Abstract
Theobroma is a plant genus included in tribe Theobromeae, subfamily Byttnerioideae Burnett and family Malvaceae. Discrepancies exist in taxonomy at family and genus level. Here, we compared structures of two previously reported chloroplast genomes of Theobroma cacao and Theobroma grandiflorum after correction of annotation and search for highly polymorphic regions which could be used to design molecular markers to investigate phylogenetic relationships among the genus. Both chloroplast genomes showed similar structure, gene content and organization. The correctly annotated genomes contained 130 genes including 8 ribosomal RNA, 37 tRNA genes and 85 protein-coding genes. The amino acids frequencies, codon usage, putative RNA editing sites, microsatellites and oligonucleotide repeats were alike in two genomes. Polymorphic hotspot regions were mostly observed in intergenic regions followed by intronic regions, as well as in coding sequences of few genes. We identified 30 polymorphic loci including trnH-psbA, ndhE-ndhG, rpl32-trnL, trnP-PsaJ, rpl33-rps18, trnQ-psbK, trnS-trnG, and ndhF-rpl32 that might be suitable for development of appropriate and suitable markers for inferring of genus Theobroma phylogeny. The inferring of phylogeny with the markers of these loci might be helpful to identify genetically compatible and closely related species to T. cacao and T. grandiflorum for breeding purposes to produce quality cultivars of these species for high quantity of fruit production and with high resistance towards the pathogens.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- LSC:
-
large single copy
- SSC:
-
small single copy
- IR:
-
inverted repeat regions
- Ts/Tv:
-
ratio of transition to transversion substitutions
- SNPs:
-
single nucleotide polymorphisms
- InDels:
-
Insertions and deletions
- Ts:
-
Transitions substitutions
- Tv :
-
Transversion substitutions
- MAFFT:
-
Multiple Alignment using Fast Fourier Transform
- IGS:
-
Intergenic spacer regions
- SSR:
-
Simple sequence repeats
References
Abdullah MF, Shahzadi I, Waseem S, Mirza B, Ahmed I, Waheed MT (2019b) Chloroplast genome of Hibiscus rosa-sinensis (Malvaceae): comparative analyses and identification of mutational hotspots. Genomics. (in press) https://doi.org/10.1016/j.ygeno.2019.04.010
Abdullah, Shahzadi I, Mehmood F, Ali Z, Malik MS, Waseem S, Mirza B, Ahmed I, Waheed MT (2019a) Comparative analyses of chloroplast genomes among three Firmiana species: identification of mutational hotspots and phylogenetic relationship with other species of Malvaceae. Plant Gene 19:100199. https://doi.org/10.1016/J.PLGENE.2019.100199
Ahmed I (2014) Evolutionary dynamics in taro. Dissertation, Massey University, Palmerston North, New Zealand
Ahmed I, Biggs PJ, Matthews PJ, Collins LJ, Hendy MD, Lockhart PJ (2012) Mutational dynamics of aroid chloroplast genomes. Genome Biol Evol 4:1316–1323. https://doi.org/10.1093/gbe/evs110
Ahmed I, Matthews PJ, Biggs PJ, Naeem M, Mclenachan PA, Lockhart PJ (2013) Identification of chloroplast genome loci suitable for high-resolution phylogeographic studies of Colocasia esculenta (L.) Schott (Araceae) and closely related taxa. Mol Ecol Resour 13:929–937. https://doi.org/10.1111/1755-0998.12128
Alves RM, Sebbenn AM, Artero AS, Clement C, Figueira A (2007) High levels of genetic divergence and inbreeding in populations of cupuassu (Theobroma grandiflorum). Tree Genet Genomes 3:289–298. https://doi.org/10.1007/s11295-006-0066-9
Amiryousefi A, Hyvönen J, Poczai P (2018) The chloroplast genome sequence of bittersweet (Solanum dulcamara): plastid genome structure evolution in Solanaceae. PLoS One 13:1–23. https://doi.org/10.1371/journal.pone.0196069
Bailey JA, Nash C, Morgan LW, O’Connell RJ, TeBeest DO (1996) Molecular taxonomy of Colletotrichum species causing anthracnose on the Malvaceae. Phytopathology 86:1076–1083. https://doi.org/10.1094/Phyto-86-1076
