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Molecular Breeding

, 39:36 | Cite as

Identification of a locus for seed shattering in rice (Oryza sativa L.) by combining bulked segregant analysis with whole-genome sequencing

  • Feng LiEmail author
  • Hisataka Numa
  • Naho Hara
  • Naoki Sentoku
  • Takurou Ishii
  • Yoshimichi Fukuta
  • Noriyuki Nishimura
  • Hiroshi Kato
Article
  • 178 Downloads

Abstract

Seed shattering is an important trait related to the efficiency of harvesting seeds in crops. Although several genes have been identified to control seed shattering in rice (Oryza sativa L.), the genetic architecture underlying extensive variation of seed shattering is yet unclear. ‘Oonari’, a moderate-shattering indica rice cultivar, was developed from a mutant obtained through gamma-ray irradiation of an easy-shattering cultivar ‘Takanari’. The grain pedicel of ‘Oonari’ showed greater resistance to bending than that of ‘Takanari’, while there were no obvious differences in resistance to pulling and abscission zone formation. Investigation of the seed shattering of an F2 population from a cross between ‘Takanari’ and ‘Oonari’ indicated a single semi-dominant locus responsible for seed shattering, which was designated as Sh13. We used bulked DNA of F3 lines with the same shattering degree as that of ‘Oonari’ and DNAs of their parents for whole-genome sequencing, localizing Sh13 at the terminal region on the long arm of chromosome 2. In the candidate genomic region of ‘Oonari’, we identified a tandem duplicated segment containing a microRNA gene, osa-mir172d, whose wheat ortholog is involved in controlling grain threshability. Quantitative RT-PCR analysis indicated that the relative expression of osa-mir172d in ‘Oonari’ was twofold higher than that in ‘Takanari’. We suppose that the duplication of osa-mir172d be involved in reducing seed shattering in ‘Oonari’.

Keywords

Seed shattering Gamma-ray mutant Bulked segregant analysis Whole-genome sequencing osa-mir172d 

Notes

Acknowledgments

We gratefully acknowledge the Advanced Analysis Center of NARO for use of high-speed processor system, Prof. Takeshi Nishio for valuable revision and comments, Mrs. Sayaka Niwa and Mrs. Kanako Matsumoto for experiment support, and Mr. Masayoshi Tobita for field support.

Funding information

This work was supported by Cabinet Office, Government of Japan, Cross-ministerial Strategic Innovation Promotion Program (SIP), “Technologies for creating next-generation agriculture, forestry and fisheries” (funding agency: Bio-oriented Technology Research Advancement Institution, NARO).

