Abstract
The fruits of P. philadelphica are of economic value in Mexico. The plants grow wild or cultivated in traditional farming systems. They are also produced as monoculture. Between the wild and cultivated pools, morphological and physiological differences exist. Plant breeding and the shift towards monoculture could modify the plastome sequence and influence the expression of certain genes. Our objectives were threefold. First, we obtained the complete sequence of the domesticated pool plastome. Then, we compared this to the plastome from the wild pool. Finally, we identified the changes that could be related to the domestication process. The plastome of the Manzano race was sequenced, characterized and compared with the plastome of the Milpero (wild) race. The plastomes had the typical circular and quadripartite structure but differed by 52 bp (domesticated 156,856 bp, wild 156,804 bp). A total of 115 genes and five pseudogenes were identified. In addition, 29 SNPs were detected in coding regions along with 19 polymorphic microsatellites. The complete sequences were highly conserved with an identity of 99.6%. No major differences were found in the coding regions that could be attributed to selection and the change from wild to monoculture. InDels in non-coding regions produced more variation. The variation observed was similar to that detected in other managed species.
References
Alcalá-Gómez G, Pérez-Alquicira J, Cabrera-Toledo D et al (2021) Genetic diversity and structure in husk tomato (Physalis philadelphica Lam.) based on SNPs: a case of diffuse domestication. Genet Resour Crop Evol. https://doi.org/10.1007/s10722-021-01278-2
Allaby RG (2015) Barley domestication: the end of a central dogma? Genome Biol 16:176. https://doi.org/10.1186/s13059-015-0743-9
Andrews S (2010) FastQC: a quality control tool for high throughput sequence dat. https://www.bioinformatics.babraham.ac.uk/projects/fastqc/
Bankevich A, Nurk S, Antipov D et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021
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
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Carbonell-Caballero J, Alonso R, Ibáñez V et al (2015) A phylogenetic analysis of 34 chloroplast genomes elucidates the relationships between wild and domestic species within the genus Citrus. Mol Biol Evol 32:2015–2035. https://doi.org/10.1093/molbev/msv082
Cárdenas-Castro AP, Perales-Vázquez GC, De la Rosa LA et al (2019) Sauces: an undiscovered healthy complement in Mexican cuisine. Int J Gastron Food Sci 17:100154. https://doi.org/10.1016/j.ijgfs.2019.100154
Chan PP, Lowe TM (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
Cho MS, Yoon HS, Kim SC (2018) Complete chloroplast genome of cultivated flowering cherry Prunus × yedoensis ‘Somei-yoshino’ in comparison with wild Prunus yedoensis Matsum (Rosaceae). Mol Breed 38:112. https://doi.org/10.1007/s11032-018-0871-5
D’Agostino N, Tamburino R, Cantarella C et al (2018) The complete plastome sequences of eleven Capsicum genotypes: insights into DNA variation and molecular evolution. Genes 9:503. https://doi.org/10.3390/genes9100503
Daniell H, Lin C, Yu M et al (2016) Chloroplast genomes: diversity evolution and applications in genetic engineering. Genome Biol 17:134. https://doi.org/10.1186/s13059-016-1004-2
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
Feng LY, Liu J, Gao CW et al (2020a) Higher genomic variation in wild than cultivated rubber trees Hevea brasiliensis revealed by comparative analyses of chloroplast genomes. Front Ecol Evol 8:237
Feng S, Zheng K, Jiao K et al (2020b) Complete chloroplast genomes of four Physalis species (Solanaceae): lights into genome structure comparative analysis and phylogenetic relationships. Plant Biol 20:242. https://doi.org/10.1186/s12870-020-02429-w
Fischer G, Almanza-Merchán PJ, Miranda D (2014) Importancia y cultivo de la uchuva (Physalis peruviana L). Rev Bras Frutic 36:1–15. https://doi.org/10.1590/0100-2945-441/13
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
Fu CN, Wu CS, Ye LJ et al (2019) Prevalence of isomeric plastomes and effectiveness of plastome super-barcodes in yews (Taxus) worldwide. Sci Rep 9:2773. https://doi.org/10.1038/s41598-019-39161-x
