Abstract
The pantropical Caesalpinia group includes 225 species in 27 monophyletic genera, and the group has undergone recent phylogenetic, taxonomic and biogeographic revisions. Previous works have reported a diverse pattern of heterochromatin distribution related to ecological niche/geographic distribution, and variation in genome size also correlated with environmental variables. In order to investigate the relationship between cytogenetic and ecological traits using the Caesalpinia group as a model, new cytomolecular data (chromosome number and morphology, CMA/DAPI staining and number and position of 5S and 35S rDNA sites) for 14 species in six genera were generated. These data were analysed by phylogenetic comparative methods. All species studied have 2n = 24 (16 M/SM + 8A), and most of them just have one pair of 5S rDNA sites and two to five pairs of 35S rDNA sites. Three heterochromatic patterns were observed on the chromosomes: (i) proximal CMA+/DAPI− bands, (ii) proximal CMA0/DAPI− bands and (iii) proximal CMA0/DAPI0 bands. The “Coulteria + Tara” and “Arquita + Balsamocarpon + Erythrostemon + Pomaria” clades (except for E. gilliesii, E. hughesii and E. mexicanus) independently showed CMA0/DAPI− bands associated with larger genomes and geographic distributions at higher latitudes. We statistically demonstrate that heterochromatin (CMA/DAPI intensity along the chromosome), genome size and latitude are autocorrelated in the Caesalpinia group. On the other hand, we found a non-significant correlation between genome size and amount of heterochromatin. We argue that environmental factors associated with different latitude may have played a role in contributing to the diversification of the heterochromatin in Caesalpinia group.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Acosta MC, Moscone EA, Cocucci AA (2016) Using chromosomal data in the phylogenetic and molecular dating framework: karyotype evolution and diversification in Nierembergia (Solanaceae) influenced by historical changes in sea level. Pl Biol 18:514–526. https://doi.org/10.1111/plb.12430
Alkhimova OG, Mazurok NA, Potapova TA, Zakian SM, Heslop-Harrison JS, Vershinin AV (2004) Diverse patterns of the tandem repeats organization in rye chromosomes. Chromosoma 113:42–52. https://doi.org/10.1007/s00412-004-0294-4
Ambrožová K, Mandáková T, Bureš P, Neumann P, Leitch IJ, Koblížková A, Lysak MA (2011) Diverse retrotransposon families and an AT-rich satellite DNA revealed in giant genomes of Fritillaria lilies. Ann Bot (Oxford) 107:255–268. https://doi.org/10.1093/aob/mcq235
Beltrão GTA, Guerra M (1990) Citogenética de angiospermas coletadas em Pernambuco-III. Ci Cult 42:839–845
Bennetzen JL, Wang H (2014) The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annual Rev Pl Biol 65:505–530. https://doi.org/10.1146/annurev-arplant-050213-035811
Berjano R, Roa F, Talavera S, Guerra M (2009) Cytotaxonomy of diploid and polyploid (Aristolochiaceae) species based on the distribution of CMA/DAPI bands and 5S and 45S rDNA sites. Pl Syst Evol 280:219–227. https://doi.org/10.1007/s00606-009-0184-6
Bilinski P, Albert PS, Berg JJ, Birchler J, Grote M, Lorant A, Quezada J, Swarts K, Yang J, Ross-Ibarra J (2017) Parallel altitudinal clines reveal adaptive evolution of genome size in Zea mays. PLoS Genet 14:e1007162. https://doi.org/10.1101/134528
Borges LA, Souza LGR, Guerra M, Machado IC, Lewis GP, Lopes AV (2012) Reproductive isolation between diploid and tetraploid cytotypes of Libidibia ferrea (= Caesalpinia ferrea) (Leguminosae): ecological and taxonomic implications. Pl Syst Evol 298:1371–1381. https://doi.org/10.1007/s00606-012-0643-3
Castañeda R, Gutiérrez H, Carrillo É, Sotelo A (2017) Leguminosas (Fabaceae) silvestres de uso medicinal del distrito de Lircay, provincia de Angaraes (Huancavelica, Perú). Bol Latinoamer Caribe Pl 16:136–149
Cavalier-Smith T (2005) Economy, speed and size matter: evolutionary forces driving nuclear genome miniaturization and expansion. Ann Bot (Oxford) 95:147–175. https://doi.org/10.1093/aob/mci010
Chiarini F, Sazatornil F, Bernardello G (2018) Data reassessment in a phylogenetic context gives insight into chromosome evolution in the giant genus Solanum (Solanaceae). Syst Biodivers 16:397–416. https://doi.org/10.1080/14772000.2018.1431320
Costa L, Oliveira Á, Carvalho-Sobrinho J, Souza G (2017) Comparative cytomolecular analyses reveal karyotype variability related to biogeographic and species richness patterns in Bombacoideae (Malvaceae). Pl Syst Evol 303:1131–1144. https://doi.org/10.1007/s00606-017-1427-6