Bartley BGD (2005) The genetic diversity of cacao and its utilization. CABI, Wallingford
Bock R, Khan MS (2004) Taming plastids for a green future. Trends Biotechnol 22:311–318. https://doi.org/10.1016/j.tibtech.2004.03.005
Cai J, Ma PF, Li HT, Li DZ (2015) Complete plastid genome sequencing of four Tilia species (Malvaceae): a comparative analysis and phylogenetic implications. PLoS One 10:1–13. https://doi.org/10.1371/journal.pone.0142705
Cavalcante PB (1991) Frutas comestíveis da Amazônia. Edições CEJUP
Christenhusz MJM, Byng JW (2016) The number of known plants species in the world and its annual increase. Phytotaxa 261:201–217. https://doi.org/10.11646/phytotaxa.261.3.1
Cooper G (2000) Chloroplasts and other plastids in the cell: a molecular approach, 2nd edn. Sunderland (MA): Sinauer Associates
Cuatrecasas J (1964) Cacao and its allies: a taxonomic revision of the genus Theobroma. Natl Herb 35:379–607. https://doi.org/10.1016/0165-5728(95)00055-7
Daniell H, Lin C-S, Yu M, Chang W-J (2016) Chloroplast genomes: diversity, evolution, and applications in genetic engineering. Genome Biol 17:134. https://doi.org/10.1186/s13059-016-1004-2
Downie SR, Palmer JD (1992) Use of chloroplast DNA rearrangements in reconstructing plant phylogeny. In: Molecular systematics of plants. Springer US, Boston, pp 14–35
Gopaulchan D, Motilal LA, Bekele FL, Clause S, Ariko JO, Ejang HP, Umaharan P (2019) Morphological and genetic diversity of cacao (Theobroma cacao L.) in Uganda. Physiol Mol Biol Plants 25:361–375. https://doi.org/10.1007/s12298-018-0632-2
Guo X, Liu J, Hao G, Zhang L, Mao K, Wang X, Zhang D, Ma T, Hu Q, Al-Shehbaz IA, Koch MA (2017) Plastome phylogeny and early diversification of Brassicaceae. BMC genomics 18:176–284. https://doi.org/10.1186/s12864-017-3555-3
Gutiérrez-López N, Ovando-Medina I, Salvador-Figueroa M, Molina-Freaner F, Avendaño-Arrazate CH, Vázquez-Ovando A (2016) Unique haplotypes of cacao trees as revealed by trnH-psbA chloroplast DNA. PeerJ 4:e1855. https://doi.org/10.7717/peerj.1855
Jansen RK, Saski C, Lee S-B, Hansen AK, Daniell H (2011) Complete plastid genome sequences of three Rosids (Castanea, Prunus, Theobroma): evidence for at least two independent transfers of rpl22 to the nucleus. Mol Biol Evol 28:835–847. https://doi.org/10.1093/molbev/msq261
Jheng C-F, Chen T-C, Lin J-Y, Chen T-C, Wu W-L, Chang C-C (2012) The comparative chloroplast genomic analysis of photosynthetic orchids and developing DNA markers to distinguish Phalaenopsis orchids. Plant Sci 190:62–73. https://doi.org/10.1016/j.plantsci.2012.04.001
Kane N, Sveinsson S, Dempewolf H, Yang JY, Zhang D, Engels JMM, Cronk Q (2012) Ultra-barcoding in cacao (Theobroma spp.; Malvaceae) using whole chloroplast genomes and nuclear ribosomal DNA. Am J Bot 99:320–329. https://doi.org/10.3732/ajb.1100570
Katoh K, Kuma KI, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518. https://doi.org/10.1093/nar/gki198
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 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Kim K, Lee SC, Lee J, Lee HO, Joh HJ, Kim NH, Park HS, Yang TJ (2015) Comprehensive survey of genetic diversity in chloroplast genomes and 45S nrDNAs within Panax ginseng species. PLoS One 10:1–14. https://doi.org/10.1371/journal.pone.0117159
Kim YM, Kim S, Koo N et al (2017) Genome analysis of Hibiscus syriacus provides insights of polyploidization and indeterminate flowering in woody plants. DNA Res 24:71–80. https://doi.org/10.1093/dnares/dsw049
Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R (2001) REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res 29:4633–4642
Lee HJ, Koo HJ, Lee J et al (2017) Authentication of Zanthoxylum species based on integrated analysis of complete chloroplast genome sequences and metabolite profiles. J Agric Food Chem 65:10350–10359. https://doi.org/10.1021/acs.jafc.7b04167