Greiner S, Lehwark P, Bock R (2019) OrganellarGenomeDRAW (OGDRAW) version 131: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Res 47:W59–W64. https://doi.org/10.1093/nar/gkz238
Guo X, Castillo-Ramírez S, González V et al (2007) Rapid evolutionary change of common bean (Phaseolus vulgaris L.) plastome and the genomic diversification of legume chloroplasts. BMC Genomics 8:228. https://doi.org/10.1186/1471-2164-8-228
Gurevich A, Saveliev V, Vyahhi N et al (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics 29:1072–1075. https://doi.org/10.1093/bioinformatics/btt086
Hazra A, Mahadani P, Das S et al (2021) Insight to the ancestral relations and varietal diversity of Indian tea [Camellia sinensis (L.) Kuntze] through plastid and nuclear phylogenetic markers. Genet Resour Crop Evol 68:773–783. https://doi.org/10.1007/s10722-020-01022-2
Hu S, Sablok G, Wang B et al (2015) Plastome organization and evolution of chloroplast genes in Cardamine species adapted to contrasting habits. BMC Genomics 16:306. https://doi.org/10.1186/s12864-015-1498-0
Hudson WD (1986) Relationships of domesticated and wild Physalis philadelphica. In: D’Arcy WG (ed) Solanaceae: biology and systematics. Columbia Univ Press, New York, pp 416–432
Jian HY, Zhang YH, Yan HJ et al (2018) The complete chloroplast genome of a key ancestor of modern roses Rosa chinensis var spontanea and a comparison with congeneric species. Molecules 23:389. https://doi.org/10.3390/molecules23020389
Jimenez HJ, da Silva ADF, Martins LSS et al (2020) Comparative genomics plastomes of the Amaryllidaceae family species. Sci Plena 16:060202. https://doi.org/10.14808/sci.plena.2020.060202
Kaur H, Singh BP, Singh H et al (2014) Comparative genomics of ten solanaceous plastomes. Adv Bioinform. https://doi.org/10.1155/2014/424873
Kazutaka 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
Labate JA, Robertson L (2015) Nucleotide diversity estimates of tomatillo (Physalis philadelphica) accessions including nine new inbred lines. Mol Breed 35:1–10. https://doi.org/10.1007/s11032-015-0302-9
Langmead B, Salzberg S (2012) Fast gapped-read alignment with Bowtie 2m. Nat Methods 9:357–359
Li S, Qu X, Zhong M et al (2019) Characterization of the complete chloroplast genome of Rosa chinensis ‘Old Blush’ (Rosaceae) an important cultivated Chinese rose. Acta Hortic 1232:119–124. https://doi.org/10.17660/ActaHortic.2019.1232.19
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 4:e2101. https://doi.org/10.7717/peerj.2101
Liu S, Wang Z, Su Y et al (2021) Comparative genomic analysis of Polypodiaceae chloroplasts reveals fine structural features and dynamic insertion sequences. BMC Plant Biol 21:3. https://doi.org/10.1186/s12870-020-02800-x
Logacheva MD, Samigullin TH, Dhingra A et al (2008) Comparative chloroplast genomics and phylogenetics of Fagopyrum esculentum ssp ancestrale- a wild ancestor of cultivated buckwheat. MBC Plant Biol 8:59. https://doi.org/10.1186/1471-2229-8-59
Magdy M, Ou L, Yu H et al (2019) Pan-plastome approach empowers the assessment of genetic variation in cultivated Capsicum species. Hortic Res 6:108. https://doi.org/10.1038/s41438-019-0191-x
Makarenko MS, Usatov AV, Markin NV et al (2016) Comparative genomics of domesticated and wild sunflower: complete chloroplast and mitochondrial genomes OnLine. J Biol Sci 16:71–75. https://doi.org/10.3844/ojbsci.2016.71.75
Martín M, Sabater B (2010) Plastid ndh genes in plant evolution. Plant Physiol Biochem 48:636–645. https://doi.org/10.1016/j.plaphy.2010.04.009
Martín M, Casano LM, Sabater B (1996) Identification of the product of ndhA gene as a thylakoid protein synthesized in response to photooxidative treatment. Plant Cell Physiol 376:293–298. https://doi.org/10.1093/oxfordjournals.pcp.a028945
Martinez M (1998) Revision of Physalis section epeteiorhiza (Solanaceae). Anales Inst Biol Univ Nac Autón México Bot 69:71–117
Martínez M, Vargas-Ponce O, Rodríguez A et al (2017) Solanaceae family in Mexico. Bot Sci 95:1–15. https://doi.org/10.17129/botsci.658
Martínez-Ainsworth NE, Tenaillon MI (2016) Superheroes and masterminds of plant domestication. C R Biol 339:268–273. https://doi.org/10.1016/j.crvi.2016.05.005
Montes-Hernández S, Aguirre-Rivera AR (1994) Etnobotánica del tomate mexicano (Physalis philadelphica Lam.). Revista de Geografía Agrícola 20:163–172