Dryflor et al (2016) Plant diversity patterns in neotropical dry forests and their conservation implications. Science 353:1383–1387. https://doi.org/10.1126/science.aaf5080
Felsenstein J (1985) Phylogenies and the comparative method. Amer Naturalist 125:1–15
Gaeta ML, Yuyama PM, Sartori D, Fungaro MHP, Vanzela ALL (2010) Occurrence and chromosome distribution of retroelements and NUPT sequences in Copaifera langsdorffii Desf. (Caesalpinioideae). Chromosome Res 18:515–524. https://doi.org/10.1007/s10577-010-9131-1
Gagnon E, Lewis GP, Sotuyo JS, Hughes CE, Bruneau A (2013) A molecular phylogeny of Caesalpinia sensu lato: increased sampling reveals new insights and more genera than expected. S African J Bot 89:111–127. https://doi.org/10.1016/j.sajb.2013.07.027
Gagnon E, Hughes CE, Lewis GP, Bruneau A (2015) A new cryptic species in a new cryptic genus in the Caesalpinia group (Leguminosae) from the seasonally dry inter Andean valleys of South America. Taxon 64:468–490. https://doi.org/10.12705/643.6
Gagnon E, Bruneau A, Hughes CE, Queiroz LP de, Lewis GP (2016) A new generic system for the pantropical Caesalpinia group (Leguminosae). PhytoKeys 71:1–160. https://doi.org/10.3897/phytokeys.71.9203
Gagnon E, Ringelberg JJ, Bruneau A, Lewis GP, Hughes CE (2019) Global Succulent Biome phylogenetic conservatism across the pantropical Caesalpinia Group (Leguminosae). New Phytologist 222:1994–2008. https://doi.org/10.1111/nph.15633
Gasson P, Warner K, Lewis G (2009) Wood anatomy of Caesalpinia ss, Coulteria, Erythrostemon, Guilandina, Libidibia, Mezoneuron, Poincianella, Pomaria and Tara (Leguminosae, Caesalpinioideae, Caesalpinieae). IAWA J 30:247–276. https://doi.org/10.1163/22941932-90000218
Guerra MS (1986) Reviewing the chromosome nomenclature of Levan. Brazil J Genet 9:741–743
Guerra M (2000) Patterns of heterochromatin distribution in plant chromosomes. Genet Molec Biol 23:1029–1041. https://doi.org/10.1590/S1415-47572000000400049
Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology, vol. 239. Oxford University Press, Oxford
Hijmans RJ, Cameron SE, Parra JL (2005) Worldclim global climate layers Version 1.4. Available at: http://www.worldclim.org. Accessed Jul 2008
Hijmans RJ, van Etten J, Cheng J, Mattiuzzi M, Sumner M, Greenberg JA, Ghosh A (2017) raster: Geographic Data Analysis and Modeling. R package version 2.6-7
Kassambara A, Mundt F (2017) Factoextra: Extract and visualize the results of multivariate data analyses. R package version 1.0.5. Available at: https://CRAN.R-project.org/package=factoextra
Kirov I, Khrustaleva L, Van Laere K, Soloviev A, Meeus S, Romanov D, Fesenko I (2017) DRAWID: user-friendly java software for chromosome measurements and idiogram drawing. Comp Cytogenet 11:747–757. https://doi.org/10.3897/CompCytogen.v11i4.20830
Kolano B, McCann J, Orzechowska M, Siwinska D, Temsch E, Weiss-Schneeweiss H (2016) Molecular and cytogenetic evidence for an allotetraploid origin of Chenopodium quinoa and C. berlandieri (Amaranthaceae). Molec Phylogen Evol 100:109–123. https://doi.org/10.1016/j.ympev.2016.04.009
Lee YI, Yap JW, Izan S, Leitch IJ, Fay MF, Lee YC, Leitch AR (2018) Satellite DNA in Paphiopedilum subgenus Parvisepalum as revealed by high-throughput sequencing and fluorescent in situ hybridization. BMC Genomics 19:578. https://doi.org/10.1186/s12864-018-4956-7
Leemann U, Ruch F (1982) Cytofluorometric determination of DNA base content in plant nuclei and chromosomes by the fluorochromes DAPI and Cromomicyn A3. Exp Cell Res 140:275–282. https://doi.org/10.1016/0014-4827(82)90115-X
Macas J, Novák P, Pellicer J, Čížková J, Koblížková A, Neumann P, Fuková I, Doležel J, Kelly LJ, Leitch IJ (2015) In depth characterization of repetitive DNA in 23 plant genomes reveals sources of genome size variation in the legume tribe Fabeae. PLoS ONE 10:e0143424. https://doi.org/10.1371/journal.pone.0143424
Manzanilla V, Bruneau A (2012) Phylogeny reconstruction in the Caesalpinieae grade (Leguminosae) based on duplicated copies of the sucrose synthase gene and plastid markers. Molec Phylogen Evol 65:149–162. https://doi.org/10.1016/j.ympev.2012.05.035
Menezes RS, Brady SG, Carvalho AF, Del Lama MA, Costa MA (2017) The roles of barriers, refugia, and chromosomal clines underlying diversification in Atlantic Forest social wasps. Sci Rep 7:7689. https://doi.org/10.1038/s41598-017-07776-7
