetic Diversity of Schinus molle L. Biology 7:43. https://doi.org/10.3390/biology7030043" target="_blank">DOI: 10.3390/biology7030043 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" target="_blank">DOI: 10.1093/bioinformatics/btp187 Liu C., Shi L., Zhu Y., Chen H., Zhang J., Lin X., Guan X., 2012. CpGAVAS, an integrated web server for the annotation, visualization, analysis, and GenBank submission of completely sequenced chloroplast genome sequences. BMC Genomics 13:715. https://doi.org/10.1186/1471-2164-13-715" target="_blank">DOI: 10.1186/1471-2164-13-715 Lohse M., Drechsel O., Kahlau S., Bock R., 2013. Organellar Genome - DRAW - a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Res 41:W575-W58. https://doi.org/10.1093/nar/gkt289" target="_blank">DOI: 10.1093/nar/gkt289 Lopes A.S., Pacheco T.G., Santos K.G., Vieira L.N., Guerra M.P., Nodari R.O., Souza E.M., Pedrosa F.O., Rogalski M., 2017. The Linum usitatissimum L. plastome reveals atypical structural evolution, new editing sites, and the phylogenetic position of Linaceae within Malpighiales. Plant Cell Rep. 37:307-328. https://doi.org/10.1007/s00299-017-2231-z" target="_blank">DOI: 10.1007/s00299-017-2231-z Lopes A.S., Pacheco T.G., Nimz T., Vieira L.N., Guerra M.P., Nodari R.O., Souza E.M., Pedrosa F.O., Rogalski M., 2018.The complete plastome of macaw palm [Acrocomia aculeata (Jacq.) Lodd. ex Mart.] and extensive molecular analyses of the evolution of plastid genes in Arecaceae. Planta 247:1011-1030. https://doi.org/10.1007/s00425-018-2841-x" target="_blank">DOI: 10.1007/s00425-018-2841-x Manos P.S., Soltis P.S., Soltis D.E., et al., 2007.Phylogeny of Extant and Fossil Juglandaceae Inferred from the Integration of Molecular and Morphological Data Sets. Syst. Biol. 56:412-430. https://doi.org/10.1080/10635150701408523" target="_blank">DOI: 10.1080/10635150701408523 Matielo C.B.D'O., Lemos R.P.M., Sarzi D.S., Machado L.O., Beise D.C., Dobbler P.C.T., Castro R.M., Fett M.S., Roesch L.F.W., Camargo F.O., Stefenon V.M., 2019. Whole plastid genome sequences of two drug-type Cannabis: insights into the use of plastid in forensic analyses. Journal of Forensic Sciences https://doi.org/10.1111/1556-4029.14155" target="_blank">DOI: 10.1111/1556-4029.14155 Park I., Yang S., Kim W.J., et al., 2019. Sequencing and Comparative Analysis of the Chloroplast Genome of Angelica polymorpha and the Development of a Novel Indel Marker for Species Identification. Molecules 24:138. https://doi.org/10.3390/molecules24061038" target="_blank">DOI: 10.3390/molecules24061038 Perdereau P.C., Kelleher C.T., DouglasG.C., Hodkinson T.R., 2014. High levels of gene flow and genetic diversity in Irish populations of Salix caprea L. inferred from chloroplast and nuclear SSR markers. BMC Plant Biology 14:202. https://doi.org/10.1186/s12870-014-0202-x" target="_blank">DOI: 10.1186/s12870-014-0202-x Poletto I., Muniz M.F.B., Poletto T., Stefenon V.M., Baggiotto C., Ceconi D.E., 2015. Germination and development of pecan cultivar seedlings by seed stratification. Pesq. Agropec. Bras. 50:1232-1235.https://doi.org/10.1590/S0100-204X2015001200014" target="_blank">DOI: 10.1590/S0100-204X2015001200014 Poletto T., Stefenon V.M., Poletto I., Muniz M.F.B., 2018. Pecan Propagation: Seed Mass as a Reliable Tool for Seed Selection. Horticulturae 4:26. https://doi.org/10.3390/horticulturae4030026" target="_blank">DOI: 10.3390/horticulturae4030026 Poletto T., Poletto I., Silva L.M.M., Muniz M.F.B., Reiniger L.R.S., Richards N., Stefenon V.M., 2019.Morphological, chemical and genetic analysis of southern Brazilian pecan(Carya