Montes S, Aguirre JR, García E et al (1991) Algunos efectos de la domesticación sobre la morfología del tomate. Agrociencia 2:7–26
Montes-Hernández S (1991) Tomate de cáscara (Physalis philadelphica Lam). In: Ortega P, Palomino G, Castillo F et al (eds) Avances en el estudio de los recursos fitogenéticos de México. Sociedad Mexicana de Fitogenética Mexico, pp 251–259
Muraguri S, Xu W, Chapman M et al (2020) Intraspecific variation within Castor bean (Ricinus communis L.) based on chloroplast genomes. Ind Crops Prod 155:112779. https://doi.org/10.1016/j.indcrop.2020.112779
Nguyen VB, Linh VN, Waminal NE et al (2020) 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 44:135–144. https://doi.org/10.1016/j.jgr.2018.06.003
Nikiforova SV, Cavalieri D, Velasco R et al (2013) Phylogenetic analysis of 47 chloroplast genomes clarifies the contribution of wild species to the domesticated apple maternal line. Mol Biol Evol 30:1751–1760. https://doi.org/10.1093/molbev/mst092
Nock CJ, Hardner CM, Montenegro JD et al (2019) Wild origins of macadamia domestication identified through intraspecific chloroplast genome sequencing. Front Plant Sci 10:334. https://doi.org/10.3389/fpls.2019.00334
Omelchenko DO, Krinitsina AA, Belenikin MS et al (2020) Complete plastome sequencing of Allium paradoxum reveals unusual rearrangements and the loss of the ndh genes as compared to Allium ursinum and other onions. Gene 726:144154. https://doi.org/10.1016/j.gene.2019.144154
Peña A, Santiaguillo JF, Magaña N (2007) Recursos y mejoramiento genético de tomate de cáscara (Physalys ixocarpa Brot). In: Bautista M, Chavarín PC (eds) Producción de tomate de cáscara. Colegio de Postgraduados, Estado de México, pp 31–71
Peña A, Molina JD, Sahagún J et al (2008) Parámetros genéticos en la variedad CHF1 Chapingo de tomate de cáscara (Physalis ixocarpa Brot). Rev Chapingo Ser Hortic 14:5–11. https://doi.org/10.5154/r.rchsh.2006.11.046
Peña A, Magaña-Lira N, Hernández S et al (2011) Manual Gráfico para la descripción varietal de tomate de cáscara (Physalis ixocarpa Brot ex Horm). SNICS-SAGARPA Universidad Autónoma Chapingo, Mexico
Qiao J, Cai M, Yan G et al (2016) High-throughput multiplex cpDNA resequencing clarifies the genetic diversity and genetic relationships among Brassica napus Brassica rapa and Brassica oleracea. Plant Biotechnol J 14:409–418. https://doi.org/10.1111/pbi12395
Rogalski M, do Nascimento VL, Fraga HP et al (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
Rose AB (2008) Intron-mediated regulation of gene expression. In: Reddy SN, Golovkin M (eds) Nuclear pre-mRNA processing in plants. Springer, Berlin, Germany, pp 277–290
Sandoval-Padilla I, Pérez-Alquicira J, Zamora-Tavares MP et al (2019) Complete sequence of wild Physalis philadelphica chloroplast genome. Mitochond DNA B Res 4:3295–3297. https://doi.org/10.1080/23802359.2019.1673231
Schuster M, Gao Y, Schöttler MA et al (2020) Limited responsiveness of chloroplast gene expression during acclimation to high light in tobacco. Plant Physiol 182:424–435. https://doi.org/10.1104/pp19.00953
Shenstone E, Lippman Z, Van Eck J (2020) A review of nutritional properties and health benefits of Physalis species. Plant Foods Hum Nutr 75:316–325. https://doi.org/10.1007/s11130-020-00821-3
Shetty SM, Shah MUM, Makale K et al (2016) Complete chloroplast genome sequence of Musa balbisiana corroborates structural heterogeneity of inverted repeats in wild progenitors of cultivated bananas and plantains. Plant Genome 9:1–14. https://doi.org/10.3835/plantgenome2015.09.0089
Shi C, Hu N, Huang H et al (2012) An improved chloroplast DNA extraction procedure for whole plastid genome sequencing. PLoS ONE 7:e31468. https://doi.org/10.1371/journal.pone.0031468
Shi H, Yang M, Mo C et al (2019) Complete chloroplast genomes of two Siraitia Merrill species: Comparative analysis positive selection and novel molecular marker development. PLoS ONE 14:e0226865. https://doi.org/10.1371/journal.pone.0226865
Solís-Montero L, Aceves-Chong L, Vega-Polanco M et al (2021) Changes in reproductive traits in Physalis philadelphica; an unexpected shift toward self-incompatibility in a domesticated annual fruit crop. Front Plant Sci 12:658406. https://doi.org/10.3389/fpls.2021.658406
