Genetic control of flowering in greater yam (Dioscorea alata L.)
Tóm tắt
Greater yam (Dioscorea alata L.) is a major tropical and subtropical staple crop cultivated for its starchy tubers. Breeding of this dioecious species is hampered by its erratic flowering, yet little is currently known on the genetic determinism of its sexual reproduction. Here we used a genome-wide association approach and identified a major genetic barrier to reproduction in yam on chromosome 1, as represented by two candidate genes. A deleterious effect on male fitness could be hypothesized considering the involvement of these two genes in male reproduction and the low frequency of this non-flowering dominant allele within the male genepool. We also extended the hypothesis of a XX/XY sex-determination system located on chromosome 6 in D. alata to encompass most of the species diversity. Moreover, a kompetitive allele-specific PCR (KASPar) marker was designed and validated that enables accurate cultivar sex estimation. The reconstruction of chromosome 6 associated with the detection of highly putative structural variations confirmed the possible involvement of a major part of the chromosome. The findings of this study, combined with proper estimation of accession ploidy levels to avoid endosperm incompatibility issues, could facilitate the design of future promising parental combinations in D. alata breeding programs. Moreover, the discovery of this genetic barrier to reproduction opens new avenues for gaining insight into yam reproductive biology and diversification.
Tài liệu tham khảo
Witcombe JR, Virk DS. Number of crosses and population size for participatory and classical plant breeding. Euphytica. 2001;122(3):451–62. https://doi.org/10.1023/A:1017524122821.
Allen AM, Hiscock SJ Evolution and Phylogeny of Self-Incompatibility Systems in Angiosperms. In: Self-Incompatibility in Flowering Plants. Berlin, Heidelberg: Springer; 2008. https://doi.org/10.1007/978-3-540-68486-2_4.
Levy YY, Dean C. The transition to flowering. Plant Cell. 1998;10(12):1973–89. https://doi.org/10.1105/tpc.10.12.1973.
Meyer RS, Purugganan MD. Evolution of crop species: genetics of domestication and diversification. Nat Rev Genet. 2013;14(12):840–52. https://doi.org/10.1038/nrg3605.
Hardigan MA, Laimbeer FPE, Newton L, Crisovan E, Hamilton JP, Vaillancourt B, et al. Genome diversity of tuber-bearing Solanum uncovers complex evolutionary history and targets of domestication in the cultivated potato. Proc Natl Acad Sci. 2017;114(46):E9999–10008. https://doi.org/10.1073/pnas.1714380114.
Barrett SCH. Influences of clonality on plant sexual reproduction. Proc Natl Acad Sci. 2015;112(29):8859–66. https://doi.org/10.1073/pnas.1501712112.
Viruel J, Segarra-Moragues JG, Raz L, Forest F, Wilkin P, Sanmartin I, et al. Late cretaceous-early Eocene origin of yams (Dioscorea, Dioscoreaceae) in the Laurasian Palaearctic and their subsequent Oligocene-Miocene diversification. J Biogeogr. 2016;43(4):750–62. https://doi.org/10.1111/jbi.12678.
Arnau G, Nemorin A, Maledon E, Abraham K. Revision of ploidy status of Dioscorea alata L. (Dioscoreaceae) by cytogenetic and microsatellite segregation analysis. Theor Appl Genet. 2009;118(7):1239–49. https://doi.org/10.1007/s00122-009-0977-6.
Sharif BM, Burgarella C, Cormier F, Mournet P, Causse S, Van KN, et al. Genome-wide genotyping elucidates the geographical diversification and dispersal of the polyploid and clonally propagated yam (Dioscorea alata). Ann Bot. 2020;126(6):1029–38. https://doi.org/10.1093/aob/mcaa122.
Abraham K, Nair PG. Polyploidy and sterility in relation to sex in Dioscoreaalata L. (Dioscoreaceae). Genetica. 1991;83(2):93–7. https://doi.org/10.1007/BF00058525.
Kouakou AM, Yao GF, Brice Dibi KE, Mahyao A, Lopez-Montes A, Essis BS, et al. Yam Cropping System in Cote d’Ivoire: Current Practices and Constraints. Eur Sci J ESJ. 2019;15. https://doi.org/10.19044/esj.2019.v15n30p278.
Abraham K, Nemorin A, Lebot V, Arnau G. Meiosis and sexual fertility of autotetraploid clones of greater yam Dioscorea alata L. Genet Resour Crop Evol. 2013;60(3):819–23. https://doi.org/10.1007/s10722-013-9973-4.
