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Divergence in flowering time is a major component contributing to reproductive isolation between two wild rice species (Oryza rufipogon and O. nivara)

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Abstract

It is of critical importance for our understanding of speciation process to determine the forms of reproductive isolation and their relative importance in species divergence. Oryza nivara and O. rufipogon are direct ancestors of Asian cultivated rice and a progenitor-daughter species pair. Investigating the reproductive isolation between them provides insights into plant speciation and helps understanding of the rice domestication. Here, we quantitatively measured the major components of reproductive isolation between the two species based on common garden and crossing experiments for three pairs of sympatric populations in Nepal, Cambodia and Laos. We revealed significant differences in the flowering times between species pairs, with O. nivara flowering much earlier than O. rufipogon. A very weak reduction in seed set but no reduction in F1 viability and fertility were detected for the crosses between species relative to those within species. Moreover, we detected asymmetrical compatibility between species and found that emasculation significantly decreased pollination success in O. nivara but not in O. rufipogon. Our study demonstrates that the divergence between O. nivara and O. rufipogon is maintained almost entirely by the difference in flowering times and suggests that differential flowering times contribute to both habitat preferences and reproductive isolation between species.

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References

  • Abbott, R.J. (2017). Plant speciation across environmental gradients and the occurrence and nature of hybrid zones. J Syst Evol 55, 238–258.

    Google Scholar 

  • Baack, E., Melo, M.C., Rieseberg, L.H., and Ortiz-Barrientos, D. (2015). The origins of reproductive isolation in plants. New Phytol 207, 968–984.

    Google Scholar 

  • Banaticla-Hilario, M.C.N., McNally, K.L., van den Berg, R.G., and Sackville Hamilton, N.R. (2013). Crossability patterns within and among Oryza series Sativae species from Asia and Australia. Genet Resour Crop Evol 60, 1899–1914.

    Google Scholar 

  • Barbier, P. (1989). Genetic variation and ecotypic differentiation in the wild rice species Oryza rufipogon. I. Population differentiation in life-history traits and isozymic loci. Jpn J Genet 64, 259–271.

    Google Scholar 

  • Briscoe Runquist, R.D., Chu, E., Iverson, J.L., Kopp, J.C., and Moeller, D. A. (2014). Rapid evolution of reproductive isolation between incipient outcrossing and selfing Clarkia species. Evolution 68, 2885–2900.

    Google Scholar 

  • Brys, R., Vanden Broeck, A., Mergeay, J., and Jacquemyn, H. (2014). The contribution of mating system variation to reproductive isolation in two closely related Centaurium species (Gentianaceae) with a generalized flower morphology. Evolution 68, 1281–1293.

    Google Scholar 

  • Burton, R.S., Pereira, R.J., and Barreto, F.S. (2013). Cytonuclear genomic interactions and hybrid breakdown. Annu Rev Ecol Evol Syst 44, 281–302.

    Google Scholar 

  • Cai, H.W., Wang, X.K., and Morishima H. (2004). Comparison of population genetic structures of common wild rice (Oryza rufipogon Griff.), as revealed by analyses of quantitative traits, allozymes, and RFLPs. Heredity 92, 409–417.

    CAS  Google Scholar 

  • Cai, Z., Zhou, L., Ren, N.N., Xu, X., Liu, R., Huang, L., Zheng, X.M., Meng, Q.L., Du, Y.S., Wang, M.X., et al. (2019). Parallel speciation of wild rice associated with habitat shifts. Mol Biol Evol 36, 875–889.

    CAS  Google Scholar 

  • Chu, Y.E., Morishima, H., and Oka, H.I. (1969). Reproductive barriers distributed in cultivated rice species and their wild relatives. Jpn J Genet 44, 207–223.

    Google Scholar 

  • Coyne, J.A., and Orr, H.A. (2004). Speciation (Sunderland: Sinauer Associates, Inc.).

    Google Scholar 

  • Delph, L.F. (2019). Pollen competition is the mechanism underlying a variety of evolutionary phenomena in dioecious plants. New Phytol 224, 1075–1079.

    Google Scholar 

  • Grillo, M.A., Li, C., Fowlkes, A.M., Briggeman, T.M., Zhou, A., Schemske, D.W., and Sang, T. (2009). Genetic architecture for the adaptive origin of annual wild rice, Oryza nivara. Evolution 63, 870–883.

