Section: Genomics
Topic: Genetics/Genomics, Plant biology

Genetic mapping of sex and self-incompatibility determinants in the androdioecious plant Phillyrea angustifolia

10.24072/pcjournal.23 - Peer Community Journal, Volume 1 (2021), article no. e15.

Get full text PDF Peer reviewed and recommended by PCI
article image

The diversity of mating and sexual systems in angiosperms is spectacular, but the factors driving their evolution remain poorly understood. In plants of the Oleaceae family, an unusual self-incompatibility (SI) system has been discovered recently, whereby only two distinct homomorphic SI specificities segregate stably. To understand the role of this peculiar SI system in preventing or promoting the diversity of sexual phenotypes observed across the family, an essential first step is to characterize the genetic architecture of these two traits. Here, we developed a high-density genetic map of the androdioecious shrub P. angustifolia based on a F1 cross between a hermaphrodite and a male parent with distinct SI genotypes. Using a double restriction-site associated digestion (ddRAD) sequencing approach, we obtained reliable genotypes for 196 offspring and their two parents at 10,388 markers. The resulting map comprises 23 linkage groups totaling 1,855.13 cM on the sex-averaged map. We found strong signals of association for the sex and SI phenotypes, that were each associated with a unique set of markers on linkage group 12 and 18 respectively, demonstrating inheritance of these traits as single, independent, mendelian factors. The P. angustifolia linkage map shows robust synteny to the olive tree genome overall. Two of the six markers strictly associated with SI in P. angustifolia have strong similarity with a recently identified 741kb chromosomal region fully linked to the SI phenotype on chromosome 18 of the olive tree genome, providing strong cross-validation support. The SI locus stands out as being markedly rearranged, while the sex locus has remained relatively more collinear between the two species. This P. angustifolia linkage map will be a useful resource to investigate the various ways by which the sex and SI determination systems have co-evolved in the broader phylogenetic context of the Oleaceae family.

Published online:
DOI: 10.24072/pcjournal.23
Type: Research article

Carré, Amélie 1; Gallina, Sophie 1; Santoni, Sylvain 2; Vernet, Philippe 1; Godé, Cécile 1; Castric, Vincent 1; Saumitou-Laprade, Pierre 1

1 CNRS, Univ. Lille, UMR 8198 – Evo-Eco-Paleo, F-59000 Lille, France
2 UMR DIAPC - Diversité et adaptation des plantes cultivées - Montpellier, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Carr\'e, Am\'elie and Gallina, Sophie and Santoni, Sylvain and Vernet, Philippe and God\'e, C\'ecile and Castric, Vincent and Saumitou-Laprade, Pierre},
     title = {Genetic mapping of sex and self-incompatibility determinants in the androdioecious plant {\protect\emph{Phillyrea} angustifolia}},
     journal = {Peer Community Journal},
     eid = {e15},
     publisher = {Peer Community In},
     volume = {1},
     year = {2021},
     doi = {10.24072/pcjournal.23},
     url = {}
AU  - Carré, Amélie
AU  - Gallina, Sophie
AU  - Santoni, Sylvain
AU  - Vernet, Philippe
AU  - Godé, Cécile
AU  - Castric, Vincent
AU  - Saumitou-Laprade, Pierre
TI  - Genetic mapping of sex and self-incompatibility determinants in the androdioecious plant Phillyrea angustifolia
JO  - Peer Community Journal
PY  - 2021
VL  - 1
PB  - Peer Community In
UR  -
DO  - 10.24072/pcjournal.23
ID  - 10_24072_pcjournal_23
ER  - 
%0 Journal Article
%A Carré, Amélie
%A Gallina, Sophie
%A Santoni, Sylvain
%A Vernet, Philippe
%A Godé, Cécile
%A Castric, Vincent
%A Saumitou-Laprade, Pierre
%T Genetic mapping of sex and self-incompatibility determinants in the androdioecious plant Phillyrea angustifolia
%J Peer Community Journal
%D 2021
%V 1
%I Peer Community In
%R 10.24072/pcjournal.23
%F 10_24072_pcjournal_23
Carré, Amélie; Gallina, Sophie; Santoni, Sylvain; Vernet, Philippe; Godé, Cécile; Castric, Vincent; Saumitou-Laprade, Pierre. Genetic mapping of sex and self-incompatibility determinants in the androdioecious plant Phillyrea angustifolia. Peer Community Journal, Volume 1 (2021), article  no. e15. doi : 10.24072/pcjournal.23.