Litz R (2005) Theobroma cacao. In Biotechnology of fruit and nut crops, CABI
Lössl AG, Waheed MT (2011) Chloroplast-derived vaccines against human diseases: achievements, challenges and scopes. Plant Biotechnol J 9:527–539. https://doi.org/10.1111/j.1467-7652.2011.00615.x
Matsuoka Y, Yamazaki Y, Ogihara Y, Tsunewaki K (2002) Whole chloroplast genome comparison of rice, maize, and wheat: implications for chloroplast gene diversification and phylogeny of cereals. Mol Biol Evol 19:2084–2091
Menezes APA, Resende-Moreira LC, Buzatti RSO, Nazareno AG, Carlsen M, Lobo FP, Kalapothakis E, Lovato MB (2018) Chloroplast genomes of Byrsonima species (Malpighiaceae): comparative analysis and screening of high divergence sequences. Sci Rep 8:1–12. https://doi.org/10.1038/s41598-018-20189-4
Morton BR, Oberholzer VM, Clegg MT (1997) The influence of specific neighboring bases on substitution bias in noncoding regions of the plant chloroplast genome. J Mol Evol 45:227–231
Motamayor JC, Lachenaud P, da Silva e Mota JW, Loor R, Kuhn DN, Brown JS, Schnell RJ (2008) Geographic and genetic population differentiation of the Amazonian chocolate tree (Theobroma cacao L). PLoS One 3:e3311. https://doi.org/10.1371/journal.pone.0003311
Motamayor JC, Mockaitis K, Schmutz J et al (2013) The genome sequence of the most widely cultivated cacao type and its use to identify candidate genes regulating pod color. Genome Biol:14. https://doi.org/10.1186/gb-2013-14-6-r53
Motamayor JC, Risterucci AM, Lopez PA, Ortiz CF, Moreno A, Lanaud C (2002) Cacao domestication I: the origin of the cacao cultivated by the Mayas. Heredity (Edinb) 89:380–386. https://doi.org/10.1038/sj.hdy.6800156
Mower JP (2009) The PREP suite: predictive RNA editors for plant mitochondrial genes, chloroplast genes and user-defined alignments. Nucleic Acids Res 37:W253–W259. https://doi.org/10.1093/nar/gkp337
Nguyen VB, Linh Giang VN, Waminal NE, Park HS, Kim NH, Jang W, Lee J, Yang TJ (2018) Comprehensive comparative analysis of chloroplast genomes from seven Panax species and development of an authentication system based on species-unique single nucleotide polymorphism markers. J Ginseng Res. https://doi.org/10.1016/j.jgr.2018.06.003
Nguyen VB, Park H-S, Lee S-C, Lee J, Park JY, Yang T-J (2017) Authentication markers for five major Panax species developed via comparative analysis of complete chloroplast genome sequences. J Agric Food Chem 65:6298–6306. https://doi.org/10.1021/acs.jafc.7b00925
Osorio-Guarín JA, Berdugo-Cely J, Coronado RA, Zapata YP, Quintero C, Gallego-Sánchez G, Yockteng R (2017) Colombia a source of cacao genetic diversity as revealed by the population structure analysis of germplasm bank of Theobroma cacao L. Front Plant Sci 8:1994. https://doi.org/10.3389/fpls.2017.01994
Palmer JD (1985) Comparative organization of chloroplast genomes. Annu Rev Genet 19:325–354. https://doi.org/10.1146/annurev.ge.19.120185.001545
Purseglove JW (1968) Tropical crops: Dicotyledons 1 and 2. Trop Crop Dicotyledons 1:2
Raman G, Park V, Kwak M, Lee B, Park SJ (2017) Characterization of the complete chloroplast genome of Arabis stellari and comparisons with related species. PLoS One 12:1–18. https://doi.org/10.1371/journal.pone.0183197
Richardson JE, Whitlock BA, Meerow AW, Madriñán S (2015) The age of chocolate: a diversification history of Theobroma and Malvaceae. Front Ecol Evol 3:1–14. https://doi.org/10.3389/fevo.2015.00120
Saina JK, Li ZZ, Gichira AW, Liao YY (2018) The complete chloroplast genome sequence of tree of heaven (Ailanthus altissima (mill.) (Sapindales: Simaroubaceae), an important pantropical tree. Int J Mol Sci 19:. doi: https://doi.org/10.3390/ijms19040929