Nemorin A, David J, Maledon E, Nudol E, Dalon J, Arnau G. Microsatellite and flow cytometry analysis to help understand the origin of Dioscorea alata polyploids. Ann Bot. 2013;112(5):811–9. https://doi.org/10.1093/aob/mct145.
Lebot V, Abraham K, Kaoh J, Rogers C, Molisalé T. Development of anthracnose resistant hybrids of the greater yam (Dioscorea alata L.) and interspecific hybrids with D. nummularia lam. Genet Resour Crop Evol. 2019;66(4):871–83. https://doi.org/10.1007/s10722-019-00756-y.
Ehounou AE, Kouakou AM, N’zi JC, Dibi KEB, Bakayoko Y, Essis BS, et al. Production of Hybrid Seeds by Intraspecific Crossing in Yam Dioscorea alata L, vol. 8; 2018. p. 11.
Cormier F, Lawac F, Maledon E, Gravillon M-C, Nudol E, Mournet P, et al. A reference high-density genetic map of greater yam (Dioscorea alata L.). Theor Appl Genet. 2019;132(6):1733–44. https://doi.org/10.1007/s00122-019-03311-6.
Malapa R, Arnau G, Noyer JL, Lebot V. Genetic diversity of the greater yam (Dioscorea alata L.) and relatedness to D. nummularia Lam. and D. transversa Br. as revealed with AFLP markers. Genet Resour Crop Evol. 2005;52:919–29. https://doi.org/10.1007/s10722-003-6122-5.
Tamiru M, Natsume S, Takagi H, White B, Yaegashi H, Shimizu M, et al. Genome sequencing of the staple food crop white Guinea yam enables the development of a molecular marker for sex determination. BMC Biol. 2017;15(1):86. https://doi.org/10.1186/s12915-017-0419-x.
Martin FW. Sex ratio and sex determination in Dioscorea. J Hered. 1966;57(3):95–9. https://doi.org/10.1093/oxfordjournals.jhered.a107485.
Terauchi R, Kahl G. Mapping of the Dioscorea tokoro genome: AFLP markers linked to sex, vol. 42; 1999. p. 11.
Girma G, Natsume S, Carluccio AV, Takagi H, Matsumura H, Uemura A, et al. Identification of candidate flowering and sex genes in white Guinea yam ( D. rotundata Poir .) by SuperSAGE transcriptome profiling. preprint. Plant Biol. 2019. https://doi.org/10.1101/626200.
Abraham K, Nair PG. Floral biology and artificial pollination in Dioscorea alata L. Euphytica1990;48:45–51.
Malumbres M. Cyclin-dependent kinases. Genome Biol. 2014;15(6):122. https://doi.org/10.1186/gb4184.
Fujita M, Horiuchi Y, Ueda Y, Mizuta Y, Kubo T, Yano K, et al. Rice expression atlas in reproductive development. Plant Cell Physiol. 2010;51(12):2060–81. https://doi.org/10.1093/pcp/pcq165.
Magwanga RO, Lu P, Kirungu JN, Cai X, Zhou Z, Wang X, et al. Whole genome analysis of Cyclin dependent kinase (CDK) gene family in cotton and functional evaluation of the role of CDKF4 gene in drought and salt stress tolerance in plants. Int J Mol Sci. 2018;19(9):2625. https://doi.org/10.3390/ijms19092625.
Kelley DR. E3 ubiquitin ligases: key regulators of hormone signaling in plants. Mol Cell Proteomics MCP. 2018;17(6):1047–54. https://doi.org/10.1074/mcp.MR117.000476.
Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, et al. A gene expression map of Arabidopsis thaliana development. Nat Genet. 2005;37(5):501–6. https://doi.org/10.1038/ng1543.
Chen Y, Fokar M, Kang M, Chen N, Allen RD, Chen Y. Phosphorylation of Arabidopsis SINA2 by CDKG1 affects its ubiquitin ligase activity. BMC Plant Biol. 2018;18(1):147. https://doi.org/10.1186/s12870-018-1364-8.
Zheng T, Nibau C, Phillips DW, Jenkins G, Armstrong SJ, Doonan JH. CDKG1 protein kinase is essential for synapsis and male meiosis at high ambient temperature in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2014;111(6):2182–7. https://doi.org/10.1073/pnas.1318460111.
Bao Y, Wang C, Jiang C, Pan J, Zhang G, Liu H, et al. The tumor necrosis factor receptor-associated factor (TRAF)-like family protein SEVEN IN ABSENTIA 2 (SINA2) promotes drought tolerance in an ABA-dependent manner in Arabidopsis. New Phytol. 2014;202(1):174–87. https://doi.org/10.1111/nph.12644.
