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Lineage-Specific Gene Acquisition Or Loss Is Involved in Interspecific

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Lineage-Specific Gene Acquisition Or Loss Is Involved in Interspecific Lineage-specific gene acquisition or loss is involved in PNAS PLUS interspecific hybrid sterility in rice Yohei Koidea,b,c,1, Atsushi Oginoa, Takanori Yoshikawad, Yuki Kitashimaa, Nozomi Saitoa, Yoshitaka Kanaokaa, Kazumitsu Onishie, Yoshihiro Yoshitakeb, Takuji Tsukiyamab, Hiroki Saitob,f, Masayoshi Teraishib, Yoshiyuki Yamagatag, Aiko Uemurah, Hiroki Takagih, Yoriko Hayashii, Tomoko Abei, Yoshimichi Fukutaf, Yutaka Okumotob, and Akira Kanazawaa aResearch Faculty of Agriculture, Hokkaido University, Sapporo, Hokkaido 060-8589, Japan; bGraduate School of Agriculture, Kyoto University, Kyoto 606- 8502, Japan; cHakubi Center for Advanced Research, Kyoto University, Kyoto 606-8501, Japan; dDepartment of Agricultural Regional Vitalization, Kibi International University, Minami-awaji, Hyogo 656-0484, Japan; eDepartment of Agro-Environmental Science, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido 080-8555, Japan; fTropical Agriculture Research Front, Japan International Research Center for Agricultural Sciences, Ishigaki, Okinawa 907-0002, Japan; gFaculty of Agriculture, Kyushu University, Fukuoka 812-8581, Japan; hDepartment of Genomics and Breeding, Iwate Biotechnology Research Center, Kitakami, Iwate 024-0003, Japan; and iAccelerator Applications Research Group, RIKEN, Wako, Saitama 351-0198, Japan Edited by June B. Nasrallah, Cornell University, Ithaca, NY, and approved January 12, 2018 (received for review July 2, 2017) Understanding the genetic basis of reproductive barriers between O. glaberrima has tolerance to various abiotic and biotic stresses species has been a central issue in evolutionary biology. The S1 (7, 8) and is therefore a valuable source of useful genes (9). locus in rice causes hybrid sterility and is a major reproductive Moreover, hybrids between O. glaberrima and O. sativa are very barrier between two rice species, Oryza sativa and Oryza glaber- vigorous (Fig. 1A and Fig. S1) (10), suggesting the potential g rima. The O. glaberrima-derived allele (denoted S1 ) on the S1 usefulness of interspecific hybrids for increasing grain pro- locus causes preferential abortion of gametes with its allelic alter- duction. However, strong hybrid sterility between O. glaberrima s g s native (denoted S1 )inS1 /S1 heterozygotes. Here, we used mu- and O. sativa (Fig. 1 B and C) has prevented the use of desirable tagenesis and screening of fertile hybrid plants to isolate a mutant traits of O. glaberrima (9, 11–14). Therefore, elucidating the mut mut g SCIENCES with an allele, S1 , which does not confer sterility in the S1 /S1 genetic basis of interspecific hybrid sterility between the two rice mut s AGRICULTURAL and S1 /S1 hybrids. We found that the causal mutation of the mut species is important not only to understand the evolutionary biology S1 allele was a deletion in the peptidase-coding gene (denoted of speciation but also to improve crops for future food production. “ ” SSP ) in the S1 locus of O. glaberrima. No orthologous genes of In Oryza, several causal genes for hybrid sterility have been SSP were found in the O. sativa genome. Transformation experi- – “ ” s cloned (15 19). The presence of neutral alleles that do not ments indicated that the introduction of SSP in carriers of the S1 mut s cause sterility in the heterozygous state at intraspecific hybrid allele did not induce sterility. In S1 /S1 heterozygotes, the in- sterility loci in O. sativa has been reported (Table S1). Although sertion of SSP led to sterility, suggesting that SSP complemented neutral alleles have facilitated a breakthrough in hybrid rice the loss of the functional phenotype of the mutant and that mul- production in Asia (18, 20), this type of naturally occurring allele tiple factors are involved in the phenomenon. The polymorphisms has never been found in interspecific cross-combinations in caused by the lineage-specific acquisition or loss of the SSP gene were implicated in the generation of hybrid sterility. Our results plants (Table S1). Recently, reverse-genetic approaches through demonstrated that artificial disruption of a single gene for the CRISPR/Cas9-mediated gene knockout successfully created reproductive barrier creates a “neutral” allele, which facilitates neutral alleles of intra- and interspecific hybrid sterility genes in interspecific hybridization for breeding programs. Significance rice | reproductive barrier | hybrid sterility | transmission ratio distortion | mutagenesis Hybrid sterility, a major reproductive barrier between species, hinders the transfer of desirable traits from one species to eproductive barriers prevent gene flow and maintain genetic another. We report