Research article

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

Jordana Caroline Nagel, Lilian de Oliveira Machado, Rafael Plá Matielo Lemos, Cristiane Barbosa D’Oliveira Matielo, Tales Poletto, Igor Poletto, Valdir Marcos Stefenon

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. Email: valdirstefenon@gmail.com

Online First: March 02, 2020
Nagel, J., de Oliveira Machado, L., Plá Matielo Lemos, R., Barbosa D’Oliveira Matielo, C., Poletto, T., Poletto, I., Marcos Stefenon, V. 2020. Structural, evolutionary and phylogenomic features of the plastid genome of Carya illinoinensis cv. Imperial. Annals of Forest Research DOI:10.15287/afr.2019.1413


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.

Amiryousefi A., Hyvönen J., Poczai P., 2018. IRscope: an online program to visualize the junction sites of chloroplast genomes. Bioinformatics 34:3030-3031. 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. 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. 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. 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. 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. 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. 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. DOI: 10.1038/srep16958

Edgar R.C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797. 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. 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. 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. 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. 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. 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. DOI: 10.3390/biology7030043

Librado P., Rozas J., 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452. 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. 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. 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. 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. 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. 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 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. 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. 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.
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. 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 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. 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. 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. 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. 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. 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. 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. 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. 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 76:273-297
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. 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. 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. 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.
DOI: 10.1111/nph.13743


Supporting Information
| DOWNLOAD 334KB
No metrics available for this article.