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.genomics.100011

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Badouin, H.; Hood, M. E.; Gouzy, J.; Aguileta, G.; Siguenza, S.; Perlin, M. H.; Cuomo, C. A.; Fairhead, C.; Branca, A.; Giraud, T. Chaos of Rearrangements in the Mating-Type Chromosomes of the Anther-Smut Fungus Microbotryum lychnidis-dioicae, Genetics, Volume 200 (2015) no. 4, pp. 1275-1284 | DOI

[2] Barrett, S. C. H. The evolution of plant sexual diversity, Nature Reviews Genetics, Volume 3 (2002) no. 4, pp. 274-284 | DOI

[3] Barrett, S. C. The evolution and adaptive significance of heterostyly, Trends in Ecology & Evolution, Volume 5 (1990) no. 5, pp. 144-148 | DOI

[4] Barrett, S. C. H. Heterostylous Genetic Polymorphisms: Model Systems for Evolutionary Analysis, In S. C. H. Barrett (Ed.), Evolution and Function of Heterostyly, Springer Berlin Heidelberg, Berlin, Heidelberg, 1992, pp. 1-29 | DOI

[5] Barrett, S. C. The evolution of mating strategies in flowering plants, Trends in Plant Science, Volume 3 (1998) no. 9, pp. 335-341 | DOI

[6] Barrett, S. C. H. ‘A most complex marriage arrangement’: recent advances on heterostyly and unresolved questions, New Phytologist, Volume 224 (2019) no. 3, pp. 1051-1067 | DOI

[7] Besnard, G.; Rubio de Casas, R.; Christin, P.-A.; Vargas, P. Phylogenetics of Olea (Oleaceae) based on plastid and nuclear ribosomal DNA sequences: Tertiary climatic shifts and lineage differentiation times, Annals of Botany, Volume 104 (2009) no. 1, pp. 143-160 | DOI

[8] Billiard, S.; Husse, L.; Lepercq, P.; Godé, C.; Bourceaux, A.; Lepart, J.; Vernet, P.; Saumitou-Laprade, P. Selfish male-determining element favors the transition from hermaphroditism to androdioecy, Evolution, Volume 69 (2015) no. 3, pp. 683-693 | DOI

[9] Billiard, S.; López-Villavicencio, M.; Devier, B.; Hood, M. E.; Fairhead, C.; Giraud, T. Having sex, yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types, Biological Reviews, Volume 86 (2011) no. 2, pp. 421-442 | DOI

[10] Carré, A.; Gallina, S. Amelie-Carre/Genetic-map-of-Phillyrea-angustifolia: First release: Genetic map of Phillyrea angustifolia (v1.0). Zenodo, 2021 | DOI

[11] Castric, V.; Vekemans, X. Plant self-incompatibility in natural populations: a critical assessment of recent theoretical and empirical advances, Molecular Ecology, Volume 13 (2004) no. 10, pp. 2873-2889 | DOI

[12] Catchen, J. M.; Amores, A.; Hohenlohe, P.; Cresko, W.; Postlethwait, J. H. Stacks: Building and Genotyping Loci De Novo From Short-Read Sequences, G3 Genes|Genomes|Genetics, Volume 1 (2011) no. 3, pp. 171-182 | DOI

[13] Chantha, S.; Herman, A. C.; Castric, V.; Vekemans, X.; Marande, W.; Schoen, D. J. The unusual S locus of Leavenworthia is composed of two sets of paralogous loci, New Phytologist, Volume 216 (2017) no. 4, pp. 1247-1255 | DOI

[14] Chantha, S.-C.; Herman, A. C.; Platts, A. E.; Vekemans, X.; Schoen, D. J. Secondary Evolution of a Self-Incompatibility Locus in the Brassicaceae Genus Leavenworthia, PLoS Biology, Volume 11 (2013) no. 5 | DOI

[15] Charlesworth, B. The population genetics of anisogamy, Journal of Theoretical Biology, Volume 73 (1978) no. 2, pp. 347-357 | DOI

[16] Charlesworth, D.; Charlesworth, B. A Model for the Evolution of Distyly, The American Naturalist, Volume 114 (1979) no. 4, pp. 467-498 | DOI

[17] De-Kayne, R.; Feulner, P. G. D. A European Whitefish Linkage Map and Its Implications for Understanding Genome-Wide Synteny Between Salmonids Following Whole Genome Duplication, G3 Genes|Genomes|Genetics, Volume 8 (2018) no. 12, pp. 3745-3755 | DOI