Moreno N, Amarilla L, Las Peñas M, Bernardello G (2015) Molecular cytogenetic insights into the evolution of the epiphytic genus Lepismium (Cactaceae) and related genera. Bot J Linn Soc 177:263–277. https://doi.org/10.1111/boj.12242
Moreno NC, Stiefkens L, Las Peñas ML, Bartoli A, Tortosa R, Bernardello G (2018) Karyotypes, heterochromatin distribution and rDNA patterns in South American Grindelia (Asteraceae). Pl Biosyst 152:166–174. https://doi.org/10.1080/11263504.2016.1265611
Paradis E, Bolker B, Claude J (2012) Package ape. Analyses of phylogenetics and evolution. R package version 2012, 04–04. Available at: https://cran.r-project.org/web/packages/ape/ape.pdf
Pellicer J, Hidalgo O, Dodsworth S, Leitch IJ (2018) Genome size diversity and its impact on the evolution of land plants. Genes 9:88. https://doi.org/10.3390/genes9020088
Pedrosa A, Sandal N, Stougaard J, Schweizer D, Bachmair A (2002) Chromosomal map of the model legume Lotus japonicus. Genetics 161:1661–1672
Plohl M, Luchetti A, Meštrović N, Mantovani B (2008) Satellite DNAs between selfishness and functionality: structure, genomics and evolution of tandem repeats in centromeric (hetero) chromatin. Gene 409:72–82. https://doi.org/10.1016/j.gene.2007.11.013
Purvis A, Rambaut A (1995) Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Bioinformatics 11:247–251
Puttick MN, Clark J (2015) Donoghue PC (2015) Size is not everything: rates of genome size evolution, not C-value, correlate with speciation in angiosperms. Proc Roy Soc B Biol Sci 282:20152289. https://doi.org/10.1098/rspb.2015.2289
R Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at: http://www.R-project.org
Ribeiro T, Marques A, Novák P, Schubert V, Vanzela AL, Macas J, Pedrosa-Harand A (2017) Centromeric and non-centromeric satellite DNA organisation differs in holocentric Rhynchospora species. Chromosoma 126:325–335. https://doi.org/10.1007/s00412-016-0616-3
Ribeiro T, Buddenhagen CE, Thomas WW, Souza G, Pedrosa-Harand A (2018) Are holocentrics doomed to change? Limited chromosome number variation in Rhynchospora Vahl (Cyperaceae). Protoplasma 255:263–272. https://doi.org/10.1007/s00709-017-1154-4
Rodrigues PS, Souza MM, Corrêa RX (2014) Karyomorphology and karyotype asymmetry in the South American Caesalpinia species (Leguminosae:Caesalpinioideae). Genet Molec Biol 13:8278–8293. https://doi.org/10.4238/2014.October.20.4
Rodrigues PS, Souza MM, Melo CAF, Pereira TNS, Corrêa RX (2018) Karyotype diversity and 2C DNA content in species of the Caesalpinia group. BMC Genet 19:25. https://doi.org/10.1186/s12863-018-0610-2
Ruban A, Fuchs J, Marques A, Schubert V, Soloviev A, Raskina O, Houben A (2014) B chromosomes of Aegilops speltoides are enriched in organelle genome–derived sequences. PLoS ONE 9:e90214. https://doi.org/10.1371/journal.pone.0090214
Sader MA, Amorim BS, Costa L, Souza G, Pedrosa-Harand A (2019) The role of chromosome changes in the diversification of Passiflora L. (Passifloraceae). Syst Biodivers 1:1–15. https://doi.org/10.1080/14772000.2018.1546777
Salim D, Gerton JL (2019) Ribosomal DNA instability and genome adaptability. Chromosome Res 27:73–87. https://doi.org/10.1007/s10577-018-9599-7
Schwarzacher T, Schweizer D (1982) Karyotype analysis and heterochromatin differentiation with Giemsa C-banding and fluorescent counterstaining in Cephalanthera (Orchidaceae). Pl Syst Evol 141:91–113
Schweizer D (1976) Reverse fluorescent chromosome banding with chromomycin and DAPI. Chromosoma 58:307–324
Seijo JG, Lavia GI, Fernández A, Krapovickas A, Ducasse D, Moscone EA (2004) Physical mapping of the 5S and 18S–25S rRNA genes by FISH as evidence that Arachis duranensis and A. ipaensis are the wild diploid progenitors of A. hypogaea (Leguminosae). Amer J Bot 91:1294–1303. https://doi.org/10.3732/ajb.91.9.1294
Siljak-Yakovlev S, Godelle B, Zoldos V, Vallès J, Garnatje T, Hidalgo O (2017) Evolutionary implications of heterochromatin and rDNA in chromosome number and genome size changes during dysploidy: a case study in Reichardia genus. PLoS ONE 12:e0182318. https://doi.org/10.1371/journal.pone.0182318
Silvestri MC, Ortiz AM, Lavia GI (2015) rDNA loci and heterochromatin positions support a distinct genome type for ‘x= 9 species’ of section Arachis (Leguminosae). Pl Syst Evol 301:555–562. https://doi.org/10.1007/s00606-014-1092-y
Soetaert K (2014) plot3D: Tools for plotting 3-D and 2-D data. R package version, 10–2.