Solorzano S, Chincoya DA, Sanchez-Flores A et al (2019) De novo assembly discovered novel structures in genome of plastids and revealed divergent inverted repeats in Mammillaria (Cactaceae, Caryophyllales). Plants 8:392. https://doi.org/10.3390/plants8100392
Sugita M, Sugiura M (1996) Regulation of gene expression in chloroplasts of higher plants. Plant Mol Biol 32:315–326
Thorvaldsdóttir H, Robinson JT, Mesirov JP (2013) Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14:178–192. https://doi.org/10.1093/bib/bbs017
Tong W, Kim TS, Park YJ (2016) Rice chloroplast genome variation architecture and phylogenetic dissection in diverse Oryza species assessed by whole-genome resequencing. Rice (n Y) 9:57. https://doi.org/10.1186/s12284-016-0129-y
Valdivia-Mares LE, Rodríguez FA, Sánchez JJ, et al. (2016) Phenology agronomic and nutritional potential of three wild husk tomato species (Physalis Solanaceae) from Mexico. Sci Hortic 200:83–94. https://doi.org/10.1016/j.scienta.2016.01.005
Vargas-Ponce O, Sánchez-Martínez J, Zamora-Tavares MP et al (2016) Traditional management of a small-scale crop of Physalis angulata in Western Mexico. Genet Resour Crop Evol 63:1383–1395. https://doi.org/10.1007/s10722‐015‐0326‐3
Wang L, He L, Li J et al (2014) Regulatory change at Physalis Organ Size 1 correlates to natural variation in tomatillo reproductive organ size. Nat Commun 5:1–12. https://doi.org/10.1038/ncomms5271
Wang J, Li C, Yan C et al (2018) A comparative analysis of the complete chloroplast genome sequences of four peanut botanical varieties. PeerJ 6:e5349. https://doi.org/10.7717/peerj.5349
Whitson M, Manos PS (2005) Untangling Physalis (Solanaceae) from the Physaloids: a two-gene phylogeny of the Physalinae. Syst Bot 30:216–230. https://doi.org/10.1600/0363644053661841
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
Zamora-Tavares P, Vargas-Ponce O, Sánchez-Martínez J et al (2015) Diversity and genetic structure of the husk tomato (Physalis philadelphica Lam) in Western Mexico. Genet Resour Crop Evol 62:141–153. https://doi.org/10.1007/s10722-014-0163-9
Zamora-Tavares MP, Sandoval-Padilla I, Chávez A et al (2020) Complete chloroplast genome of Physalis chenopodifolia Lam (Solanaceae). Mitochond DNA B Res 5:162–163. https://doi.org/10.1080/23802359.2019.1698364
Zhao DN, Ren Y, Zhang JQ (2020) Conservation and innovation: plastome evolution during rapid radiation of Rhodiola on the Qinghai-Tibetan plateau. Mol Phylogenet Evol 144:106713. https://doi.org/10.1016/j.ympev.2019.106713
Zhou Q, Lin CW, Ng WL et al (2019) Analyses of plastome sequences improve phylogenetic resolution and provide new insight into the evolutionary history of asian Sonerileae/Dissochaeteae. Front Plant Sci 10:1477. https://doi.org/10.3389/fpls2019.01477
Zong D, Gan P, Zhang Y et al (2019) Plastome sequences help to resolve deep-level relationships of Populus in the family Salicaceae. Front Plant Sci 10:5. https://doi.org/10.3389/fpls.2019.00005
Acknowledgements
This work was supported by UDG and CONACyT-Laboratorio Nacional de Identificación y Caracterización Vegetal (LaniVeg) [Grant No. 293833], Universidad de Guadalajara [Grant Prosni-2018 to OVP] and CONACyT-México through a Masters scholarship for graduate studies in Maestría en Biosistemática y Manejo de Recursos Naturales y Agrícolas (BIMARENA) [Grant No. 928518 awarded to ISP].
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OVP, PZT and ISP conceived and designed the study. ISP, OVP, JPA and AR led the writing. ISP developed the molecular methods, sequencing libraries and bioinformatics analyses. MPZT supported the laboratory work and JPA advised on bioinformatics analysis. All authors reviewed drafts of the paper and approved the final manuscript.
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Sandoval-Padilla, I., Pérez-Alquicira, J., Rodríguez, A. et al. The plastome of the husk tomato (Physalis philadelphica Lam., Solanaceae): a comparative analysis between wild and cultivated pools. Genet Resour Crop Evol 69, 1391–1405 (2022). https://doi.org/10.1007/s10722-021-01334-x
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DOI: https://doi.org/10.1007/s10722-021-01334-x