    CAS  Google Scholar 

  • Hey, J. (2006). Recent advances in assessing gene flow between diverging populations and species. Curr Opin Genets Dev 16, 592–596.

    CAS  Google Scholar 

  • Hipperson, H., Dunning, L.T., Baker, W.J., Butlin, R.K., Hutton, I., Papadopulos, A.S.T., Smadja, C.M., Wilson, T.C., Devaux, C., and Savolainen, V. (2016). Ecological speciation in sympatric palms: 2. Pre-and post-zygotic isolation. J Evol Biol 29, 2143–2156.

    CAS  Google Scholar 

  • Huang, P., and Schaal, B.A. (2012). Association between the geographic distribution during the last glacial maximum of Asian wild rice, Oryza rufipogon (Poaceae), and its current genetic variation. Am J Bot 99, 1866–1874.

    Google Scholar 

  • Kuroda, Y., Sato, Y.I., Bounphanousay, C., Kono, Y., and Tanaka, K. (2007). Genetic structure of three Oryza AA genome species (O. rufipogon, O. nivara and O. sativa) as assessed by SSR analysis on the Vientiane Plain of Laos. Conserv Genet 8, 149–158.

    CAS  Google Scholar 

  • Li, G., Jin, J., Zhou, Y., Bai, X., Mao, D., Tan, C., Wang, G., and Ouyang, Y. (2019). Genome-wide dissection of segregation distortion using multiple inter-subspecific crosses in rice. Sci China Life Sci 62, 507–516.

    Google Scholar 

  • Liu, R., Zheng, X.M., Zhou, L., Zhou, H.F., and Ge, S. (2015). Population genetic structure of Oryza rufipogon and Oryza nivara: implications for the origin of O. nivara. Mol Ecol 24, 5211–5228.

    Google Scholar 

  • Lowry, D.B., Modliszewski, J.L., Wright, K.M., Wu, C.A., and Willis, J.H. (2008). The strength and genetic basis of reproductive isolating barriers in flowering plants. Phil Trans R Soc B 363, 3009–3021.

    Google Scholar 

  • Lu, B.R. (1996). A report on collecting of wild Oryza species in Lao PDR and Cambodia. (Los Banos: International Rice Research Institute).

    Google Scholar 

  • Lu, B.R. (1998). A report on NARC-IRRI cooperative collection of wild Oryza species in Nepal. (Los Banos: International Rice Research Institute).

    Google Scholar 

  • Martin, H., Touzet, P., Dufay, M., Godé, C., Schmitt, E., Lahiani, E., Delph, L.F., and Van Rossum, F. (2017). Lineages of Silene nutans developed rapid, strong, asymmetric postzygotic reproductive isolation in allopatry. Evolution 71, 1519–1531.

    CAS  Google Scholar 

  • Martin, N.H., and Willis, J.H. (2007). Ecological divergence associated with mating system causes nearly complete reproductive isolation between sympatric Mimulus species. Evolution 61, 68–82.

    Google Scholar 

  • Mayr, E. (1942). Systematics and the origin of species (New York: Columbia University Press).

    Google Scholar 

  • Morishima, H. (1985). Habitat, genetic structure and dynamics of perennial and annual populations of the Asian wild rice Oryza perennis. In Genetic Differentiation and Dispersal in Plants, P. Jacquard, G. Heim, and J. Antonovics, eds. (Berlin: Springe-Verlag).

  • Morishima, H., Chang, W.T., and Oka, H.I. (1961). Directions of differentiation in populations of wild rice, Oryza perennis and O. sativa f. spontanea. Evolution 15, 326–339.

    Google Scholar 

  • Morishima, H., Sano, Y., and Oka, H.I. (1984). Differentiation of perennial and annual types due to habitat conditions in the wild rice Oryza perennis. Pl Syst Evol 144, 119–135.

    Google Scholar 

  • Naredo, M.E.B., Juliano, A.B., Lu, B.R., and Jackson, M.T. (1997). Hybridization of AA genome rice species from Asia and Australia I. Genet Resources Crop Evol 44, 17–23.

    Google Scholar 

  • Naredo, M.E.B., Juliano, A.B., Lu, B.R., and Jackson, M.T. (1998). Taxonomic status of Oryza glumaepatula Steud. Genet Resources Crop Evol 45, 205–214.