illinoinensis) accessions. Scientia Horticulturae https://doi.org/10.1016/j.scienta.2019.108863" target="_blank">DOI: 10.1016/j.scienta.2019.108863 Rogalski M., Vieira L.N., Fraga H.P., Guerra M.P., 2015.Plastid genomics in horticultural species: importance and applications for plant population genetics, evolution, and biotechnology. Front Plant Sci 6:586. https://doi.org/10.3389/fpls.2015.00586" target="_blank">DOI: 10.3389/fpls.2015.00586 Stanford A.M., Harden R., Parks C.R., 2000. Phylogeny and biogeography of Juglans (Juglandaceae) based on matK and its sequence data. Am. J. Bot. 87:872-882. https://doi.org/10.2307/2656895" target="_blank">DOI: 10.2307/2656895 Stefenon V.M., Kablunde G., Lemos R.P.M.,Rogalski M., Nodari R.O., 2019a. Phylogeography of plastid DNA sequences suggests post-glacial southward demographic expansion and the existence of several glacial refugia for Araucaria angustifolia. Scientific Reports 9:2752. https://doi.org/10.1038/s41598-019-39308-w" target="_blank">DOI: 10.1038/s41598-019-39308-w Stefenon V.M., Sarzi D.S., Roesch L.F.W., 2019b. High throughput sequencing analysis of Eugenia uniflora: insights into repetitive DNA, gene content and potential biotechnological applications. 3 Biotech 9:200. https://doi.org/10.1007/s13205-019-1729-1" target="_blank">DOI: 10.1007/s13205-019-1729-1 Tamura K., Stecher G., Peterson D., Filipski A., Kumar S., 2013. MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30:2725-2729. https://doi.org/10.1093/molbev/mst197" target="_blank">DOI: 10.1093/molbev/mst197 Tillich M., Lehwark P., Pellizzer T., 2017. GeSeq - versatile and accurate annotation of organelle genomes. Nucleic Acids Research 45:W6-W11. https://doi.org/10.1093/nar/gkx391" target="_blank">DOI: 10.1093/nar/gkx391 Vieira L.N., Rogalski M., Faoro H., Fraga H.P., Anjos K.G., Picchi G.F.A., Nodari R.O., Pedrosa F.O., Souza E.M., Guerra M.P., 2016. The plastome sequence of the endemic Amazonian conifer, Retro- phyllum piresii (Silba) C.N.Page, reveals different recombination events and plastome isoforms. Tree Genet Genomes 12:10. https://doi.org/10.1007/s11295-016-0968-0" target="_blank">DOI: 10.1007/s11295-016-0968-0 Wheeler G.L., Dorman H.E., Buchanan A., Challagundla L., Wallace L.E., 2014. A review of the prevalence, utility, and caveats of using chloroplast simple sequence repeats for studies of plant biology. Appl Plant Sci. https://doi.org/10.3732/apps.1400059" target="_blank">DOI: 10.3732/apps.1400059 Wicke S., Schneeweiss G.M., dePamphilis C.W., Müller K.F., Quandt D., 2011.The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Mol Biol 76:273-297https://doi.org/10.1007/s11103-011-9762-4" target="_blank">DOI: 10.1007/s11103-011-9762-4 Wolfe K.H., Li W.H., Sharp P.M., 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" target="_blank">DOI: 10.1073/pnas.84.24.9054 Ye L., Fu C., Wang Y., Liu J., Gao L., 2018. Characterization of the complete plastid genome of a Chinese endemic species Carya kweichowensis. Mitochondrial DNA Part B: Resources 3:492-493. https://doi.org/10.1080/23802359.2018.1464414" target="_blank">DOI: 10.1080/23802359.2018.1464414 Zhai D-C., Yao Q., Cao X-F., Hao Q-Q., Ma M-T., Pan J., Bai X-H., 2019.Complete chloroplast genome of the wild-type Hickory Carya cathayensis. Mitochondrial DNA Part B: Resources 4:1457-1458. https://doi.org/10.1080/23802359.2019.1598815" target="_blank">DOI: 10.1080/23802359.2019.1598815 Zhu A., Guo W., Gupta S., Fan W., Mower J.P., 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" target="_blank">DOI: 10.1111/nph.13743

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