Gene count from target sequence capture places three whole genome duplication events in Hibiscus L. (Malvaceae)
Tóm tắt
The great diversity in plant genome size and chromosome number is partly due to polyploidization (i.e. genome doubling events). The differences in genome size and chromosome number among diploid plant species can be a window into the intriguing phenomenon of past genome doubling that may be obscured through time by the process of diploidization. The genus Hibiscus L. (Malvaceae) has a wide diversity of chromosome numbers and a complex genomic history. Hibiscus is ideal for exploring past genomic events because although two ancient genome duplication events have been identified, more are likely to be found due to its diversity of chromosome numbers. To reappraise the history of whole-genome duplication events in Hibiscus, we tested three alternative scenarios describing different polyploidization events. Using target sequence capture, we designed a new probe set for Hibiscus and generated 87 orthologous genes from four diploid species. We detected paralogues in > 54% putative single-copy genes. 34 of these genes were selected for testing three different genome duplication scenarios using gene counting. All species of Hibiscus sampled shared one genome duplication with H. syriacus, and one whole genome duplication occurred along the branch leading to H. syriacus. Here, we corroborated the independent genome doubling previously found in the lineage leading to H. syriacus and a shared genome doubling of this lineage and the remainder of Hibiscus. Additionally, we found a previously undiscovered genome duplication shared by the /Pavonia and /Malvaviscus clades (both nested within Hibiscus) with the occurrences of two copies in what were otherwise single-copy genes. Our results highlight the complexity of genomic diversity in some plant groups, which makes orthology assessment and accurate phylogenomic inference difficult.
Tài liệu tham khảo
Bates DM. Generic relationships in the Malvaceae, Tribe Malvaea. Gentes Herb. 1969;10:117–35.
Bates DM, Blanchard OJ Jr. Chromosome numbers in the Malvales. II. New or otherwise noteworthy counts relevant to classification in the Malvaceae, tribe Malveae. Am J Bot. 57(8):927.
Baum DA, DeWitt Smith S, Yen A, Alverson WS, Nyffeler R, et al. Phylogenetic relationships of Malvatheca (Bombacoideae and Malvoideae; Malvaceae sensu lato) as inferred from plastid DNA sequences. Am J Bot. 2004;91:1863–71.
Blanc G, Wolfe KH. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell. 2004;16:1667–78.
Borrill P, Adamski N, Uauy C. Genomics as the key to unlocking the polyploid potential of wheat. New Phytol. 2015;208:1008–22.
Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C-H, et al. BEAST 2: a software platform for Bayesian evolutionary analysis. J PLoS Comput Biol. 2014;10:e1003537.
Browning SR, Browning BL. Haplotype phasing: existing methods and new developments. Nat Rev Genet. 2011;12:703.
Buggs RJ, Renny-Byfield S, Chester M, Jordon-Thaden IE, Viccini LF, et al. Next-generation sequencing and genome evolution in allopolyploids. Am J Bot. 2012;99:372–82.
Cannon SB, Sterck L, Rombauts S, Sato S, Cheung F, et al. Legume genome evolution viewed through the Medicago truncatula and Lotus japonicus genomes. Proc Natl Acad Sci USA. 2006;103:14959–64.
Dasgupta A. Cytotaxonomy of Malvaceae II. Cytologia. 1981;46:149–60.
Davie JH. Cytological studies in the Malvaceae and certain related families. J Genet. 1933;28:33–67.
Drummond AJ, Ho SYW, Phillips MJ, Rambaut A, Penny D. Relaxed phylogenetics and dating with confidence. J PLoS Biol. 2006;4(5):e88.
Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29:1969–73.
Eriksson JS, Blanco-Pastor JL, Sousa F, Bertrand YJK, Pfeil BE. A cryptic species produced by autopolyploidy and subsequent introgression involving Medicago prostrata (Fabaceae). Mol Phylogenet Evol. 2017;107:367–81.
Fawcett JA, Maere S, Van de Peer Y. Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proc Natl Acad Sci USA. 2009;106:5737–42.
Fernández A, Krapovickas A, Lavia G, Seijo G. Cromosomas de Malváceas. Bonplandia. 2003;12(1/4):141–145. http://www.jstor.org/stable/41941249. Accessed 9 Feb 2021.
Fryxell PA. Pavonia Cavanilles (Malvaceae). Flora Neotropica Monograph. 1999;76:1–284. http://www.jstor.org/stable/4393884. Accessed 9 Feb 2021.
Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 2012;28:3150–2.
Grant V. Plant speciation. New York: Columbia University Press; 1981.
Gregg WT, Ather SH, Hahn WM. Gene-tree reconciliation with MUL-trees to resolve polyploidy events. Syst Biol. 2017;66:1007–18.
