The genus Camelina (Brassicaceae) comprises 7-8 diploid, tetraploid, and hexaploid species. Of particular agricultural interest is the biofuel crop, C. sativa (gold-of-pleasure or false flax), an allohexaploid domesticated from the widespread weed, C. microcarpa. Recent cytogenetics and genomics work has uncovered the identity of the parental diploid species involved in ancient polyploidization events in Camelina. However, little is known about the maternal subgenome ancestry of contemporary polyploid species. To determine the diploid maternal contributors of polyploid Camelina lineages, we sequenced and assembled 84 Camelina chloroplast genomes for phylogenetic analysis. Divergence time estimation was used to infer the timing of polyploidization events. Chromosome counts were also determined for 82 individuals to assess ploidy and cytotypic variation. Chloroplast genomes showed minimal divergence across the genus, with no observed gene-loss or structural variation. Phylogenetic analyses revealed C. hispida as a maternal diploid parent to the allotetraploid Camelina rumelica, and C. neglecta as the closest extant diploid contributor to the allohexaploids C. microcarpa and C. sativa. The tetraploid C. rumelica appears to have evolved through multiple independent hybridization events. Divergence times for polyploid lineages closely related to C. sativa were all inferred to be very recent, at only ~65 thousand years ago. Chromosome counts confirm that there are two distinct cytotypes within C. microcarpa (2n = 38 and 2n = 40). Based on these findings and other recent research, we propose a model of Camelina subgenome relationships representing our current understanding of the hybridization and polyploidization history of this recently-diverged genus.

CEITEC Central European Institute of Technology Masaryk University Kamenice 5 625 00 Brno Czech Republic

Department of Biological Sciences The University of Alabama 411 Mary Harmon Bryant Hall Tuscaloosa Alabama 35487 USA

Department of Biology Washington University in St Louis St Louis Missouri 63130 USA

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Nock CJ, Waters DLE, Edwards MAet al. . Chloroplast genome sequences from total DNA for plant identification. Plant Biotechnol J. 2011;9:328–33. PubMed

Li P, Zhang S, Li Fet al. . A phylogenetic analysis of chloroplast genomes elucidates the relationships of the six economically important brassica species comprising the triangle of U. Front Plant Sci. 2017;8:111. PubMed PMC

Allender CJ, King GJ. Origins of the amphiploid species Brassica napus L. investigated by chloroplast and nuclear molecular markers. BMC Plant Biol. 2010;10:54. PubMed PMC

Carreel F, Gonzalez de Leon D, Logada Pet al. . Ascertaining maternal and paternal lineage within Musa by chloroplast and mitochondrial DNA RFLP analyses. Genome. 2002;45:679–92. PubMed

Middleton CP, Senerchia N, Stein Net al. . Sequencing of chloroplast genomes from wheat, barley, rye and their relatives provides a detailed insight into the evolution of the Triticeae tribe. PLoS One. 2014;9:e85761. PubMed PMC

Wendel JF. New World tetraploid cottons contain Old World cytoplasm. Proc Natl Acad Sci. 1989;86:4132–6. PubMed PMC

Carbonell-Caballero J, Alonso R, Ibañez Vet al. . A phylogenetic analysis of 34 chloroplast genomes elucidates the relationships between wild and domestic species within the genus citrus. Mol Biol Evol. 2015;32:2015–35. PubMed PMC

Nikiforova SV, Cavalieri D, Velasco Ret al. . Phylogenetic analysis of 47 chloroplast genomes clarifies the contribution of wild species to the domesticated apple maternal line. Mol Biol Evol. 2013;30:1751–60. PubMed

Ceplitis A, Su Y, Lascoux M. Bayesian inference of evolutionary history from chloroplast microsatellites in the cosmopolitan weed Capsella bursa-pastoris (Brassicaceae). Mol Ecol. 2005;14:4221–33. PubMed

Gutiérrez-Rodríguez C, Ornelas JF, Rodríguez-Gómez F. Chloroplast DNA phylogeography of a distylous shrub (Palicourea padifolia, Rubiaceae) reveals past fragmentation and demographic expansion in Mexican cloud forests. Mol Phylogenet Evol. 2011;61:603–15. PubMed

Saeidi S, McKain MR, Kellogg EA. Robust DNA isolation and high-throughput sequencing library construction for herbarium specimens. JoVE. J Vis Exp. 2018;e56837. 10.3791/56837. PubMed DOI PMC

Brock JR, Mandáková T, Lysak MAet al. . Camelina neglecta (Brassicaceae, Camelineae), a new diploid species from Europe. PhytoKeys. 2019;115:51–7. PubMed PMC

Al-Shehbaz I, Beilstein M. Camelina Flora N Am Editor Comm. 2010;7:451–3.

