The evolution of huge Y chromosomes in Coccinia grandis and its sister, Coccinia schimperi
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
35306898
PubMed Central
PMC8935295
DOI
10.1098/rstb.2021.0294
Knihovny.cz E-zdroje
- Klíčová slova
- XY divergence, cytogenetics, genetic map, heteromorphic XY chromosomes, sex chromosomes,
- MeSH
- chromozomy rostlin * genetika MeSH
- Cucurbitaceae * genetika MeSH
- molekulární evoluce MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Microscopically dimorphic sex chromosomes in plants are rare, reducing our ability to study them. One difficulty has been the paucity of cultivatable species pairs for cytogenetic, genomic and experimental work. Here, we study the newly recognized sisters Coccinia grandis and Coccinia schimperi, both with large Y chromosomes as we here show for Co. schimperi. We built genetic maps for male and female Co. grandis using a full-sibling family, inferred gene sex-linkage, and, with Co. schimperi transcriptome data, tested whether X- and Y-alleles group by species or by sex. Most sex-linked genes for which we could include outgroups grouped the X- and Y-alleles by species, but some 10% instead grouped the two species' X-alleles. There was no relationship between XY synonymous-site divergences in these genes and gene position on the non-recombining part of the X, suggesting recombination arrest shortly before or after species divergence, here dated to about 3.6 Ma. Coccinia grandis and Co. schimperi are the species pair with the most heteromorphic sex chromosomes in vascular plants (the condition in their sister remains unknown), and future work could use them to study mechanisms of Y chromosome enlargement and parallel degeneration, or to test Haldane's rule about lower hybrid fitness in the heterogametic sex. This article is part of the theme issue 'Sex determination and sex chromosome evolution in land plants'.
Department of Biology Washington University Saint Louis MO USA
Institute of Biophysics of the Czech Academy of Sciences Královopolská 135 61265 Brno Czech Republic
Zobrazit více v PubMed
Ming R, Bendahmane A, Renner SS. 2011. Sex chromosomes in land plants. Annu. Rev. Plant Biol. 62, 485-514. (10.1146/annurev-arplant-042110-103914) PubMed DOI
Renner SS. 2014. The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. Am. J. Bot. 101, 1588-1596. (10.3732/ajb.1400196) PubMed DOI
Papadopulos AS, Chester M, Ridout K, Filatov DA. 2015. Rapid Y degeneration and dosage compensation in plant sex chromosomes. Proc. Natl Acad. Sci. USA 112, 13 021-13 026. (10.1073/pnas.1508454112) PubMed DOI PMC
Krasovec M, Zhang Y, Filatov DA. 2020. The location of the pseudoautosomal boundary in Silene latifolia. Genese 11, 610. (10.3390/genes11060610) PubMed DOI PMC
Sousa A, Fuchs J, Renner SS. 2013. Molecular cytogenetics (FISH, GISH) of Coccinia grandis: a ca. 3 myr-old species of Cucurbitaceae with the largest Y/autosome divergence in flowering plants. Cytogenet. Genome Res. 139, 107-118. (10.1159/000345370) PubMed DOI
Fruchard C, et al. 2020. Evidence for dosage compensation in Coccinia grandis, a plant with a highly heteromorphic XY system. Genes (Basel) 11, 1-18. (10.3390/genes11070787) PubMed DOI PMC
Prentout D, Razumova O, Rhoné B, Badouin H, Henri H, Feng C, Käfer J, Karlov G, Marais GAB. 2020. An efficient RNA-seq-based segregation analysis identifies the sex chromosomes of Cannabis sativa. Genome Res. 30, 164-172. (10.1101/gr.251207.119) PubMed DOI PMC
Muyle A, Zemp N, Deschamps C, Mousset S, Widmer A, Marais GA. 2012. Rapid de novo evolution of X chromosome dosage compensation in Silene latifolia, a plant with young sex chromosomes. PLoS Biol. 10, e1001308. (10.1371/journal.pbio.1001308) PubMed DOI PMC
Holstein N. 2015. Monograph of Coccinia (Cucurbitaceae). PhytoKeys 54, 1-166. (10.3897/phytokeys.54.3285) PubMed DOI PMC
Holstein N, Renner SS. 2011. A dated phylogeny and collection records reveal repeated biome shifts in the African genus Coccinia (Cucurbitaceae). BMC Evol. Biol. 11, 28. (10.1186/1471-2148-11-28) PubMed DOI PMC
Kumar LS, Vishveshwaraiah S. 1952. Sex mechanism in Coccinia indica Wight and Arn. Nature 170, 330-331. (10.1038/170330a0) PubMed DOI
Sousa A, Bellot S, Fuchs J, Houben A, Renner SS. 2016. Analysis of transposable elements and organellar DNA in male and female genomes of a species with a huge Y chromosome reveals distinct Y centromeres. Plant J. 88, 387-396. (10.1111/tpj.13254) PubMed DOI
Sousa A, Fuchs J, Renner SS. 2017. Cytogenetic comparison of heteromorphic and homomorphic sex chromosomes in Coccinia (Cucurbitaceae) points to sex chromosome turnover. Chromosom. Res. 25, 191-200. (10.1007/s10577-017-9555-y) PubMed DOI
Naudin C. 1859. Revue des Cucurbitacées cultivées au Muséum, en 1859. Ann. Sci. Nat. Bot. Ser. 4, 79-164.