Slatkin M. Linkage disequilibrium — understanding the evolutionary past and mapping the medical future. Nat Rev Genet. 2008;9(6):477–85. https://doi.org/10.1038/nrg2361.
Kumar S, Kumari R, Sharma V. Genetics of dioecy and causal sex chromosomes in plants. J Genet. 2014;93(1):241–77. https://doi.org/10.1007/s12041-014-0326-7.
Otto SP, Pannell JR, Peichel CL, Ashman T-L, Charlesworth D, Chippindale AK, et al. About PAR: the distinct evolutionary dynamics of the pseudoautosomal region. Trends Genet. 2011;27(9):358–67. https://doi.org/10.1016/j.tig.2011.05.001.
Vandenbroucke H, Mournet P, Vignes H, Chaïr H, Malapa R, Duval MF, et al. Somaclonal variants of taro (Colocasia esculenta Schott) and yam (Dioscorea alata L.) are incorporated into farmers’ varietal portfolios in Vanuatu. Genet Resour Crop Evol. 2016;63:495–511.
Chen ZJ. Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant Polyploids. Annu Rev Plant Biol. 2007;58(1):377–406. https://doi.org/10.1146/annurev.arplant.58.032806.103835.
Hyde PT, Guan X, Abreu V, Setter TL. The anti-ethylene growth regulator silver thiosulfate (STS) increases flower production and longevity in cassava (Manihot esculenta Crantz). Plant Growth Regul. 2020;90(3):441–53. https://doi.org/10.1007/s10725-019-00542-x.
Hamadina E. Duration of tuber dormancy in yam Dioscorea rotundata: effect of plant growth regulators and its relationship with tuber age. J Adv Biol. 2015;7:1230–7.
Risterucci A-M, Hippolyte I, Perrier X, Xia L, Caig V, Evers M, et al. Development and assessment of diversity arrays technology for high-throughput DNA analyses in Musa. Theor Appl Genet. 2009;119(6):1093–103. https://doi.org/10.1007/s00122-009-1111-5.
Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One. 2011;6(5). https://doi.org/10.1371/journal.pone.0019379.
Garsmeur O, Droc G, Antonise R, Grimwood J, Potier B, Aitken K, et al. A mosaic monoploid reference sequence for the highly complex genome of sugarcane. Nat Commun. 2018;9(1):2638. https://doi.org/10.1038/s41467-018-05051-5.
Knaus BJ, Grünwald NJ. vcfr: a package to manipulate and visualize variant call format data in R. Mol Ecol Resour. 2017;17(1):44–53. https://doi.org/10.1111/1755-0998.12549.
Yu JM, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, et al. A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet. 2006;38(2):203–8. https://doi.org/10.1038/ng1702.
Butler DG, Cullis BR, Gilmour AR, Gogel BJ, Thompson R. ASReml estimates variance components under a general linear. VSN International Ltd, Hemel Hempstead, HP1 1ES, UK; 2018.
Cormier F, Mournet P, Causse S, Arnau G, Maledon E, Gomez R-M, et al. Development of a cost-effective single nucleotide polymorphism genotyping array for management of greater yam germplasm collections. Ecol Evol. 2019;9:5617–36. https://doi.org/10.1002/ece3.5141.
Dereeper A, Homa F, Andres G, Sempere G, Sarah G, Hueber Y, et al. SNiPlay3: a web-based application for exploration and large scale analyses of genomic variations. Nucleic Acids Res. 2015;43(Web Server issue):W295–300.
Sarah G, Homa F, Pointet S, Contreras S, Sabot F, Nabholz B, et al. A large set of 26 new reference transcriptomes dedicated to comparative population genomics in crops and wild relatives. Mol Ecol Resour. 2017;17(3):565–80. https://doi.org/10.1111/1755-0998.12587.
Van Ooijen JW. JoinMap 4.1, Software for the calculation of genetic linkage maps in experimental populations of diploid species. Kyazma BV, Wageningen, Netherlands; 2012.
Martin G, Carreel F, Coriton O, Hervouet C, Cardi C, Derouault P, et al. Evolution of the Banana genome (Musa acuminata) is impacted by large chromosomal translocations. Mol Biol Evol. 2017;34(9):2140–52. https://doi.org/10.1093/molbev/msx164.
Gu Z, Gu L, Eils R, Schlesner M, Brors B. Circlize implements and enhances circular visualization in R. Bioinformatics. 2014;30(19):2811–2. https://doi.org/10.1093/bioinformatics/btu393.
Langmead B, Salzberg SL. Fast gapped-read alignment with bowtie 2. Nat Methods. 2012;9(4):357–9. https://doi.org/10.1038/nmeth.1923.