Chloroplast phylogenomics in Camelina (Brassicaceae) reveals multiple origins of polyploid species and the maternal lineage of C. sativa

Jordan R. Brock , Terezie Mandáková , Michael McKain , Martin A. Lysak , Kenneth M. Olsen

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhab050

PDF (477KB)
Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhab050 DOI: 10.1093/hr/uhab050
Article
research-article
Chloroplast phylogenomics in Camelina (Brassicaceae) reveals multiple origins of polyploid species and the maternal lineage of C. sativa
Author information +
History +
PDF (477KB)

Abstract

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.

Cite this article

Download citation ▾
Jordan R. Brock, Terezie Mandáková, Michael McKain, Martin A. Lysak, Kenneth M. Olsen. Chloroplast phylogenomics in Camelina (Brassicaceae) reveals multiple origins of polyploid species and the maternal lineage of C. sativa. Horticulture Research, 2022, 9 (1) : uhab050 DOI:10.1093/hr/uhab050

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

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

[2]

Li P, Zhang S, Li F et 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.

[3]

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.

[4]

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

[5]

Middleton CP, Senerchia N, Stein N et 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.

[6]

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

[7]

Carbonell-Caballero J, Alonso R, Ibañez V et 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.

[8]

Nikiforova SV, Cavalieri D, Velasco R et 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.

[9]

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.

[10]

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.

[11]

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

[12]

Brock JR, Mandáková T, Lysak MA et al. Camelina neglecta (Brassicaceae, Camelineae), a new diploid species from Europe. PhytoKeys. 2019; 115: 51-7.

[13]

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

[14]

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

[15]

Žerdoner Čalasan A, Seregin AP, Hurka H et 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.

[16]

Ghamkhar KG, Croser J, Aryamanesh N et al. Camelina (Camelina sativa (L.) Crantz) as an alternative oilseed: molecular and ecogeographic analyses. Genome. 2010. https://doi.org/10.1139/G10-034.

[17]

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

[18]

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

[19]

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

[20]

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

[21]

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

[22]

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

[23]

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

[24]

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

[25]

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

[26]

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

[27]

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

[28]

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.

[29]

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.

[30]

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

[31]

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

[32]

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

[33]

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

[34]

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

[35]

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.

[36]

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

[37]

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

[38]

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

[39]

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

[40]

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

[41]

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.

[42]

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

[43]

Wick RR, Schultz MB, Zobel J et al. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics. 2015; 31: 3350-2.

[44]

Shi L, Chen H, Jiang M et al. CPGAVAS2, an integrated plastome sequence annotator and analyzer. Nucleic Acids Res. 2019; 47: W65-73.

[45]

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.

[46]

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

[47]

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

[48]

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

[49]

Darriba D, Taboada GL, Doallo R et al. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012; 9: 772-2.

[50]

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

[51]

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

[52]

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

[53]

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). https://doi.org/10.1109/IPDPS.2002.1016585.

[54]

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

[55]

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

[56]

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

[57]

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

PDF (477KB)

34

Accesses

0

Citation

Detail

Sections
Recommended

/