Abstract
Main conclusion
Bignoniaceae species have conserved chloroplast structure, with hotspots of nucleotide diversity. Several genes are under positive selection, and can be targets for evolutionary studies.
Abstract
Bignoniaceae is one of the most species-rich family of woody plants in Neotropical seasonally dry forests. Here we report the assembly of Handroanthus impetiginosus chloroplast genome and evolutionary comparative analyses of ten Bignoniaceae species representing the genera for which whole-genome chloroplast sequences were available. The chloroplast genome of H. impetiginosus is 159,462 bp in size and has a similar structure compared to the other nine species. The total number of genes was slightly variable amongst the Bignoniaceae, ranging from 124 in H. impetiginosus to 144 in Anemopaegma acutifolium. The inverted repeat (IR) size was variable, ranging from 24,657 bp (Tecomaria capensis) to 40,481 bp (A. acutifolium), due to the contraction and retraction at its boundaries. However, gene boundaries were very similar among the ten species. We found 98 forward and palindromic dispersed repeats, and 85 simple sequence repeats (SSRs). In general, chloroplast sequences were highly conserved, with few nucleotide diversity hotspots in the genes accD, clpP, rpoA, ycf1, ycf2. The phylogenetic analysis based on 77 coding genes was highly consistent with Angiosperm Phylogeny Group (APG) IV. Our results also indicate that most genes are under negative selection or neutral evolution. We found no evidence of branch-site selection, implying that H. impetiginosus is not evolving faster than the other species analyzed, notwithstanding we found site positive selection signal in several genes. These genes can provide targets for evolutionary studies in Bignoniaceae and Lamiales species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability statement
Additional data are provided as supporting information in the online version of this article.
Abbreviations
- AICc:
-
Akaike Information Criterion corrected for small sample size
- FDR:
-
False Discovery Rate
- HMM:
-
Hidden Markov Model
- IR:
-
Inverted Repeat
- LSC:
-
Large Single Copy
- LRT:
-
Likelihood Ratio Test
- RSCU:
-
Relative Synonymous Codon Usage
- SSC:
-
Small Single Copy
- SSR:
-
Simple Sequence Repeats
References
Asaf S, Khan AL, Khan AR et al (2016) Complete chloroplast genome of Nicotiana otophora and its comparison with related species. Front Plant Sci 7:843. https://doi.org/10.3389/fpls.2016.00843
Beier S, Thiel T, Münch T et al (2017) MISA-web: a web server for microsatellite prediction. Bioinformatics 33:2583–2585. https://doi.org/10.1093/bioinformatics/btx198
Bouckaert R, Heled J, Kühnert D et al (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537. https://doi.org/10.1371/journal.pcbi.1003537
Brandvain Y, Wade MJ (2009) The functional transfer of genes from the mitochondria to the nucleus: the effects of selection, mutation, population size and rate of self-fertilization. Genetics 182:1129–1139. https://doi.org/10.1534/genetics.108.100024
Brudno M, Do CB, Cooper GM et al (2003) LAGAN and Multi-LAGAN: efficient tools for large-scale multiple alignment of genomic DNA. Genome Res 13:721–731
Chase MW, Cowan RS, Hollingsworth PM et al (2007) A proposal for a standardised protocol to barcode all land plants. Taxon 56:295–299
Chase MW, Christenhusz MJM, Fay MF et al (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20. https://doi.org/10.1111/boj.12385
Collevatti RG, Dornelas MC (2016) Clues to the evolution of genome size and chromosome number in Tabebuia alliance (Bignoniaceae). Plant Syst Evol 302:601–607. https://doi.org/10.1007/s00606-016-1280-z