[18] De Cauwer, I.; Vernet, P.; Billiard, S.; Godé, C.; Bourceaux, A.; Ponitzki, C.; Saumitou-Laprade, P. Widespread coexistence of self-compatible and self-incompatible phenotypes in a diallelic self-incompatibility system in Ligustrum vulgare (Oleaceae), Heredity, Volume 127 (2021) no. 4, pp. 384-392 | DOI

[19] de Nettancourt, D. Incompatibility in Angiosperms, Monographs on Theoretical and Applied Genetics, Springer Berlin Heidelberg, Berlin, Heidelberg, 1977 | DOI

[20] Diggle, P. K.; Di Stilio, V. S.; Gschwend, A. R.; Golenberg, E. M.; Moore, R. C.; Russell, J. R.; Sinclair, J. P. Multiple developmental processes underlie sex differentiation in angiosperms, Trends in Genetics, Volume 27 (2011) no. 9, pp. 368-376 | DOI

[21] Dommée, B.; Thompson, J. D.; Cristini, F. Distylie chezJasminum fruticansL.: hypothèse de la pollinisation optimale basée sur les variations de l'écologie intraflorale, Bulletin de la Société Botanique de France. Lettres Botaniques, Volume 139 (1992) no. 3, pp. 223-234 | DOI

[22] Dulberger, R. Floral Polymorphisms and Their Functional Significance in the Heterostylous Syndrome, In S. C. H. Barrett (Ed.), Evolution and Function of Heterostyly, Springer Berlin Heidelberg, Berlin, Heidelberg, 1992, pp. 41-84 | DOI

[23] Dupin, J.; Raimondeau, P.; Hong-Wa, C.; Manzi, S.; Gaudeul, M.; Besnard, G. Resolving the Phylogeny of the Olive Family (Oleaceae): Confronting Information from Organellar and Nuclear Genomes, Genes, Volume 11 (2020) no. 12 | DOI

[24] Dussert, Y.; Legrand, L.; Mazet, I. D.; Couture, C.; Piron, M.-C.; Serre, R.-F.; Bouchez, O.; Mestre, P.; Toffolatti, S. L.; Giraud, T.; Delmotte, F. Identification of the First Oomycete Mating-type Locus Sequence in the Grapevine Downy Mildew Pathogen, Plasmopara viticola, Current Biology, Volume 30 (2020) no. 20 | DOI

[25] Geng, S.; De Hoff, P.; Umen, J. G. Evolution of Sexes from an Ancestral Mating-Type Specification Pathway, PLoS Biology, Volume 12 (2014) no. 7 | DOI

[26] Goubet, P. M.; Bergès, H.; Bellec, A.; Prat, E.; Helmstetter, N.; Mangenot, S.; Gallina, S.; Holl, A.-C.; Fobis-Loisy, I.; Vekemans, X.; Castric, V. Contrasted Patterns of Molecular Evolution in Dominant and Recessive Self-Incompatibility Haplotypes in Arabidopsis, PLoS Genetics, Volume 8 (2012) no. 3 | DOI

[27] Guo, Y.-L.; Zhao, X.; Lanz, C.; Weigel, D. Evolution of the S-Locus Region in Arabidopsis Relatives    , Plant Physiology, Volume 157 (2011) no. 2, pp. 937-946 | DOI

[28] Husse, L.; Billiard, S.; Lepart, J.; Vernet, P.; Saumitou-Laprade, P. A one-locus model of androdioecy with two homomorphic self-incompatibility groups: expected vs. observed male frequencies, Journal of Evolutionary Biology, Volume 26 (2013) no. 6, pp. 1269-1280 | DOI

[29] Iwano, M.; Ito, K.; Shimosato-Asano, H.; Lai, K.-S.; Takayama, S. Self-Incompatibility in the Brassicaceae, Sexual Reproduction in Animals and Plants, Springer Japan, Tokyo, 2014, pp. 245-254 | DOI

[30] Iwano, M.; Takayama, S. Self/non-self discrimination in angiosperm self-incompatibility, Current Opinion in Plant Biology, Volume 15 (2012) no. 1, pp. 78-83 | DOI