Mandáková T, Pouch M, Brock JRet al. . Origin and evolution of diploid and allopolyploid Camelina genomes were accompanied by chromosome shattering. Plant Cell. 2019;31:2596–612. PubMed PMC

Žerdoner Čalasan A, Seregin AP, Hurka Het al. . The Eurasian steppe belt in time and space: phylogeny and historical biogeography of the false flax (Camelina Crantz, Camelineae, Brassicaceae). Flora. 2019;260:151477.

Ghamkhar KG, Croser J, Aryamanesh Net al. . Camelina (Camelina sativa (L.) Crantz) as an alternative oilseed: molecular and ecogeographic analyses. Genome. 2010. 10.1139/G10-034. PubMed DOI

Vollmann J, Grausgruber H, Stift Get al. . Genetic diversity in camelina germplasm as revealed by seed quality characteristics and RAPD polymorphism. Plant Breed. 2005;124:446–53.

Singh R, Bollina V, Higgins EEet al. . Single-nucleotide polymorphism identification and genotyping in Camelina sativa. Mol Breed. 2015;35:35. PubMed PMC

Luo Z, Brock J, Dyer JMet al. . Genetic diversity and population structure of a Camelina sativa spring panel. Front Plant Sci. 2019;10:184. PubMed PMC

Chaudhary R, Koh CS, Kagale Set al. . Assessing diversity in the Camelina genus provides insights into the genome structure of Camelina sativa. G3 (Bethesda). 2020;10:1297–308. PubMed PMC

Berti M, Gesch R, Eynck Cet al. . Camelina uses, genetics, genomics, production, and management. Industrial Crops and Products. 2016;94:690–710.

Gugel RK, Falk KC. Agronomic and seed quality evaluation of Camelina sativa in western Canada. Can J Plant Sci. 2006;86:1047–58.

Zubr J. Oil-seed crop: Camelina sativa. Ind Crops Prod. 1997;6:113–9.

Shonnard DR, Williams L, Kalnes TN. Camelina-derived jet fuel and diesel: sustainable advanced biofuels. Environ Prog Sustain Energy. 2010;29:382–92.

Martin SL, Lujan-Toro BE, Sauder CAet al. . Hybridization rate and hybrid fitness for Camelina microcarpa Andrz. Ex DC (♀) and Camelina sativa (L.) Crantz(Brassicaceae) (♂). Evol Appl. 2019;12:443–55. PubMed PMC

Séguin-Swartz G, Nettleton JA, Sauder Cet al. . Hybridization between Camelina sativa (L.) Crantz (false flax) and north American Camelina species. Plant Breed. 2013;132:390–6.

Zhang C-J, Auer C. Hybridization between Camelina sativa (L.) Crantz and common brassica weeds. Ind Crops Prod. 2020;147:112240.

Becker HC, Engqvist GM, Karlsson B. Comparison of rapeseed cultivars and resynthesized lines based on allozyme and RFLP markers. Theor Appl Genet. 1995;91:62–7. PubMed

Girke A, Schierholt A, Becker HC. Extending the rapeseed genepool with resynthesized Brassica napus L. I: genetic diversity. Genet Resour Crop Evol. 2012;59:1441–7.