Collevatti RG, Grattapaglia D, Hay JD (2003) Evidences for multiple maternal lineages of Caryocar brasiliense populations in the Brazilian Cerrado based on the analysis of chloroplast DNA sequences and microsatellite haplotype variation. Mol Ecol 12:105–115. https://doi.org/10.1046/j.1365-294X.2003.01701.x
Collevatti RG, Terribile LC, Lima-Ribeiro MS et al (2012) A coupled phylogeographical and species distribution modelling approach recovers the demographical history of a Neotropical seasonally dry forest tree species. Mol Ecol 21:5845–5863. https://doi.org/10.1111/mec.12071
Collevatti RG, Terribile LC, Rabelo SG, Lima-Ribeiro MS (2015) Relaxed random walk model coupled with ecological niche modeling unravel the dispersal dynamics of a Neotropical savanna tree species in the deeper Quaternary. Front Plant Sci 6:653. https://doi.org/10.3389/fpls.2015.00653
Cui Y, Nie L, Sun W et al (2019) Comparative and phylogenetic analyses of ginger (Zingiber officinale) in the family Zingiberaceae based on the complete chloroplast genome. Plants 8:283. https://doi.org/10.3390/plants8080283
Darriba D, Taboada GL, Doallo R, Posada D (2012) JModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772
Dastpak A, Osaloo SK, Maassoumi AA, Safar KN (2018) Molecular phylogeny of Astragalus sect. Ammodendron (Fabaceae) inferred from chloroplast ycf1 gene. Ann Bot Fenn 55:75–82. https://doi.org/10.5735/085.055.0108
De Melo WA, Lima-Ribeiro MS, Terribile LC, Collevatti RG (2016) Coalescent simulation and paleodistribution modeling for Tabebuia rosealba do not support south American dry forest refugia hypothesis. PLoS ONE 11(7):e0159314. https://doi.org/10.1371/journal.pone.0159314
Dong W, Xu C, Li C et al (2015) ycf1, the most promising plastid DNA barcode of land plants. Sci Rep 5:8348. https://doi.org/10.1038/srep08348
Drouin G, Daoud H, Xia J (2008) Relative rates of synonymous substitutions in the mitochondrial, chloroplast and nuclear genomes of seed plants. Mol Phylogenet Evol 49:827–831. https://doi.org/10.1016/j.ympev.2008.09.009
Ekblom R, Galindo J (2011) Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity (Edinb) 107:1–15
Fan WB, Wu Y, Yang J et al (2018) Comparative chloroplast genomics of dipsacales species: insights into sequence variation, adaptive evolution, and phylogenetic relationships. Front Plant Sci 9:689. https://doi.org/10.3389/fpls.2018.00689
Fargo DC, Boynton JE, Gillham NW (2001) Chloroplast ribosomal protein S7 of Chlamydomonas binds to chloroplast mRNA leader sequences and may be involved in translation initiation. Plant Cell 13:207–218. https://doi.org/10.1105/tpc.13.1.207
Firetti F, Zuntini AR, Gaiarsa JW et al (2017) Complete chloroplast genome sequences contribute to plant species delimitation: a case study of the Anemopaegma species complex. Am J Bot 104:1493–1509. https://doi.org/10.3732/ajb.1700302
Fischer N, Hippler M, Sétif P et al (1998) The PsaC subunit of photosystem I provides an essential lysine residue for fast electron transfer to ferredoxin. EMBO J 17:849–858. https://doi.org/10.1093/emboj/17.4.849
Fonseca LHM, Lohmann LG (2017) Plastome rearrangements in the “Adenocalymma-Neojobertia” clade (Bignonieae, Bignoniaceae) and its phylogenetic implications. Front Plant Sci 8:1875. https://doi.org/10.3389/fpls.2017.01875
Fonseca LHM, Lohmann LG (2018) Combining high-throughput sequencing and targeted loci data to infer the phylogeny of the “Adenocalymma-Neojobertia” clade (Bignonieae, Bignoniaceae). Mol Phylogenet Evol 123:1–15. https://doi.org/10.1016/j.ympev.2018.01.023