Huelsenbeck JP, Larget B, Alfaro ME. Bayesian phylogenetic model selection using reversible jump Markov chain Monte Carlo. Mol Biol Evol. 2004;21:1123–33.
Jaillon O, Aury J-M, Noel B, Policriti A, Clepet C, et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature. 2007;449:463.
Jiao Y, Leebens-Mack J, Ayyampalayam S, Bowers JE, McKain MR, et al. A genome triplication associated with early diversification of the core eudicots. Genome Biol. 2012;13:R3.
Johnson MT, Carpenter EJ, Tian Z, Bruskiewich R, Burris JN, et al. Evaluating methods for isolating total RNA and predicting the success of sequencing phylogenetically diverse plant transcriptomes. PLoS ONE. 2012;7:e50226.
Kates HR, Johnson MG, Gardner EM, Zerega NJC, Wickett NJ. Allele phasing has minimal impact on phylogenetic reconstruction from targeted nuclear gene sequences in a case study of Artocarpus. Am J Bot 2018;105(3):404–16.
Katoh K, Misawa K, Kuma KI, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. J Nucleic Acids Res. 2002;30:3059–66.
Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80.
Kay KM, Whittall JB, Hodges SA. A survey of nuclear ribosomal internal transcribed spacer substitution rates across angiosperms: an approximate molecular clock with life history effects. BMC Evol Biol. 2006;6:36.
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–9.
Kim Y, Kim S, Koo N, Shin A, Yeom S, et al. Genome analysis of Hibiscus syriacus provides insights of polyploidization and indeterminate flowering in woody plants. DNA Res. 2017;24:71–80.
Koopman MM, Baum DA. Phylogeny and biogeography of tribe Hibisceae (Malvaceae) on Madagascar. Syst Bot. 2008;33:364–74.
Landis JB, Soltis DE, Li Z, Marx HE, Barker MS, Tank DC, Soltis PS. Impact of whole-genome duplication events on diversification rates in angiosperms. Am J Bot. 2018;105:348–63.
Lawrence WJC. The secondary association of chromosomes. Cytologia. 1931;2:352–84.
Les DH. Aquatic dicotyledons of North America: ecology, life history, and systematics. Boca Raton: CRC Press; 2017.
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25:2078–9.
Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics. 2006;22:1658–9.
Marshall DC, Simon C, Buckley TR. Accurate branch length estimation in partitioned Bayesian analyses requires accommodation of among-partition rate variation and attention to branch length priors. Syst Biol. 2006;55:993–1003.
Martin M, Patterson M, Garg S, Fischer SO, Pisanti N, Klau GW, Schöenhuth A, Marschall T. WhatsHap: fast and accurate read-based phasing. https://doi.org/10.1101/085050.
Matasci N, Hung L-H, Yan Z, Carpenter EJ, Wickett NJ, et al. Data access for the 1,000 Plants (1KP) project. GigaScience. 2014;3:17.
Menzel MY. The pachytene chromosome complement of Hibiscus cannabinus. Cytologia. 1966;31:36–42.
Menzel MY, Wilson FD. Genetic relationships in Hibiscus sect. Furcaria Brittonia. 1969;21:91.
Murray BG, Craven LA, De Lange PJ. New observations on chromosome number variation in Hibiscus trionum s.l. (Malvaceae) and their implications for systematics and conservation. NZ J Bot. 2008;46:315–9.
Otto SP, Whitton J. Polyploid incidence and evolution. Annu Rev Genet. 2000;34:401–37.
Paterson AH, Wendel JF, Gundlach H, Guo H, Jenkins J, et al. Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature. 2012;492:423.
Pellicer J, Hidalgo O, Dodsworth S, Leitch IJ. Genome size diversity and its impact on the evolution of land plants. Genes. 2018;9:88.
Pfeil B, Brubaker C, Craven L, Crisp M. Phylogeny of Hibiscus and the tribe Hibisceae (Malvaceae) using chloroplast DNA sequences of ndhF and the rpl16 intron. Syst Bot. 2020;333–350. https://doi.org/10.1043/0363-6445-27.2.333.
Pfeil B, Brubaker CL, Craven LA, Crisp M. Paralogy and orthology in the Malvaceae rpb2 gene family: investigation of gene duplication in Hibiscus. Mol Biol Evol. 2004;21:1428–37.
Pfeil B, Crisp M. What to do with Hibiscus? A proposed nomenclatural resolution for a large and well known genus of Malvaceae and comments on paraphyly. Aust Syst Bot. 2005;18:49–60.
Rabier C-E, Ta T, Ané C. Detecting and locating whole genome duplications on a phylogeny: a probabilistic approach. Mol Biol Evol. 2013;31:750–62.
Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–4.
Schnable JC, Springer NM, Freeling M. Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc Natl Acad Sci USA. 2011;108:4069–74.
Schranz ME, Mitchell-Olds T. Independent ancient polyploidy events in the sister families Brassicaceae and Cleomaceae. Plant Cell. 2006;18:1152–65.
Seelanan T, Schnabel A, Wendel JF. Congruence and consensus in the cotton tribe (Malvaceae). Syst Bot. 1997;22:259–90.
Skovsted A. Chromosome numbers in the Malvaceae II. Comptes rendus des traveaux du laboratoire Carlberg. Physiologique. 1941; 195–242.
Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, et al. Polyploidy and angiosperm diversification. Am J Bot. 2009;96:336–48.
Soltis PS, Marchant DB, Van de Peer Y, Soltis DE. Polyploidy and genome evolution in plants. Curr Opin Genet Dev. 2015;35:119–25.
Stebbins G. Types of polyploids: their classification and significance. Adv Genet. 1947;1:403–29.
Stebbins C Jr. Variation and evolution in plants: progress during the past twenty years. In: Hecht MK, Steere WC, editors. Essays in evolution and genetics in honor of Theodosius Dobzhansky. Boston: Springer; 1950.
Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993;10:512–26.
Tang H, Wang X, Bowers JE, Ming R, Alam M, Paterson AH. Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res. 2008;18(12):1944–54.
Thomas BC, Pedersen B, Freeling M. Following tetraploidy in an Arabidopsis ancestor, genes were removed preferentially from one homeolog leaving clusters enriched in dose-sensitive genes. Genome Res. 2006;16:934–46.
Turner BL, Mendenhall MG. A revision of Malvaviscus (Malvaceae). Ann Missouri Botanical Garden. 1993. https://doi.org/10.2307/2399792.
Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science. 2006;313:1596–604.
Wagenmakers EJ, Farrell S. AIC model selection using Akaike weights. Psychonomic Bull. 2004;11:192–6.
Wang K, Wang Z, Li F, Ye W, Wang J, et al. The draft genome of a diploid cotton Gossypium raimondii. Nat Genet. 2012;44:1098.
Vanneste K, Van de Peer Y, Maere S. Inference of genome duplications from age distributions revisited. Mol Biol Evol. 2012;30:177–90.
Wanscher J. The basic chromosome number of the higher plants. New Phytol. 1934;33:101–26.
Wendel JF. The wondrous cycles of polyploidy in plants. Am J Bot. 2015;102:1753–6.
Wendel JF, Cronn RC. Polyploidy and the evolutionary history of cotton. Adv Agron. 2003;78:139.
Wendel JF, Schnabel A, Seelanan T. An unusual ribosomal DNA sequence from Gossypium gossypioides reveals ancient, cryptic, intergenomic introgression. Mol Phylogenet Evol. 1995;4:298–313.
Wickett NJ, Mirarab S, Nguyen N, Warnow T, Carpenter E, et al. Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc Natl Acad Sci USA. 2014;111:E4859–68.
Wilson FD. The genome biogeography of Hibiscus L. section Furcaria DC. Genet Resour Crop Evol. 1994;41:13–25.
Wilson FD. A distributional and cytological survey of the presently recognized taxa of Hibiscus section Furcaria (Malvaceae). Bonplandia. 2006;15(1/2):53–62. http://www.jstor.org/stable/41941285. Accessed 9 Feb 2021.
Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, et al. The frequency of polyploid speciation in vascular plants. Proc Natl Acad Sci USA. 2009;106:13875–9.
Woodhouse MR, Schnable JC, Pedersen BS, Lyons E, Lisch D, Subramaniam S, Freeling M. Following tetraploidy in maize, a short deletion mechanism removed genes preferentially from one of the two homologs. PLoS Biol. 2010;8:e1000409.
Xie Y, Wu G, Tang J, Luo R, Patterson J, et al. SOAPdenovo-Trans: de novo transcriptome assembly with short RNA-Seq reads. Bioinformatics. 2014;30:1660–6.
Xu Q, Xiong G, Li P, He F, Huang Y, Wang K, Li Z, Hua J, Badger JH. Analysis of complete nucleotide sequences of 12 Gossypium chloroplast genomes: origin and evolution of allotetraploids. PloS One. 2012;7(8):e37128.
Zheng L, Michael SB. Inferring putative ancient whole-genome duplications in the 1000 Plants (1KP) initiative: access to gene family phylogenies and age distributions. GigaScience. 2020;9.
Zhang Y, Xu G-H, Guo X-Y, Fan L-J. Two ancient rounds of polyploidy in rice genome. J Zhejiang Univ Sci B. 2005;6:87–90.