Sloan DB, Triant DA, Forrester NJ, Bergner LM, Wu M, Taylor DR (2014) A recurring syndrome of accelerated plastid genome evolution in the angiosperm tribe Sileneae (Caryophyllaceae). Mol Phylogenet Evol 72:82–89. https://doi.org/10.1016/J.YMPEV.2013.12.004
Thiel T, Michalek W, Varshney R, Graner A (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet 106:411–422. https://doi.org/10.1007/s00122-002-1031-0
Thomas E, van Zonneveld M, Loo J, Hodgkin T, Galluzzi G, van Etten J (2012) Present spatial diversity patterns of Theobroma cacao L. in the Neotropics reflect genetic differentiation in Pleistocene Refugia followed by human-influenced dispersal. PLoS one 7:e47676. https://doi.org/10.1371/journal.pone.0047676
Tillich M, Lehwark P, Pellizzer T, Ulbricht-Jones ES, Fischer A, Bock R, Greiner S (2017) GeSeq – versatile and accurate annotation of organelle genomes. Nucleic Acids Res 45:W6–W11. https://doi.org/10.1093/nar/gkx391
Wambugu PW, Brozynska M, Furtado A, Waters DL, Henry RJ (2015) Relationships of wild and domesticated Rices (Oryza AA genome species) based upon whole chloroplast genome sequences. Sci Rep 5:13957–13966. https://doi.org/10.1038/srep13957
Wyman SK, Jansen RK, Boore JL (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20:3252–3255. https://doi.org/10.1093/bioinformatics/bth352
Xu J-H, Liu Q, Hu W, Wang T, Xue Q, Messing J (2015) Dynamics of chloroplast genomes in green plants. Genomics 106:221–231. https://doi.org/10.1016/J.YGENO.2015.07.004
Xu Q, Xiong G, Li P, He F, Huang Y, Wang K, Li Z, Hua J (2012) Analysis of complete nucleotide sequences of 12 Gossypium chloroplast genomes: origin and evolution of Allotetraploids. PLoS One 7. https://doi.org/10.1371/journal.pone.0037128
Xu Z, Deng M (2017) Malvaceae. In: identification and control of common weeds, 1st edn. Springer Netherlands, pp 717–735
Yang JY, Motilal LA, Dempewolf H, Maharaj K, Cronk QCB (2011) Chloroplast microsatellite primers for cacao ( Theobroma cacao ) and other Malvaceae. Am J Bot 98:e372–e374. https://doi.org/10.3732/ajb.1100306
Yang X, Luo X, Cai X (2014) Analysis of codon usage pattern in Taenia saginata based on a transcriptome dataset. Parasit vectors 7:527–537. https://doi.org/10.1186/s13071-014-0527-1
Yang Y, Zhou T, Duan D, Yang J, Feng L, Zhao G (2016) Comparative analysis of the complete chloroplast genomes of five Quercus species. Front Plant Sci 7:959–972. https://doi.org/10.3389/fpls.2016.00959
Yu X, Zuo L, Lu D, Lu B, Yang M, Wang J (2019) Comparative analysis of chloroplast genomes of five Robinia species: genome comparative and evolution analysis. Gene 689:141–151. https://doi.org/10.1016/J.GENE.2018.12.023
Zhang D, Figueira A, Motilal L, Lachenaud P, Meinhardt LW (2011) Theobroma. In: Wild crop relatives: genomic and breeding resources. Springer, Berlin Heidelberg, Berlin, Heidelberg, pp 277–296
Zhao K-K, Wang J-H, Cai Y-C, Zhu Z-X, López-Pujol J, Wang H-F (2018) Complete chloroplast genome sequence of Heritiera angustata (Malvaceae): an endangered plant species. Mitochondrial DNA Part B Resour 3:141–142. https://doi.org/10.1080/23802359.2017.1422398
Acknowledgments
We are thankful to Higher Education Commission of Pakistan for provision of funds to scholar Abdullah under indigenous scholarship program.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Ethical statement
Ethics related study was not performed in current research.
Conflict of interest
There is no conflict exist for any author of this study.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(DOCX 52 kb)
Rights and permissions
About this article
Cite this article
Abdullah, Waseem, S., Mirza, B. et al. Comparative analyses of chloroplast genomes of Theobroma cacao and Theobroma grandiflorum. Biologia 75, 761–771 (2020). https://doi.org/10.2478/s11756-019-00388-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11756-019-00388-8