Frailey DC, Chaluvadi SR, Vaughn JN et al (2018) Gene loss and genome rearrangement in the plastids of five Hemiparasites in the family Orobanchaceae. BMC Plant Biol 18:1–12. https://doi.org/10.1186/s12870-018-1249-x
Francisco P, Ortega MJ (2007) The codon usage of leucine, serine and arginine reveals evolutionary stability of proteomes and protein-coding genes. In: Sagot M-F, Walter MEMT (eds) Bsb. Angra dos Reis, p 149
Frazer KA, Pachter L, Poliakov A et al (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Res 32:W273–W279. https://doi.org/10.1093/nar/gkh458
Gao C, Deng Y, Wang J (2019) The complete chloroplast genomes of Echinacanthus species (Acanthaceae): phylogenetic relationships, adaptive evolution, and screening of molecular markers. Front Plant Sci 9:1989. https://doi.org/10.3389/fpls.2018.01989
Gentry AH (1974) Coevolutionary patterns in Central American Bignoniaceae. Ann Missouri Bot Gard 61:728. https://doi.org/10.2307/2395026
Grantham R, Perrin P, Mouchiroud D (1986) Patterns in codon usage of different kinds of species. Oxford Surv Evol Biol 3:48–81
Grose SO, Olmstead RG (2007a) Taxonomic revisions in the polyphyletic genus Tabebuia s. l. (Bignoniaceae). Syst Bot 32:660–670. https://doi.org/10.1600/036364407782250652
Grose SO, Olmstead RG (2007b) Evolution of a charismatic neotropical clade: molecular phylogeny of Tabebuia s. l., Crescentieae, and allied genera (Bignoniaceae). Syst Bot 32:650–659. https://doi.org/10.1600/036364407782250553
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704. https://doi.org/10.1080/10635150390235520
Guisinger MM, Kuehl JV, Boore JL, Jansen RK (2008) Genome-wide analyses of Geraniaceae plastid DNA reveal unprecedented patterns of increased nucleotide substitutions. Proc Natl Acad Sci USA 105:18424–18429. https://doi.org/10.1073/pnas.0806759105
Guisinger MM, Chumley TW, Kuehl JV et al (2010) Implications of the plastid genome sequence of Typha (Typhaceae, Poales) for understanding genome evolution in Poaceae. J Mol Evol 70:149–166. https://doi.org/10.1007/s00239-009-9317-3
Harrison N, Harrison RJ, Kidner CA (2016) Comparative analysis of Begonia plastid genomes and their utility for species-level phylogenetics. PLoS ONE. https://doi.org/10.1371/journal.pone.0153248
Hernández-León S, Gernandt DS, Pérez de la Rosa JA, Jardón-Barbolla L (2013) Phylogenetic relationships and species delimitation in Pinus section Trifoliae inferrred from plastid DNA. PLoS ONE 8:70501. https://doi.org/10.1371/journal.pone.0070501
Hildebrand M, Hallick RB, Passavant CW, Bourque DP (1988) Trans-splicing in chloroplasts: the rps 12 loci of Nicotiana tabacum. Proc Natl Acad Sci USA 85:372–376. https://doi.org/10.1073/pnas.85.2.372
Huang S, Ge X, Cano A et al (2020) Comparative analysis of chloroplast genomes for five Dicliptera species (Acanthaceae): molecular structure, phylogenetic relationships, and adaptive evolution. PeerJ 2020:e8450. https://doi.org/10.7717/peerj.8450
Inagaki R, Ninomiya M, Tanaka K, Watanabe K, Koketsu M (2013) Synthesis and cytotoxicity on human leukemia cells of furonaphthoquinones isolated from Tabebuia plants. Chem Pharm Bull 61:670–673
Jiang M, Chen H, He S et al (2018) Sequencing, characterization, and comparative analyses of the plastome of Caragana rosea var. Rosea Int J Mol Sci 19:1419. https://doi.org/10.3390/ijms19051419
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Kumar S, Stecher G, Li M et al (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Kurtz S (2001) REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res 29:4633–4642. https://doi.org/10.1093/nar/29.22.4633