    Google Scholar 

  • Nezu, M., Katayama, T.C., and Kihara, H. (1960). Genetic study of the genus Oryza. I. Crossability and chromosomal affinity among 17 species. Rep Kihara Inst biol Res, 1–11.

  • Nosil, P. (2012). Ecological Speciation (Oxford: Oxford University Press).

    Google Scholar 

  • Oka, H.I., and Morishima, H. (1967). Variations in the breeding systems of a wild rice, Oryza perennis. Evolution 21, 249–258.

    Google Scholar 

  • Ostevik, K.L., Andrew, R.L., Otto, S.P., and Rieseberg, L.H. (2016). Multiple reproductive barriers separate recently diverged sunflower ecotypes. Evolution 70, 2322–2335.

    Google Scholar 

  • Pereira, M.R., Ledent, A., Mardulyn, P., Zartman, C.E., and Vanderpoorten, A. (2019). Maintenance of genetic and morphological identity in two sibling Syrrhopodon species (Calymperaceae, Bryopsida) despite extensive introgression. J Syst Evol 57, 395–403.

    Google Scholar 

  • Pianka, E.R. (1970). On r- and K-Selection. Am Natist 104, 592–597.

    Google Scholar 

  • Ramsey, J., Bradshaw, H.D., and Schemske, D.W. (2003). Components of reproductive isolation between the monkey flowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution 57, 1520–1534.

    Google Scholar 

  • Ren, N.N. (2019). Studies on the phenotypic variaiton and its evolutioanry significance of wild rice Oryza rufipogon and O. nivara. (Beijing: Institute of Botany, the Chinese Academy of Sciences).

    Google Scholar 

  • Richards, T.J., Walter, G.M., McGuigan, K., and Ortiz-Barrientos, D. (2016). Divergent natural selection drives the evolution of reproductive isolation in an Australian wildflower. Evolution 70, 1993–2003.

    Google Scholar 

  • Rieseberg, L.H., and Carney, S.E. (1998). Plant hybridization. New Phytol 140, 599–624.

    Google Scholar 

  • Samal, R., Roy, P.S., Sahoo, A., Kar, M.K., Patra, B.C., Marndi, B.C., and Gundimeda, J.N.R. (2018). Morphological and molecular dissection of wild rices from eastern India suggests distinct speciation between O. rufipogon and O. nivara populations. Sci Rep 8, 2773.

    Google Scholar 

  • Sang, T., and Ge, S. (2007a). Genetics and phylogenetics of rice domestication. Curr Opin Genets Dev 17, 533–538.

    CAS  Google Scholar 

  • Sang, T., and Ge, S. (2007b). The puzzle of rice domestication. J Integrative Plant Biol 49, 760–768.

    CAS  Google Scholar 

  • Seehausen, O., Butlin, R.K., Keller, I., Wagner, C.E., Boughman, J.W., Hohenlohe, P.A., Peichel, C.L., Saetre, G.P., Bank, C., Brännström, A., et al. (2014). Genomics and the origin of species. Nat Rev Genet 15, 176–192.

    CAS  Google Scholar 

  • Sharma, S.D., and Shastry, S.V.S. (1965). Taxonomic studies in genus Oryza L. III. O. rufipogon Griff. sensu stricto and O. nivara Sharma et Shastry nom. nov. Indian J Genet PL BR 25, 157–167.

    Google Scholar 

  • Sobel, J.M., and Chen, G.F. (2014). Unification of methods for estimating the strength of reproductive isolation. Evolution 68, 1511–1522.

    Google Scholar 

  • Sobel, J.M., Chen, G.F., Watt, L.R., and Schemske, D.W. (2010). The biology of speciation. Evolution 64, 295–315.

    Google Scholar 

  • Sobel, J.M., and Streisfeld, M.A. (2015). Strong premating reproductive isolation drives incipient speciation in Mimulus aurantiacus. Evolution 69, 447–461.

    Google Scholar 

  • Suni, S.S., and Hopkins, R. (2018). The relationship between postmating reproductive isolation and reinforcement in Phlox. Evolution 72, 1387–1398.

    Google Scholar 

  • Tiffin, P., Olson, M.S., and Moyle, L.C. (2001). Asymmetrical crossing barriers in angiosperms. Proc R Soc Lond B 268, 861–867.