Mandáková T, Lysak MA. Post-polyploid diploidization and diversification through dysploid changes. Curr Opin Plant Biol. 2018;42:55–65. PubMed

Brock JR, Scott T, Lee AYet al. . Interactions between genetics and environment shape Camelina seed oil composition. BMC Plant Biol. 2020;20:423. PubMed PMC

Guo X, Liu J, Hao Get al. . Plastome phylogeny and early diversification of Brassicaceae. BMC Genomics. 2017;18:176. PubMed PMC

Martin SL, Smith TW, James Tet al. . An update to the Canadian range, abundance, and ploidy of Camelina spp. (Brassicaceae) east of the Rocky Mountains. Botany. 2017;95:405–17.

Tepfer M, Hurel A, Tellier Fet al. . Evaluation of the progeny produced by interspecific hybridization between Camelina sativa and C. microcarpa. Ann Bot. 2020;125:993–1002. PubMed PMC

Mirek Z. Monographic studies in genus Camelina Cr. 1. Camelina anomala Boiss. Et Hausskn. Acta Soc. Acta Soc Bot Pol Pol Tow Bot. 2014;53:429–32.

Brock JR, Dönmez AA, Beilstein MAet al. . Phylogenetics of Camelina Crantz. (Brassicaceae) and insights on the origin of gold-of-pleasure (Camelina sativa). Mol Phylogenet Evol. 2018;127:834–42. PubMed

Dillenberger MS, Wei N, Tennessen JAet al. . Plastid genomes reveal recurrent formation of allopolyploid Fragaria. Am J Bot. 2018;105:862–74. PubMed

Soltis DE, Soltis PS. Polyploidy: recurrent formation and genome evolution. Trends Ecol Evol. 1999;14:348–52. PubMed

Hohmann N, Wolf EM, Lysak MAet al. . A time-calibrated road map of Brassicaceae species radiation and evolutionary history. Plant Cell. 2015;27:2770–84. PubMed PMC

Edger PP, McKain MR, Bird KAet al. . Subgenome assignment in allopolyploids: challenges and future directions. Curr Opin Plant Biol. 2018;42:76–80. PubMed

Mosyakin SL, Brock JR. On the proper type designation for Camelina microcarpa, a wild relative and possible progenitor of the crop species C. sativa (Brassicaceae). Candollea. 2021;76:55–63.

Jin JJ, Yu WB, Yang JBet al. . GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol. 2020;21:241. PubMed PMC

Wick RR, Schultz MB, Zobel Jet al. . Bandage: interactive visualization of de novo genome assemblies. Bioinformatics. 2015;31:3350–2. PubMed PMC

Shi L, Chen H, Jiang Met al. . CPGAVAS2, an integrated plastome sequence annotator and analyzer. Nucleic Acids Res. 2019;47:W65–73. PubMed PMC

Lohse M, Drechsel O, Bock R. OrganellarGenomeDRAW (OGDRAW): a tool for the easy generation of high-quality custom graphical maps of plastid and mitochondrial genomes. Curr Genet. 2007;52:267–74. PubMed

Amiryousefi A, Hyvönen J, Poczai P. IRscope: an online program to visualize the junction sites of chloroplast genomes. Bioinformatics. 2018;34:3030–1. PubMed

Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80. PubMed PMC

Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540–52. PubMed

Darriba D, Taboada GL, Doallo Ret al. . jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9:772–2. PubMed PMC

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–3. PubMed PMC

Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JCet al. . DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol. 2017;34:3299–302. PubMed

Leigh JW, Bryant D. Popart: full-feature software for haplotype network construction. Methods Ecol Evol. 2015;6:1110–6.

Clement, M., Snell, Q., Walke, P.et al. . TCS: estimating gene genealogies. in Proceedings 16th International Parallel and Distributed Processing Symposium 7 pp ( IEEE, 2002). 10.1109/IPDPS.2002.1016585. DOI

Bouckaert R, Heled J, Kuhnert Det al. . BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol. 2014;10:e1003537. PubMed PMC

Novikova PY, Hohmann N, Nizhynska Vet al. . Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism. Nat Genet. 2016;48:1077–82. PubMed

Team, R. C . othersR: A language and environment for statistical computing. In: 2013.

Heibl C. PHYLOCH: R Language Tree Plotting Tools and Interfaces to Diverse Phylogenetic Software Packages. 2008.

The evolution of the hypotetraploid Catolobus pendulus genome - the poorly known sister species of Capsella