Genetic and Geographic Patterns of Duplicate DPL Genes Causing Genetic Incompatibility Within Rice: Implications for Multiple Domestication Events in Rice
Received date: 2020-04-07
Accepted date: 2020-06-20
Online published: 2021-01-28
Strong genetic incompatibilities exist between two primary rice subspecies, indica and japonica. However, the wild ancestors of rice, O. nivara Sharma et Shastry and O. rufipogon Griff., are genetically compatible. How this genetic incompatibility became established has not been clearly elucidated. To provide insights into the process, we analyzed a pair of hybrid sterility genes in rice, DOPPELGANGER 1 (DPL1) and DOPPELGANGER 2 (DPL2). Either of the two loci can have one defective allele (DPL1- and DPL2-). Hybrid pollen carrying both DPL1- and DPL2- alleles is sterile. To explore the origination of DPL1- and DPL2-, we sequenced the DPL1 and DPL2 genes of 811 individual plants, including Oryza sativa (132), O. nivara (296) and O. rufipogon (383). We then obtained 20 DPL1 and 34 DPL2 sequences of O. sativa from online databases. Using these sequences, we analyzed the genetic and geographic distribution patterns of DPL genes in modern rice and its wild ancestors. Compared with the ancestral populations, DPL1- and DPL2- showed reduced diversity but increased frequency in modern rice. We speculated that the diversity reduction was due to a historic genetic bottleneck, and the frequency had likely increased because the defective alleles were preferred following this artificial selection. Such results indicated that standing variances in ancestral lines can lead to severe incompatibilities among descendants. Haplotype analysis indicated that the DPL1- haplotype of rice emerged from an O. nivara population in India, whereas the DPL2- haplotype emerged from O. rufipogon in South China. Hence, the evolutionary history of DPLs conforms to the presumed multiple domestication events of modern rice.
Key words： rice; DPL gene; domestication; genetic incompatibility; phylogeography
Xun Xu, Song Ge, Fumin Zhang . Genetic and Geographic Patterns of Duplicate DPL Genes Causing Genetic Incompatibility Within Rice: Implications for Multiple Domestication Events in Rice[J]. Rice Science, 2021 , 28(1) : 58 -68 . DOI: 10.1016/j.rsci.2020.11.007
| [1] | Bandelt H J, Forster P, Rohl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol, 16(1): 37-48 |
| [2] | Bank C, Burger R, Hermisson J. 2012. The limits to parapatric speciation: Dobzhansky-Muller incompatibilities in a Continent- Island Model. Genetics, 191(3): 845-345 |
| [3] | 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, Geng M F, Chen W L, Jing C Y, Zou X H, Guo J, Chen C B, Zeng H Z, Liang Y T, Wei X H, Guo Y L, Zhou H F, Zhang F M, Ge S. 2019. Parallel speciation of wild rice associated with habitat shifts. Mol Biol Evol, 36(5): 875-889 |
| [4] | Chen J J, Ding J H, Ouyang Y D, Du H Y, Yang J Y, Cheng K, Zhao J, Qiu S Q, Zhang X L, Yao J L, Liu K D, Wang L, Xu C G, Li X H, Xue Y B, Xia M, Ji Q, Lu J F, Xu M L, Zhang Q F. 2008. A triallelic system of S5 is a major regulator of the reproductive barrier and compatibility of indica-japonica hybrids in rice. Proc Natl Acad Sci USA, 105(32): 11436-11441 |
| [5] | Civan P, Craig H, Cox C J, Brown T A. 2015. Three geographically separate domestications of Asian rice. Nat Plants, 1(11): 1-5 |
| [6] | Corbett-Detig R B, Zhou J, Clark A G, Hartl D L, Ayroles J F. 2013. Genetic incompatibilities are widespread within species. Nature, 504: 135-137 |