Lahaye R, Van Der Bank M, Bogarin D et al (2008) DNA barcoding the floras of biodiversity hotspots. Proc Natl Acad Sci USA 105:2923–2928. https://doi.org/10.1073/pnas.0709936105
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
Liu Q, Xue Q (2005) Comparative studies on codon usage pattern of chloroplasts and their host nuclear genes in four plant species. J Genet 84:55–62. https://doi.org/10.1007/BF02715890
Liu TJ, Zhang CY, Yan HF et al (2016) Complete plastid genome sequence of Primula sinensis (Primulaceae): structure comparison, sequence variation and evidence for accD transfer to nucleus. PeerJ. https://doi.org/10.7717/peerj.2101
Liu B, Tan YH, Liu S et al (2020) Phylogenetic relationships of Cyrtandromoea and Wightia revisited: a new tribe in Phrymaceae and a new family in Lamiales. J Syst Evol 58:1–17. https://doi.org/10.1111/jse.12513
Lohmann LG, Ulloa Ulloa C (2015) Bignoniaceae in iPlants prototype checklist. https://www.iplants.org/. Accessed 7 Jul 2020
Lohse M, Drechsel O, Kahlau S, Bock R (2013) OrganellarGenomeDRAW–a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Res 41:575–581. https://doi.org/10.1093/nar/gkt289
Ma PF, Zhang YX, Zeng CX et al (2014) Chloroplast phylogenomic analyses resolve deep-level relationships of an intractable Bamboo tribe Arundinarieae (Poaceae). Syst Biol 63:933–950. https://doi.org/10.1093/sysbio/syu054
Magee AM, Aspinall S, Rice DW et al (2010) Localized hypermutation and associated gene losses in legume chloroplast genomes. Genome Res 20:1700–1710. https://doi.org/10.1101/gr.111955.110
Marçais G, Kingsford C (2011) A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27:764–770. https://doi.org/10.1093/bioinformatics/btr011
Menezes APA, Resende-Moreira LC, Buzatti RSO et al (2018) Chloroplast genomes of Byrsonima species (Malpighiaceae): comparative analysis and screening of high divergence sequences. Sci Rep 8:2210. https://doi.org/10.1038/s41598-018-20189-4
Moghaddam M, Kazempour-Osaloo S (2020) Extensive survey of the ycf4 plastid gene throughout the IRLC legumes: robust evidence of its locus and lineage specific accelerated rate of evolution, pseudogenization and gene loss in the tribe Fabeae. PLoS ONE 15(3):e0229846. https://doi.org/10.1371/journal.pone.0229846
Moore MJ, Soltis PS, Bell CD et al (2010) Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots. Proc Natl Acad Sci USA 107:4623–4628. https://doi.org/10.1073/pnas.0907801107
Moreira PA, Mariac C, Scarcelli N et al (2016) Chloroplast sequence of treegourd (Crescentia cujete, Bignoniaceae) to study phylogeography and domestication. Appl Plant Sci 4:1600048. https://doi.org/10.3732/apps.1600048
Morton BR (1993) Chloroplast DNA codon use: evidence for selection at the psb A locus based on tRNA availability. J Mol Evol 37:273–280. https://doi.org/10.1007/BF00175504
Nazareno AG, Carlsen M, Lohmann LG (2015) Complete chloroplast genome of Tanaecium tetragonolobum: the first Bignoniaceae plastome. PLoS ONE 10:e0129930. https://doi.org/10.1371/journal.pone.0129930
Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273. https://doi.org/10.1073/pnas.76.10.5269
Nie X, Deng P, Feng K et al (2014) Comparative analysis of codon usage patterns in chloroplast genomes of the Asteraceae family. Plant Mol Biol Report 32:828–840. https://doi.org/10.1007/s11105-013-0691-z
Nielsen R, Yang Z (1998) Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148:929–936
Olmstead RG, Zjhra ML, Lohmann LG et al (2009) A molecular phylogeny and classification of Bignoniaceae. Am J Bot 96:1731–1743. https://doi.org/10.3732/ajb.0900004