Naudin C. 1862. Cucurbitacées cultivées au muséum d'histoire naturelle en 1862. Ann. Sci. Nat. Bot. Ser. 4, 159-208.
Marza VD, Cerchez N. 1967. Charles Naudin, a pioneer of contemporary biology. J. d'Agriculture Tropicale et de Botanique Appl. 14, 369-401. (10.3406/jatba.1967.2944) DOI
Devani RS, Sinha S, Banerjee J, Sinha RK, Bendahmane A, Banerjee AK. 2017. De novo transcriptome assembly from flower buds of dioecious, gynomonoecious and chemically masculinized female Coccinia grandis reveals genes associated with sex expression and modification. BMC Plant Biol. 17, 241. (10.1186/s12870-017-1187-z) PubMed DOI PMC
Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-2120. (10.1093/bioinformatics/btu170) PubMed DOI PMC
Haas BJ, et al. 2013. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494-1512. (10.1038/nprot.2013.084) PubMed DOI PMC
Bushmanova E, Antipov D, Lapidus A, Prjibelski AD. 2019. RnaSPAdes: a de novo transcriptome assembler and its application to RNA-Seq data. Gigascience 8, giz100. (10.1093/gigascience/giz100) PubMed DOI PMC
Gilbert D. 2013. Gene-omes built from mRNA seq not genome DNA. In 7th annual arthropod genomics symposium. Notre Dame. F1000Research 5, 1695. (10.7490/f1000research.1112594.1) DOI
Seppey M, Manni M, Zdobnov EM. 2019. BUSCO: assessing genome assembly and annotation completeness. Methods Mol. Biol. 1962, 227-245. (10.1007/978-1-4939-9173-0_14) PubMed DOI
Guo J, Xu W, Hu Y, Huang J, Zhao Y, Zhang L, Huang CH, Ma H. 2020. Phylotranscriptomics in Cucurbitaceae reveal multiple whole-genome duplications and key morphological and molecular innovations. Mol. Plant 13, 1117-1133. (10.1016/j.molp.2020.05.011) PubMed DOI
Schaefer H, Renner SS. 2011. Phylogenetic relationships in the order Cucurbitales and a new classification of the gourd family (Cucurbitaceae). Taxon 60, 122-138. (10.1002/tax.601011) DOI
Muyle A, Käfer J, Zemp N, Mousset S, Picard F, Marais GA. 2016. SEX-DETector: a probabilistic approach to study sex chromosomes in non-model organisms. Genome Biol. Evol. 8, 2530-2543. (10.1093/gbe/evw172) PubMed DOI PMC
Liao Y, Smyth GK, Shi W. 2013. The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Res. 41, e108. (10.1093/nar/gkt214) PubMed DOI PMC
Tsagkogeorga G, Cahais V, Galtier N. 2012. The population genomics of a fast evolver: high levels of diversity, functional constraint, and molecular adaptation in the tunicate Ciona intestinalis. Genome Biol. Evol. 4, 740-749. (10.1093/gbe/evs054) PubMed DOI PMC
Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. 2011. Integrative genomics viewer. Nat. Biotechnol. 29, 24-26. (10.1038/nbt.1754) PubMed DOI PMC
Rastas P. 2017. Lep-MAP3: robust linkage mapping even for low-coverage whole genome sequencing data. Bioinformatics 33, 3726-3732. (10.1093/bioinformatics/btx494) PubMed DOI
Rastas P, Calboli FCF, Guo B, Shikano T, Merilä J. 2016. Construction of ultra-dense linkage maps with Lep-MAP2: stickleback F2 recombinant crosses as an example. Genome Biol. Evol. 8, 78-93. (10.1093/gbe/evv250) PubMed DOI PMC
Holtz Y, David J, Ranwez V. 2017. The genetic map comparator: a user-friendly application to display and compare genetic maps. Bioinformatics 33, btw816. (10.1093/bioinformatics/btw816) PubMed DOI
R Core Team. 2020. R: a language and environment for statistical computing (v.4.0.2). Vienna, Austria: R Foundation for Statistical Computing. (https://cran.r-project.org/)
Ouellette LA, Reid RW, Blanchard SG, Brouwer CR. 2018. LinkageMapView-rendering high-resolution linkage and QTL maps. Bioinformatics 34, 306-307. (10.1093/bioinformatics/btx576) PubMed DOI PMC
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. 2009. BLAST+: architecture and applications. BMC Bioinf. 10, 421. (10.1186/1471-2105-10-421) PubMed DOI PMC
Ranwez V, Harispe S, Delsuc F, Douzery EJP. 2011. MACSE: Multiple alignment of coding sequences accounting for frameshifts and stop codons. PLoS ONE 6, e22594. (10.1371/journal.pone.0022594) PubMed DOI PMC
Talavera G, Castresana J. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 56, 564-577. (10.1080/10635150701472164) PubMed DOI
Ronquist F, et al. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539-542. (10.1093/sysbio/sys029) PubMed DOI PMC
Rambaut A, Suchard MA, Xie D, Drummond AJ. 2013. Tracer v1.7.1. See https://github.com/beast-dev/tracer/releases/latest (accessed Oct 2021).