| [7] | Craig S M, Reagon M, Resnick L E, Caicedo A L. 2014. Allele distributions at hybrid incompatibility loci facilitate the potential for gene flow between cultivated and weedy rice in the US. PLoS One, 9(1): e86647. |
| [8] | Cutter A D. 2012. The polymorphic prelude to Bateson-Dobzhansky- Muller incompatibilities. Trends Ecol Evol, 27(4): 209-218 |
| [9] | Du H, Ouyang Y, Zhang C, Zhang Q. 2011. Complex evolution of S5, a major reproductive barrier regulator, in the cultivated rice Oryza sativa and its wild relatives. New Phytol, 191(1): 275-287 |
| [10] | Garris A J, Tai T H, Coburn J, Kresovich S, McCouch S. 2005. Genetic structure and diversity in Oryza sativa L. Genetics, 169(3): 1631-1638 |
| [11] | Gavrilets S. 1997. Hybrid zones with Dobzhansky-type epistatic selection. Evolution, 51(4): 1027-1035 |
| [12] | Hall T A. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser, 41: 95-98 |
| [13] | Huang X H, Kurata N, Wei X H, Wang Z X, Wang A, Zhao Q, Zhao Y, Liu K Y, Lu H Y, Li W J, Guo Y L, Lu Y Q, Zhou C C, Fan D L, Weng Q J, Zhu C R, Huang T, Zhang L, Wang Y C, Feng L, Furuumi H, Kubo T, Miyabayashi T, Yuan X P, Xu Q, Dong G J, Zhan Q L, Li C Y, Fujiyama A, Toyoda A, Lu T, Feng Q, Qian Q, Li J Y, Han B. 2012. A map of rice genome variation reveals the origin of cultivated rice. Nature, 490: 497-501 |
| [14] | Khush G S. 1997. Origin, dispersal, cultivation and variation of rice. Plant Mol Biol, 35(1): 25-34 |
| [15] | Kovach M J, Sweeney M T, McCouch S R. 2007. New insights into the history of rice domestication. Trends Genet, 23(11): 578-587 |
| [16] | Li G W, Li X T, Wang Y, Mi J M, Xing F, Zhang D H, Dong Q Y, Li X H, Xiao J H, Zhang Q F, Ouyang Y D. 2017. Three representative inter and intra-subspecific crosses reveal the genetic architecture of reproductive isolation in rice. Plant J, 92(3): 349-362 |
| [17] | Librado P, Rozas J. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25(11): 1451-1452 |
| [18] | Lindtke D, Buerkle C A.2015. The genetic architecture of hybrid incompatibilities and their effect on barriers to introgression in secondary contact. Evolution, 69(8): 1987?2004. |
| [19] | Liu R, Zheng X M, Zhou L, Zhou H F, Ge S. 2015. Population genetic structure of Oryza rufipogon and Oryza nivara: Implications for the origin of O. nivara. Mol Ecol, 24(20): 5211-5228 |
| [20] | Londo J P, Chiang Y C, Hung K H, Chiang T Y, Schaal B A. 2006. Phylogeography of Asian wild rice, Oryza rufipogon, reveals multiple independent domestications of cultivated rice, Oryza sativa. Proc Natl Acad Sci USA, 103(25): 9578-9583 |
| [21] | Long Y M, Zhao L F, Niu B X, Su J, Wu H, Chen Y L, Zhang Q Y, Guo J X, Zhuang C X, Mei M T, Xia J X, Wang L, Wu H B, Liu Y G. 2008. Hybrid male sterility in rice controlled by interaction between divergent alleles of two adjacent genes. Proc Natl Acad Sci USA, 105(48): 18871-18876 |
| [22] | Mizuta Y, Harushima Y, Kurata N. 2010. Rice pollen hybrid incompatibility caused by reciprocal gene loss of duplicated genes. Proc Natl Acad Sci USA, 107(47): 20417-20422 |
| [23] | Morishima H, Sano Y, Oka H.1992. Evolutionary Studies in Cultivated Rice and Its Wild Relatives. Oxford: Oxford University Press. |
| [24] | Oka H I. 1988. Origin of Cultivated Rice. Amsterdam, Holland: Elsevier. |
| [25] | Ouyang Y D, Liu Y G, Zhang Q F. 2010. Hybrid sterility in plant: Stories from rice. Curr Opin Plant Biol, 13(2): 186-192 |