[31] Jiménez‐Ruiz, J.; Ramírez‐Tejero, J. A.; Fernández‐Pozo, N.; Leyva‐Pérez, M. d. l. O.; Yan, H.; Rosa, R. d. l.; Belaj, A.; Montes, E.; Rodríguez‐Ariza, M. O.; Navarro, F.; Barroso, J. B.; Beuzón, C. R.; Valpuesta, V.; Bombarely, A.; Luque, F. Transposon activation is a major driver in the genome evolution of cultivated olive trees ( Olea europaea L.), The Plant Genome, Volume 13 (2020) no. 1 | DOI

[32] Keller, B.; Thomson, J. D.; Conti, E. Heterostyly promotes disassortative pollination and reduces sexual interference in Darwin's primroses: evidence from experimental studies, Functional Ecology, Volume 28 (2014) no. 6, pp. 1413-1425 | DOI

[33] Kozielska, M.; Weissing, F. J.; Beukeboom, L. W.; Pen, I. Segregation distortion and the evolution of sex-determining mechanisms, Heredity, Volume 104 (2010) no. 1, pp. 100-112 | DOI

[34] Krzywinski, M.; Schein, J.; Birol, İ.; Connors, J.; Gascoyne, R.; Horsman, D.; Jones, S. J.; Marra, M. A. Circos: An information aesthetic for comparative genomics, Genome Research, Volume 19 (2009) no. 9, pp. 1639-1645 | DOI

[35] Kubo, K.-i.; Paape, T.; Hatakeyama, M.; Entani, T.; Takara, A.; Kajihara, K.; Tsukahara, M.; Shimizu-Inatsugi, R.; Shimizu, K. K.; Takayama, S. Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia, Nature Plants, Volume 1 (2015) no. 1, pp. 1-9 | DOI

[36] Langmead, B.; Salzberg, S. L. Fast gapped-read alignment with Bowtie 2, Nature Methods, Volume 9 (2012) no. 4, pp. 357-359 | DOI

[37] Li, H.; Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform, Bioinformatics, Volume 25 (2009) no. 14, pp. 1754-1760 | DOI

[38] Li, J.; Cocker, J. M.; Wright, J.; Webster, M. A.; McMullan, M.; Dyer, S.; Swarbreck, D.; Caccamo, M.; Oosterhout, C. v.; Gilmartin, P. M. Genetic architecture and evolution of the S locus supergene in Primula vulgaris, Nature Plants, Volume 2 (2016) no. 12 | DOI

[39] Lundqvist, A. Self-incompatibility in rye, Hereditas, Volume 42 (1956) no. 3-4, pp. 293-348 | DOI

[40] Mariotti, R.; Pandolfi, S.; De Cauwer, I.; Saumitou‐Laprade, P.; Vernet, P.; Rossi, M.; Baglivo, F.; Baldoni, L.; Mousavi, S. Diallelic self‐incompatibility is the main determinant of fertilization patterns in olive orchards, Evolutionary Applications, Volume 14 (2021) no. 4, pp. 983-995 | DOI

[41] Muyle, A.; Käfer, J.; Zemp, N.; Mousset, S.; Picard, F.; Marais, G. A. SEX-DETector: A Probabilistic Approach to Study Sex Chromosomes in Non-Model Organisms, Genome Biology and Evolution, Volume 8 (2016) no. 8, pp. 2530-2543 | DOI

[42] Olofsson, J. K.; Cantera, I.; Van de Paer, C.; Hong‐Wa, C.; Zedane, L.; Dunning, L. T.; Alberti, A.; Christin, P.; Besnard, G. Phylogenomics using low‐depth whole genome sequencing: A case study with the olive tribe, Molecular Ecology Resources, Volume 19 (2019) no. 4, pp. 877-892 | DOI

[43] Pannell, J. R.; Korbecka, G. Mating-System Evolution: Rise of the Irresistible Males, Current Biology, Volume 20 (2010) no. 11 | DOI

[44] Pannell, J. R.; Voillemot, M. Plant Mating Systems: Female Sterility in the Driver’s Seat, Current Biology, Volume 25 (2015) no. 12 | DOI

[45] Peterson, B. K.; Weber, J. N.; Kay, E. H.; Fisher, H. S.; Hoekstra, H. E. Double Digest RADseq: An Inexpensive Method for De Novo SNP Discovery and Genotyping in Model and Non-Model Species, PLoS ONE, Volume 7 (2012) no. 5 | DOI

[46] Rastas, P. Lep-MAP3: robust linkage mapping even for low-coverage whole genome sequencing data, Bioinformatics, Volume 33 (2017) no. 23, pp. 3726-3732 | DOI

[47] Rochette, N. C.; Catchen, J. M. Deriving genotypes from RAD-seq short-read data using Stacks, Nature Protocols, Volume 12 (2017) no. 12, pp. 2640-2659 | DOI