a forward genetic approach for creating a “ ” Rdiscontinuities between species. One of the central issues in neutral allele of the S1 locus, a major interspecific hybrid evolutionary biology is how genic incompatibility between species sterility locus in rice. This neutral allele does not induce hybrid arose and became fixed without causing deleterious interaction sterility in combination with alleles from either Asian or Afri- within a species. The Bateson–Dobzhansky–Muller (BDM) model can rice species. The allele carries a deletion in the peptidase- indicates that incompatibilities are generally caused by an in- coding gene, SSP,intheS1 locus. This work provides mechanistic teraction between genes that have functionally diverged in each and evolutionary insights into hybrid sterility and demonstrates population (1). BDM-type genic incompatibilities are caused by the feasibility of the approach that allows broader access to several types of genetic differences between species, including nu- desirable traits in distantly related species during crop breeding. cleotide substitutions, the presence of transposable elements or Author contributions: Y. Koide, Y.F., Y.O., and A.K. designed research; Y. Koide, A.O., noncoding repeats, gene transposition, and reciprocal gene loss (2). T.Y., Y. Kitashima, N.S., Y. Kanaoka, K.O., Y. Yoshitake, T.T., H.S., M.T., A.U., H.T., Y.H., In addition to these differences, recent genome sequence analyses T.A., Y.F., and A.K. performed research; Y. Koide contributed new reagents/analytic tools; in animal and plant species revealed widespread gene-presence/ Y. Koide and Y. Yamagata analyzed data; and Y. Koide and A.K. wrote the paper. absence polymorphisms represented by coding sequences that are The authors declare no conflict of interest. present in some genomes but completely absent in others (3, 4). The This article is a PNAS Direct Submission. species-specific genes, also known as “orphan genes,” are shown to Published under the PNAS license. contribute to species-specific adaptations (5). However, it has not Data deposition: Sequencing data have been deposited in the DNA Data Bank of Japan been known whether gene-presence/absence polymorphisms are (DDBJ) (accession nos. DRA006416 to DRA006419). involved in the reproductive barrier between species. 1To whom correspondence should be addressed. Email: [email protected]. There are two cultivated rice species, Asian (Oryza sativa) and This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. African (Oryza glaberrima) (6). Although O. glaberrima is rapidly 1073/pnas.1711656115/-/DCSupplemental. being replaced by O. sativa cultivars that produce higher yields, www.pnas.org/cgi/doi/10.1073/pnas.1711656115 PNAS Latest Articles | 1of8 Downloaded by guest on October 2, 2021 s g Fig. 1. Effects of lines carrying S1 , S1 , and the Acc108S1M on hybrid sterility. (A) Hybrid vigor observed in F1 plants derived from a cross between O. sativa (cultivar, NERICA10) and O. glaberrima (cultivar, CG14). (Scale bar: 10 cm.) (B) Panicles of O. sativa (cultivar, T65), O. glaberrima (cultivar, CG14), and an interspecific hybrid. (Scale bar: 2 cm.) (C) Mean ± SD seed fertility of O. sativa (cultivar, T65), O. glaberrima (cultivar, CG14), and an interspecific hybrid. Means labeled with different letters differed significantly in Tukey’s honestly significant difference (HSD) test (n = 3 plants). (D) Plant type of Acc108, Acc108S1,and their F1 progeny. (Scale bars: 10 cm.) (E) Light micrographs of developing female gametophytes of Acc108 and F1 derived from a cross between Acc108 and Acc108S1 stained with Delafield’s hematoxylin (Muto Pure Chemicals). (Scale bars: 50 μm.) (F)I2-KI–stained pollen of Acc108 and of F1 plants derived from a cross between Acc108 and Acc108S1. TY and SP indicate typical and spherical-type aborted pollen grains, respectively. (Scale bar: 50 μm.) (G) Plant types of Acc108S1M, Acc108S1M × Acc108, and Acc108S1M × Acc108S1. (Scale bars: 10 cm.) (H) Panicles of Acc108 × Acc108S1, Acc108S1M, Acc108S1M × Acc108, and Acc108S1M × Acc108S1 plants. (Scale bars: 4 cm.) (I) Mean ± SD seed fertility (Upper) and frequency of pollen types (Lower) of Acc108 and Acc108S1 plants and their F1 progeny. Means labeled with different letters differed significantly in Tukey’s HSD test (n = 3 plants). (J) Interfertility relationships among Acc108, Acc108S1, and Acc108S1M. F1 plants derived from a cross between Acc108 and Acc108S1 are seed and pollen sterile, while F1 plants derived from a cross between Acc108S1M and either Acc108 or Acc108S1 are seed and pollen fertile. 2of8 | www.pnas.org/cgi/doi/10.1073/pnas.1711656115 Koide et al. Downloaded by guest on October 2, 2021 rice (21–23). However, such reverse-genetic approaches need Results PNAS PLUS detailed information about the causative genes before applica- Histological
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