Park BS, Kim JR, Lee SE, Kim KS, Takeoka GR, Ahn YJ, Kim JH (2005) Selective growth-inhibiting effects of compounds identified in Tabebuia impetiginosa inner bark on human intestinal bacteria. J Agric Food Chem 53:1152–1157
Pennington TR, Prado DE, Pendry CA (2000) Neotropical seasonally dry forests and Quaternary vegetation changes. J Biogeogr 27:261–273. https://doi.org/10.1046/j.1365-2699.2000.00397.x
Pennington TR, Lewis G, Ratter J (2006) An overview of the plant diversity, biogeography and conservation of neotropical savannas and seasonally dry forests. CRC Press, Boca Raton
Piot A, Hackel J, Christin PA, Besnard G (2018) One-third of the plastid genes evolved under positive selection in PACMAD grasses. Planta 247:255–266. https://doi.org/10.1007/s00425-017-2781-x
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rambaut A (2016) FigTree v1.4.3 software. Institute of Evolutionary Biology. Inst Evol Biol Univ Edinburgh
Redwan RM, Saidin A, Kumar SV (2015) Complete chloroplast genome sequence of MD-2 pineapple and its comparative analysis among nine other plants from the subclass Commelinidae. BMC Plant Biol 15:196. https://doi.org/10.1186/s12870-015-0587-1
Refulio-Rodriguez NF, Olmstead RG (2014) Phylogeny of Lamiidae. Am J Bot 101:287–299. https://doi.org/10.3732/ajb.1300394
Reveal JL (2011) Summary of recent systems of angiosperm classification. Kew Bull 66:5–48. https://doi.org/10.1007/s12225-011-9259-y
Ronquist F, Teslenko M, Van Der Mark P et al (2012) Mrbayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC et al (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248
Schulze M, Grogan J, Uhl C et al (2008) Evaluating ipê (Tabebuia, Bignoniaceae) logging in Amazonia: Sustainable management or catalyst for forest degradation? Biol Conserv 141:2071–2085. https://doi.org/10.1016/j.biocon.2008.06.003
Sharp PM, Tuohy TMF, Mosurski KR (1986) Codon usage in yeast: cluster analysis clearly differentiates highly and lowly expressed genes. Nucleic Acids Res 14:5125–5143. https://doi.org/10.1093/nar/14.13.5125
Shi C, Han K, Li L, et al (2019) Complete chloroplast genomes of 14 mangroves: phylogenetic and genomic comparative analyses. Biomed Res Int 2020: Article ID 8731857. https://doi.org/10.1101/787556
Silva-Junior OB, Grattapaglia D, Novaes E, Collevatti RG (2017) Genome assembly of the Pink Ipê (Handroanthus impetiginosus, Bignoniaceae), a highly-valued ecologically keystone Neotropical timber forest tree. Gigascience 7:1–12. https://doi.org/10.1093/gigascience/gix125
Stothard P (2000) The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques 28(6):1102–1104. https://doi.org/10.2144/00286ir01
Sugiura C, Kobayashi Y, Aoki S et al (2003) Complete chloroplast DNA sequence of the moss Physcomitrella patens: evidence for the loss and relocation of rpoA from the chloroplast to the nucleus. Nucleic Acids Res 31:5324–5331. https://doi.org/10.1093/nar/gkg726
Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577. https://doi.org/10.1080/10635150701472164
Thode VA, Lohmann LG (2019) Comparative chloroplast genomics at low taxonomic levels: a case study using Amphilophium (Bignonieae, Bignoniaceae). Front Plant Sci 10:796. https://doi.org/10.3389/fpls.2019.00796
Tillich M, Lehwark P, Pellizzer T et al (2017) GeSeq—versatile and accurate annotation of organelle genomes. Nucleic Acids Res 45:W6–W11. https://doi.org/10.1093/nar/gkx391
Vaidya G, Lohman DJ, Meier R (2011) SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27:171–180. https://doi.org/10.1111/j.1096-0031.2010.00329.x