| [26] | Ouyang Y D, Zhang Q F. 2013. Understanding reproductive isolation based on the rice model. Annu Rev Plant Biol, 64(1): 111-135 |
| [27] | Ouyang Y D, Zhang Q F. 2018. The molecular and evolutionary basis of reproductive isolation in plants. J Genet Genom, 45(11): 613-620 |
| [28] | Polzin T, Daneshmand S V. 2003. On Steiner trees and minimum spanning trees in hypergraphs. Oper Res Lett, 31(1): 12-20 |
| [29] | Rieseberg L H, Blackman B K. 2010. Speciation genes in plants. Ann Bot, 106(3): 439-455 |
| [30] | Sang T, Ge S. 2007. The puzzle of rice domestication. J Integr Plant Biol, 49(6): 760-768 |
| [31] | Seidel H S, Rockman M V, Kruglyak L. 2008. Widespread genetic incompatibility in C. elegans maintained by balancing selection. Science, 319: 589-594 |
| [32] | Shen R X, Wang L, Liu X P, Wu J, Jin W W, Zhao X C, Xie X R, Zhu Q L, Tang H W, Li Q, Chen L T, Liu Y G. 2017. Genomic structural variation-mediated allelic suppression causes hybrid male sterility in rice. Nat Commun, 8: 1310. |
| [33] | Shuker D M, Underwood K, King T M, Butlin R K. 2005. Patterns of male sterility in a grasshopper hybrid zone imply accumulation of hybrid incompatibilities without selection. Proc R Soc Lond Ser B-Biol Sci, 272: 2491-2497 |
| [34] | Sicard A, Kappel C, Josephs E B, Lee Y W, Marona C, Stinchcombe J R, Wright S I, Lenhard M. 2015. Divergent sorting of a balanced ancestral polymorphism underlies the establishment of gene-flow barriers inCapsella. Nat Commun, 6: 7960. |
| [35] | Sweeney M, McCouch S. 2007. The complex history of the domestication of rice. Ann Bot, 100(5): 951-957 |
| [36] | Tajima F. 1989. Statistical-method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123(3): 585-595 |
| [37] | Thompson J D, Gibson T J, Plewniak F, Jeanmougin F, Higgins D G. 1997. The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res, 25(24): 4876-4882 |
| [38] | Vaughan D A, Lu B R, Tomooka N. 2008. The evolving story of rice evolution. Plant Sci, 174(4): 394-408 |
| [39] | Wang C H, Zheng X M, Xu Q, Yuan X P, Huang L, Zhou H F, Wei X H, Ge S. 2014. Genetic diversity and classification of Oryza sativa with emphasis on Chinese rice germplasm. Heredity, 112: 489-496 |
| [40] | Woerner A E, Cox M P, Hammer M F. 2007. Recombination- filtered genomic datasets by information maximization. Bioinformatics, 23(14): 1851-1853 |
| [41] | Xie Y Y, Shen R X, Chen L T, Liu Y G. 2019. Molecular mechanisms of hybrid sterility in rice. Sci China Life Sci, 62(6): 737-743 |
| [42] | Yamagata Y, Yamamoto E, Aya K, Win K T, Doi K, Sobrizal , Ito T, Kanamori H, Wu J, Matsumoto T, Matsuoka M, Ashikari M, Yoshimura A. 2010. Mitochondrial gene in the nuclear genome induces reproductive barrier in rice. Proc Natl Acad Sci USA, 107(4): 1494?1499. |
| [43] | Yang C C, Kawahara Y, Mizuno H, Wu J Z, Matsumoto T, Itoh T. 2012. Independent domestication of Asian rice followed by gene flow from japonica to indica. Mol Biol Evol, 29(5): 1471-1479 |
| [44] | Yang J Y, Zhao X B, Cheng K, Du H Y, Ouyang Y D, Chen J J, Qiu S Q, Huang J Y, Jiang Y H, Jiang L W, Ding J H, Wang J, Xu C G, Li X H, Zhang Q F. 2012. A killer-protector system regulates both hybrid sterility and segregation distortion in rice. Science, 337: 1336-1340 |
| [45] | Zheng X M, 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(12): 2439-2454 |
| [46] | Zuellig M P, Sweigart A L. 2018. A two-locus hybrid incompatibility is widespread, polymorphic, and active in natural populations of Mimulus. Evolution, 72(11): 2394-2405 |
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