    CAS  Google Scholar 

  • Vaughan, D.A. (1989). The genus Oryza L. current status of taxonomy. IRRI Res Pap Ser 138, 21.

    Google Scholar 

  • Vaughan, D.A., Lu, B.R., and Tomooka, N. (2008). The evolving story of rice evolution. Plant Sci 174, 394–408.

    CAS  Google Scholar 

  • Via, S. (2009). Natural selection in action during speciation. Proc Natl Acad Sci USA 106, 9939–9946.

    CAS  Google Scholar 

  • Widmer, A., Lexer, C., and Cozzolino, S. (2009). Evolution of reproductive isolation in plants. Heredity 102, 31–38.

    CAS  Google Scholar 

  • Xie, Y., Shen, R., Chen, L., and Liu, Y.G. (2019). Molecular mechanisms of hybrid sterility in rice. Sci China Life Sci 62, 737–743.

    Google Scholar 

  • Zheng, X.M., and Ge, S. (2010). Ecological divergence in the presence of gene flow in two closely related Oryza species (Oryza rufipogon and O. nivara). Mol Ecol 19, 2439–2454.

    Google Scholar 

  • Zhou, H.F., Zheng, X.M., Wei, R.X., Second, G., Vaughan, D.A., and Ge, S. (2008). Contrasting population genetic structure and gene flow between Oryza rufipogon and Oryza nivara. Theor Appl Genet 117, 1181–1189.

    CAS  Google Scholar 

  • Zhou, L. (2019). Studies on flowering time variation and Hd1 gene in wild rice Oryza rufipogon and O. nivara. (Beijing: Institute of Botany, the Chinese Academy of Sciences).

    Google Scholar 

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Acknowledgements

We thank Bao-Rong Lu, Wen-Li Chen, Cheng-Bin Chen, Hua-Zhong Zeng, Yun-Tao Liang for their helps in the field surveys and common garden experiment. We also thank the International Rice Research Institute (Los Banos, Philippines) for providing seed samples. This work was supported by the National Natural Science Foundation of China (91731301), the grants from the Chinese Academy of Sciences (XDB31000000, XDA08020103) and CAS/SAFEA International Partnership Program for Creative Research Teams.

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Correspondence to Song Ge.

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Supporting Information

Figure S1 Variation of first heading of three pairs of O. rufipogon (blue) and O. nivara (red) populations from 2011 to 2013 in the common garden experiment. Boxes and horizontal bars represent the central 50% and median of heading dates, respectively. Dots represent the outliers beyond 1.5 times the interquartile range. Numbers of individuals (O. rufipogon/O. nivara) that were observed are in parentheses.

Table S1 Information on the O. rufipogon and O. nivara populations used in this study. N, number of individuals sampled

Table S2 Flowering phenology of three pairs of O. rufipogon and O. nivara populations in the common garden expriment in three consecutive years in Guanxi, China

Table S3 Summary of different types of crosses for six O. rufipogon and O. nivara populations

Table S4 Seed set of the self-pollinations with and without emasculation. em, emasculation; ns, no significance; **, P < 0.01; ***, P < 0.001

Table S5 Significant tests for the seed sets between different types of crosses. ns, no significance; ***, P<0.001

Table S6 Significant tests for the viability of F1 hybrids between different types of crosses. Level of significances is listed in the following order: germination rate, seedling survival rate and total survival rate. ns, no significance; *, P<0.05; ***, P<0.001

Table S7 Viability and fertility of the F1 hybrids between pairs of species populations. *, this index is the absolute contribution (AC) of germination rate (AC1) and seedling survival (AC2) to the total isolation, and zero represents a higher fitness of F1 hybrids relative to their parents

Table S8 Design of crossing experiments. Population codes are the same to those in Table S1 in Supporting Information. Numbers of crosses are in the parentheses

The supporting information is available online at http://life.scichina.com and https://link.springer.com. The supporting materials are published as submitted, without typesetting or editing. The responsibility for scientific accuracy and content remains entirely with the authors.

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Xu, X., Meng, QL., Geng, MF. et al. Divergence in flowering time is a major component contributing to reproductive isolation between two wild rice species (Oryza rufipogon and O. nivara). Sci. China Life Sci. 63, 1714–1724 (2020). https://doi.org/10.1007/s11427-019-1678-6

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