Vitorino LC, Lima-Ribeiro MS, Terribile LC, Collevatti RG (2018) Demographical expansion of Handroanthus ochraceus in the Cerrado during the Quaternary: Implications for the genetic diversity of Neotropical trees. Biol J Linn Soc 123:561–577. https://doi.org/10.1093/biolinnean/blx163
Wolfe KH, Li WH, 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
Xu C, Dong J, Tong C et al (2013) Analysis of synonymous codon usage patterns in seven different citrus species. Evol Bioinforma 2013:215–228. https://doi.org/10.4137/EBO.S11930
Xu JH, Liu Q, Hu W et al (2015) Dynamics of chloroplast genomes in green plants. Genomics 106:221–231. https://doi.org/10.1016/j.ygeno.2015.07.004
Xu C, Dong W, Li W et al (2017) Comparative analysis of six Lagerstroemia complete chloroplast genomes. Front Plant Sci 8:15. https://doi.org/10.3389/fpls.2017.00015
Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591
Yang Z, Nielsen R (2002) Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 19:908–917. https://doi.org/10.1093/oxfordjournals.molbev.a004148
Yang Z, Nielsen R, Goldman N, Pedersen AMK (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449
Yang Z, Wong WSW, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118. https://doi.org/10.1093/molbev/msi097
Yi X, Gao L, Wang B et al (2013) The complete chloroplast genome sequence of Cephalotaxus oliveri (Cephalotaxaceae): Evolutionary comparison of Cephalotaxus chloroplast DNAs and insights into the loss of inverted repeat copies in gymnosperms. Genome Biol Evol 5:688–698. https://doi.org/10.1093/gbe/evt042
Yin K, Zhang Y, Li Y, Du FK (2018) Different natural selection pressures on the atpF gene in evergreen sclerophyllous and deciduous oak species: evidence from comparative analysis of the complete chloroplast genome of Quercus aquifolioides with other oak species. Int J Mol Sci 19(4):1042. https://doi.org/10.3390/ijms19041042
Zhang J, Nielsen R, Yang Z (2005) Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22:2472–2479. https://doi.org/10.1093/molbev/msi237
Zhang Y, Nie X, Jia X et al (2012) Analysis of codon usage patterns of the chloroplast genomes in the Poaceae family. Aust J Bot 60:461–470. https://doi.org/10.1071/BT12073
Zhou T, Chen C, Wei Y et al (2016) Comparative transcriptome and chloroplast genome analyses of two related Dipteronia species. Front Plant Sci 7:1512. https://doi.org/10.3389/fpls.2016.01512
Zong D, Zhou A, Zhang Y et al (2019) Characterization of the complete chloroplast genomes of five Populus species from the western Sichuan plateau, southwest China: comparative and phylogenetic analyses. PeerJ. https://doi.org/10.7717/peerj.6386
Acknowledgements
This work was supported by competitive grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) to RGC (project no. 470306/2013-0 and CNPq/PPBio project no. 457406/2012-7), and Procad/Capes project # 88881.068425/2014-01), and to DG (PRONEX FAP-DF Project Grant “NEXTREE” 193.000.570/2009). RGC and DG have been supported by productivity grants from CNPq, which we acknowledge. MBS and LDV received a doctoral fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). RN received a fellowship from Nacional Institutes for Science and Technology in Ecology, Evolution and Biodiversity Conservation (INCT—EECBio), supported by CNPq and Fundação de Amparo à Pesquisa do Estado de Goiás (FAPEG).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sobreiro, M.B., Vieira, L.D., Nunes, R. et al. Chloroplast genome assembly of Handroanthus impetiginosus: comparative analysis and molecular evolution in Bignoniaceae. Planta 252, 91 (2020). https://doi.org/10.1007/s00425-020-03498-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-020-03498-9