Souza G, Costa L, Guignard MS, Van-Lume B, Pellicer J, Gagnon E, Lewis GP (2019) Do tropical plants have smaller genomes? Correlation between genome size and climatic variables in the Caesalpinia Group (Caesalpinioideae, Leguminosae). Perspect Pl Ecol 38:13–23. https://doi.org/10.1016/j.ppees.2019.03.002
Vaio M, Nascimento J, Mendes S, Ibiapino A, Felix LP, Gardner A, Emshwiller E, Fiaschi P, Guerra M (2018) Multiple karyotype changes distinguish two closely related species of Oxalis (O. psoraleoides and O. rhombeo-ovata) and suggest an artificial grouping of section Polymorphae (Oxalidaceae). Bot J Linn Soc 188:269–280. https://doi.org/10.1093/botlinnean/boy054
Van-Lume B, Souza G (2018) Cytomolecular analysis of species in the Peltophorum clade (Caesalpinioideae, Leguminosae). Brazilian J Bot 41:385–392. https://doi.org/10.1007/s40415-018-0449-9
Van-Lume B, Esposito T, Diniz-filho J, Gagnon E, Lewis G (2017) Souza G (2017) Heterochromatic and cytomolecular diversification in the Caesalpinia group (Leguminosae): relationships between phylogenetic and cytogeographical data. Perspect Pl Ecol 29:51–63. https://doi.org/10.1016/j.ppees.2017.11.004
Van-Lume B, Mata-Sucre Y, Báez M, Ribeiro T, Huettel B, Gagnon E, Leitch IJ, Pedrosa-Harand A, Lewis GP, Souza G (2019) Evolutionary convergence or homology? Comparative cytogenomics of Caesalpinia group species (Leguminosae) reveals diversification in the pericentromeric heterochromatic composition. Planta 250:2173–2186. https://doi.org/10.1007/s00425-019-03287-z
Acknowledgements
The authors wish to thank the Brazilian agencies Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Ciência e Tecnologia de Pernambuco (FACEPE—APQ-0970-2.03/15) for financial support and a post-doc grant to G.S. by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES—Estágio Pós-Doutoral 88881.119479/2016–01). This study was partly financed by the CAPES (finance Code 001). G.S. receives a productivity fellowship from CNPq (process number PQ—310693/2018–7).
Author information
Authors and Affiliations
Contributions
YMS conducted the experiments and wrote the manuscript. LC contributed in bioinformatics analyses and manuscript revisions. EG, GPL and IJL provided the plant material, contributed to critical discussions, manuscript revisions and the correction of the English. GS conceived and designed the research, contributed to critical discussions and manuscript revisions.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Handling Editor: Jorg Fuchs.
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.
Information on Electronic Supplementary Material
Information on Electronic Supplementary Material
Online Resource 1. List of analysed species describing their chromosome number (CP), chromosome length (CL), standard deviation (SD), the ratio of chromosome arms (AR) and the CMA/DAPI intensity index (CDI index)
Online Resource 2. Scatterplots of independent contrasts between genome size and heterochromatin proportion in clade I (a), clade II (b) and the Caesalpinia group (c). Phylogeny includes species characterized in this study (black) and those obtained from Van-Lume et al. (2017) (grey).
Rights and permissions
About this article
Cite this article
Mata-Sucre, Y., Costa, L., Gagnon, E. et al. Revisiting the cytomolecular evolution of the Caesalpinia group (Leguminosae): a broad sampling reveals new correlations between cytogenetic and environmental variables. Plant Syst Evol 306, 48 (2020). https://doi.org/10.1007/s00606-020-01674-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00606-020-01674-8