Rambaut A. 2012. FigTree v1.4.0. See http://tree.bio.ed.ac.uk/software/figtree/ (accessed Oct 2021).
Stephens TG, Bhattacharya D, Ragan MA, Chan CX. 2016. PhySortR: a fast, flexible tool for sorting phylogenetic trees in R. PeerJ 4, e2038. (10.7717/peerj.2038) PubMed DOI PMC
Larget BR, Kotha SK, Dewey CN, Ané C. 2010. BUCKy: gene tree/species tree reconciliation with Bayesian concordance analysis. Bioinformatics 26, 2910-2911. (10.1093/bioinformatics/btq539) PubMed DOI
Sukumaran J, Holder MT. 2010. DendroPy: a Python library for phylogenetic computing. Bioinformatics 26, 1569-1571. (10.1093/bioinformatics/btq228) PubMed DOI
Wickham H. 2016. Ggplot2: elegant graphics for data analysis. New York, NY: Springer.
Emms DM, Kelly S. 2019. DendroPy: a OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biology 20, 238. PubMed PMC
Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591. (10.1093/molbev/msm088) PubMed DOI
Schaefer H, Heibl C, Renner SS. 2009. Gourds afloat: a dated phylogeny reveals an Asian origin of the gourd family (Cucurbitaceae) and numerous oversea dispersal events. Proc. R. Soc. B 276, 843-851. (10.1098/rspb.2008.1447) PubMed DOI PMC
Bacovsky V, Čegan R, Šimoníková D, Hřibová E, Hobza R. 2020. The formation of sex chromosomes in Silene latifolia and S. dioica was accompanied by multiple chromosomal rearrangements. Front. Plant Sci. 11, 205. (10.3389/fpls.2020.00205) PubMed DOI PMC
Nicolas M, et al. 2005. A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants. PLoS Biol. 3, e4. (10.1371/journal.pbio.0030004) PubMed DOI PMC
Prentout D, Stajner N, Cerenak A, Tricou T, Brochier-Armanet C, Jakse J, Käfer J, Marais GAB. 2021. Plant genera Cannabis and Humulus share the same pair of well-differentiated sex chromosomes. New Phytol. 231, 1599-1611. (10.1111/nph.17456) PubMed DOI
Haldane JBS. 1922. Sex ratio and unisexual sterility in hybrid animals. J. Genet. 12, 101-109. (10.1007/BF02983075) DOI
Brothers AN, Delph LF. 2010. Haldane's rule is extended to plants with sex chromosomes. Evolution 64, 3643-3648. (10.1111/j.1558-5646.2010.01095.x) PubMed DOI
Demuth JP, Flanagan RJ, Delph LF. 2014. Genetic architecture of isolation between two species of Silene with sex chromosomes and Haldane's rule. Evolution 68, 332-342. (10.1111/evo.12269) PubMed DOI
Janousek B, Gogela R, Bacovsky V, Renner SS. 2022. The evolution of huge Y chromosomes in Coccinia grandis and its sister, Coccinia schimperi. Figshare. PubMed PMC
Sexy ways: approaches to studying plant sex chromosomes
The evolution of huge Y chromosomes in Coccinia grandis and its sister, Coccinia schimperi
figshare
10.6084/m9.figshare.c.5879864