Supplementary material

11032_2019_941_MOESM1_ESM.pptx (2 mb)
Supplementary Fig. 1 Evaluation of shattering degree using a tension testing machine equipped with a digital force gauge. (a) Measurement method and the direction of pulling strength (PS). (b) Close-up view corresponding to the red box in (a). (c) Measurement method and the direction of bending strength (BS). (d) Close-up view corresponding to the red box in (c). (e) Measurement method and the direction of press stress for the rate of grain shattering by pushing (RSP). (f) Close-up view corresponding to the red box in (e). (PPTX 2088 kb)
11032_2019_941_MOESM2_ESM.pptx (5.6 mb)
Supplementary Fig. 2 Representative images of pedicels of ‘Takanari’ (a) and ‘Oonari’ (b) after pushing the lower end of a pedicel vertically. (PPTX 5755 kb)
11032_2019_941_MOESM3_ESM.pptx (54 kb)
Supplementary Fig. 3 Comparison of shattering degrees between different cultivars at maturity stage in 2018. (a) Comparison of pulling strength (PS). (b) Comparison of bending strength (BS). (c) Comparison of rate of grain shattering by pushing (RSP). Bars indicate mean values ± standard deviation (n = 4). (PPTX 53 kb)
11032_2019_941_MOESM4_ESM.pptx (1.3 mb)
Supplementary Fig. 4 Longitudinal sections (10-μm thick) across the abscission zone of ‘Takanari’ (a) and ‘Oonari’ (b) grown in the early season. The sections were stained by toluidine blue. The read arrows indicate the abscission zones. (PPTX 1295 kb)
11032_2019_941_MOESM5_ESM.pptx (1003 kb)
Supplementary Fig. 5 Longitudinal sections (2-μm thick) across the abscission zone of ‘Takanari’ (a) and ‘Oonari’ (b) grown in the late season. The sections were stained by toluidine blue. The read arrows indicate the abscission zones. (PPTX 1002 kb)
11032_2019_941_MOESM6_ESM.pptx (44 kb)
Supplementary Fig. 6 Frequency distribution of the rate of grain shattering by pushing (RSP) in F2_c population. Horizontal bar and solid dot indicate the RSP range and mean value of ‘Oonari’ or ‘Takanari’ (n = 3 independent replicates with 4 plants grown in a row analyzed in each assay). (PPTX 43 kb)
11032_2019_941_MOESM7_ESM.pptx (577 kb)
Supplementary Fig. 7 Validation of the tandem duplication mutation on chromosome 2 of ‘Oonari’. (a) Schematic representation of the duplication mutation of the genomic region from ‘Takanari’ to ‘Oonari’. Directions of arrow-shaped boxes indicate 5’ to 3’ directions based on the ‘Nipponbare’ genome sequence. Arrowheads indicate the primer positions, and the predicted PCR product sizes are shown at the lower part. The positions of break points and rejoined sites of the duplication are shown at the upper part. Note that the diagram is not drawn to scale. (b) Agarose gel electrophoresis of the amplification products obtained by PCR. The primer sets are shown at the lower part, and sample names are shown at the upper part. T and O represent ‘Takanari’ and ‘Oonari’, respectively. (PPTX 576 kb)
11032_2019_941_MOESM8_ESM.pptx (2.1 mb)
Supplementary Fig. 8 Validation of the inversion on chromosome 6 of ‘Oonari’. (a) Schematic representation of inversion of the genomic region in ‘Takanari’ to that of ‘Oonari’. Directions of arrow-shaped boxes indicate 5’ to 3’ directions based on the ‘Nipponbare’ genome sequence. Arrowheads indicate the primer positions, and the predicted PCR product sizes are shown at the lower part. The positions of break points and rejoined sites of the inversion are shown at the upper part. Note that the diagram is not drawn to scale. (b) Agarose gel electrophoresis of the amplification products obtained after PCR. The primer sets are shown at the lower part, and sample names are shown at the upper part. T and O represent ‘Takanari’ and ‘Oonari’, respectively. (c) The nucleotide sequences of break points and rejoined sites of the inversion were determined by sanger sequencing. (PPTX 2155 kb)
11032_2019_941_MOESM9_ESM.pptx (44 kb)
Supplementary Fig. 9 Variance of rate of grain shattering by pushing (RSP) at the three mutation sites with different parental genotypes in partial F2-c population (n = 16). Bars indicate mean values ± standard deviation. T/T and O/O represent homozygous ‘Takanari’ and ‘Oonari’ alleles, respectively. Double asterisks (**) represent significant difference in RSP between the different genotypes at P < 0.01 level. (PPTX 43 kb)
11032_2019_941_MOESM10_ESM.pptx (44 kb)
Supplementary Fig. 10 Correlation between rate of grain shattering by grasping (RSG) and rate of grain shattering by pushing (RSP) (n = 53). (PPTX 43 kb)
11032_2019_941_MOESM11_ESM.pptx (48 kb)
Supplementary Fig. 11 Variance of rate of grain shattering by grasping (RSG) between different genotypes at the TO20 mutation site in F2-c population (n = 53) (a) and F3-b population (n = 75) (b). T/T_TO20 represents a homozygous allele for ‘Takanari’, O/O_TO20 for ‘Oonari’, and T/O_TO20 for a heterozygous allele at the TO20 mutation site. Different small and capital letters over the bars show significance levels at 0.05 and 0.01, respectively. Bars indicate mean values ± standard deviation. (PPTX 47 kb)
11032_2019_941_MOESM12_ESM.pptx (170 kb)
Supplementary Fig. 12 Identification of individuals and lines in which TO20 genotypes were not associated with seed shattering. (a) Detection of TO20 genotype with the dCAPS marker. F1: an F1 from the crossing of ‘Takanari’ and ‘Oonari’, T: ‘Takanari’, O: ‘Oonari’, TS185 and TS198: two F3 lines in the F3_c population, TS64: an individual in the F2-b population, TS64-2-T and TS64-2-O: F4 lines with homozygous ‘Takanari’ and ‘Ooanri’ alleles at TO20 site, respectively, derived from TS64. (b) Rate of grain shattering by pushing (RSP) of exceptional lines on 18th day after heading in the late season of 2016. T and O were used for controls. Different lowercase and uppercase letters over the bars show significance levels at 0.05 and 0.01, respectively. Bars indicate mean values ± standard deviation (n = 4). (PPTX 170 kb)
11032_2019_941_MOESM13_ESM.pptx (53 kb)
Supplementary Fig. 13 Genotypes at TO20 and TO21 sites in different cultivars or lines and their shattering degrees. There are an SNP (A/G) and a tandem duplication at TO20 and TO21 sites, respectively. The red arrows indicate the positions of the osmir172d genes. Note that the diagram is not drawn to scale. The cultivars or lines with duplication showed moderate shattering, while those without duplication showed easy shattering. (PPTX 52 kb)
11032_2019_941_MOESM14_ESM.xlsx (10 kb)
Supplementary Table 1 Primers used in this study. (XLSX 9 kb)
11032_2019_941_MOESM15_ESM.xlsx (11 kb)
Supplementary Table 2 Summary of Illumina sequencing data. (XLSX 10 kb)
11032_2019_941_MOESM16_ESM.xlsx (35 kb)
Supplementary Table 3 Mutations identified in ‘Oonari’, ‘Tankari’, and F3 bulk (XLSX 35 kb)
11032_2019_941_MOESM17_ESM.xlsx (32 kb)
Supplementary Table 4 Summary of the alignment of all of the NGS data of ‘Takanari’ and ‘Oonari’, respectively, to the ‘Nipponbare’ or ‘Minghui 63’ genome. (XLSX 31 kb)
11032_2019_941_MOESM18_ESM.xlsx (52 kb)
Supplementary Table 5 Genes in gap regions when the ‘Nipponbare’ genome was used as a reference genome (XLSX 51 kb)
11032_2019_941_MOESM19_ESM.xlsx (27 kb)
Supplementary Table 6 Genes in gap regions when ‘Minghui 63’ genome was used as a reference genome (XLSX 27 kb)

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Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Radiation Breeding Division, Institute of Crop ScienceNational Agricultural and Food Research Organization (NARO)Hitachi-ohmiyaJapan
  2. 2.Advanced Analysis CenterNational Agricultural and Food Research Organization (NARO)TsukubaJapan
  3. 3.Institute of Agrobiological ScienceNational Agricultural and Food Research Organization (NARO)TsukubaJapan
  4. 4.Rice Breeding UnitNational Agricultural and Food Research Organization (NARO)TsukubaJapan
  5. 5.Tropical Agriculture Research Front (TARF)Japan International Research Center for Agricultural Sciences (JIRCAS)IshigakiJapan
  6. 6.Genetic Resources CenterNAROTsukubaJapan

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