[48] Sakai, A. K.; Weller, S. G. Gender and Sexual Dimorphism in Flowering Plants: A review of Terminology, Biogeographic Patterns, Ecological Correlates, and Phylogenetic Approaches, In M. A. Geber, T. E. Dawson, & L. F. Delph (Eds.), Gender and Sexual Dimorphism in Flowering Plants, Springer Berlin Heidelberg, Berlin, Heidelberg, 1999, pp. 1-31 | DOI

[49] Saumitou-Laprade, P.; Vernet, P.; Dowkiw, A.; Bertrand, S.; Billiard, S.; Albert, B.; Gouyon, P.-H.; Dufay, M. Polygamy or subdioecy? The impact of diallelic self-incompatibility on the sexual system in Fraxinus excelsior (Oleaceae), Proceedings of the Royal Society B: Biological Sciences, Volume 285 (2018) no. 1873 | DOI

[50] Saumitou-Laprade, P.; Vernet, P.; Vassiliadis, C.; Hoareau, Y.; de Magny, G.; Dommée, B.; Lepart, J. A Self-Incompatibility System Explains High Male Frequencies in an Androdioecious Plant, Science, Volume 327 (2010) no. 5973, pp. 1648-1650 | DOI

[51] Saumitou-Laprade, P.; Vernet, P.; Vekemans, X.; Billiard, S.; Gallina, S.; Essalouh, L.; Mhaïs, A.; Moukhli, A.; El Bakkali, A.; Barcaccia, G.; Alagna, F.; Mariotti, R.; Cultrera, N. G. M.; Pandolfi, S.; Rossi, M.; Khadari, B.; Baldoni, L. Elucidation of the genetic architecture of self-incompatibility in olive: Evolutionary consequences and perspectives for orchard management, Evolutionary Applications, Volume 10 (2017) no. 9, pp. 867-880 | DOI

[52] Taylor, H. Cyto-Taxonomy and Phylogeny of the Oleaceae, Brittonia, Volume 5 (1945) no. 4, pp. 337-367 | DOI

[53] Tsagkogeorga, G.; Cahais, V.; Galtier, N. The Population Genomics of a Fast Evolver: High Levels of Diversity, Functional Constraint, and Molecular Adaptation in the Tunicate Ciona intestinalis, Genome Biology and Evolution, Volume 4 (2012) no. 8, pp. 852-861 | DOI

[54] Unver, T.; Wu, Z.; Sterck, L.; Turktas, M.; Lohaus, R.; Li, Z.; Yang, M.; He, L.; Deng, T.; Escalante, F. J.; Llorens, C.; Roig, F. J.; Parmaksiz, I.; Dundar, E.; Xie, F.; Zhang, B.; Ipek, A.; Uranbey, S.; Erayman, M.; Ilhan, E.; Badad, O.; Ghazal, H.; Lightfoot, D. A.; Kasarla, P.; Colantonio, V.; Tombuloglu, H.; Hernandez, P.; Mete, N.; Cetin, O.; Van Montagu, M.; Yang, H.; Gao, Q.; Dorado, G.; Van de Peer, Y. Genome of wild olive and the evolution of oil biosynthesis, Proceedings of the National Academy of Sciences, Volume 114 (2017) no. 44 | DOI

[55] Vassiliadis, C.; Saumitou-Laprade, P.; Lepart, J.; Viard, F. HIGH MALE REPRODUCTIVE SUCCESS OF HERMAPHRODITES IN THE ANDRODIOECIOUS PHILLYREA ANGUSTIFOLIA, Evolution, Volume 56 (2002) no. 7, pp. 1362-1373 | DOI

[56] Vernet, P.; Lepercq, P.; Billiard, S.; Bourceaux, A.; Lepart, J.; Dommée, B.; Saumitou‐Laprade, P. Evidence for the long‐term maintenance of a rare self‐incompatibility system in Oleaceae, New Phytologist, Volume 210 (2016) no. 4, pp. 1408-1417 | DOI

[57] Wallander, E.; Albert, V. A. Phylogeny and classification of Oleaceae based on rps16 and trnL-F sequence data, American Journal of Botany, Volume 87 (2000) no. 12, pp. 1827-1841 | DOI

[58] Wright, S. The distribution of self-sterility alleles in populations, Genetics, Volume 24 (1939) no. 4, pp. 538-552 | DOI

Cited by Sources: