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Acta Agronomica Sinica ›› 2025, Vol. 51 ›› Issue (7): 1712-1724.doi: 10.3724/SP.J.1006.2025.42059

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

OsWRI3, identified based on QTL mapping, regulates seed shattering in rice

YANG Hai-Yang**(), WU Lin-Xuan**, LI Bo-Wen, SHI Han-Feng, YUAN Xi-Long, LIU Jin-Zhao, CAI Hai-Rong, CHEN Shi-Yi, GUO Tao(), WANG Hui()   

  1. South China Agricultural University / National Engineering Research Center of Plant Space Breeding, Guangzhou 510642, Guangdong, China
  • Received:2024-12-19 Accepted:2025-03-26 Online:2025-07-12 Published:2025-04-07
  • Contact: *E-mail: wanghui@scau.edu.cn; E-mail: guo.tao@vip.163.com
  • About author:**Contributed equally to this work
  • Supported by:
    China Agriculture Research System of MOF and MARA(CARS-01);Innovative Team Project of Ordinary Colleges and Universities of Guangdong Province(2021KCXTD029)

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Abstract:

Rice is a staple food crop worldwide, and seed shattering is a critical trait that directly affects yield. Developing rice varieties with moderate seed shattering that are suitable for mechanized harvesting is essential for improving yield. However, seed shattering is a complex quantitative trait influenced by multiple factors, and existing theories do not fully explain its underlying mechanisms. To identify quantitative trait loci (QTL) associated with seed shattering and refine the gene regulatory network governing this trait, we utilized a population of 192 recombinant inbred lines (RILs) derived from a cross between the male parent YZX, which exhibits high seed shattering, and the female parent 02428, which has low seed shattering. QTL mapping was conducted using seed shattering data collected at 30 days after flowering, assessed through both pulling and bending methods under different environmental conditions. A total of 19 QTL associated with seed shattering were identified across various environments and methods. Notably, a novel co-located QTL, qBSH5.2, was detected using the bending method. Further analysis, including database searches, gene expression profiling, RNA sequencing, and gene sequence analysis, identified OsWRI3 as a candidate gene within the qBSH5.2 locus. Functional validation showed that the OsWRI3 mutant exhibited significantly reduced seed shattering compared to the wild type (WT). Scanning electron microscopy revealed that the fracture surface of the mutant was rougher and contained spring-like burr structures, distinguishing it from the WT. Additionally, OsWRI3 expression in the rice panicle and abscission zone was positively correlated with maturity, and genes involved in ethylene precursor synthesis were downregulated in the abscission zone of the mutant compared to the WT. Haplotype analysis further confirmed the regulatory role of OsWRI3 in seed shattering, and we identified favorable haplotype combinations that confer moderate seed shattering, making them suitable for mechanized harvesting. In conclusion, the discovery of OsWRI3, an AP2 transcription factor, not only enhances our understanding of the genetic regulation of seed shattering but also provides valuable genetic resources for breeding rice varieties optimized for mechanized harvesting.

Key words: rice, seed shattering, QTL mapping, AP2 transcription factor, haplotype analysis

Table S1

Primers used in this study"

引物名称
Primer name		 正向引物
Forward primer (5'-3')		 反向引物
Reverse primer (5'-3')		 用途
Application
4100 GAGGACCTGTTTCAAGGCCA CCGGCAAAAACCTGTGATGG 基因筛选 Gene screening
4400 TTGGGGAGTTTGTACGGTCG TCCTCAGGGTCTATCCTGCC 基因筛选 Gene screening
4500 GTTGATGGCACGAGGACACT CAAATCCACCTCGAACCACG 基因筛选 Gene screening
5100 GATGGTGGTAGCAAGCCAGT GCACACCAGCCTTCCTTAGT 基因筛选 Gene screening
5200 AGCATCTTCGCCTCAGCTAC TTGGAAAGAAGGCACCCCAA 基因筛选 Gene screening
5900 ACTCCAAGCCCTGATTCGTG CACTCCCCGACTGTTGTTGA 基因筛选 Gene screening
6250 CGTCACGAACTTCGACCTCA TCACCACCACCCAGTGATTG 基因筛选 Gene screening
70actin GGCAGGTTCTGCAGTGGTAT TAAGGTCGGTATCGCCAATC 肌动蛋白基因 Actin gene
6250-CX2 TGATGGTGACACCAATGGTG GCTCCAAGATAGACTGATGC 靶点检测 Target detection
OsACS1 GCAGAGAGGGTACAAGGTGG ACCCTGGGTAGTATGGGGTG 功能分析 Functional analysis
OsACS2 GAGGCATCCATTTGCACACC TAAACTGGGCCATCGCCTTT 功能分析 Functional analysis
OsACS4 GATGTTGCGCTGGAGAGGAT TGTTGCACATGCCCTTGGTA 功能分析 Functional analysis
OsACS5 GCTGGTTCAGGGTGTGCTTC GCTTGTTGCTTTGTTCCATTCC 功能分析 Functional analysis
OsACO1 GCAGCATTGTCGTTCCCG CGAGATGCCGTGGTTCAGG 功能分析 Functional analysis
OsACO2 GGAGCAGCTGGATGATGCTT CACACGCTTGTAGTGGTCCT 功能分析 Functional analysis
OsACO4 GGTTTGAGGAGTGGGGGTTC ACTGCGGGGTTGGATTCTTT 功能分析 Functional analysis
OsACO5 CGACAATGGCTGCGAGGAGT CAAGCACACCTTCTTCACCCG 功能分析 Functional analysis
WRI3-1 GTCTCTCCTGGATCAAATCC TGGTACCTCCTTAGAGATGC 序列分析 Sequence analysis
WRI3-2 CAGCAAGGGCTTATGACCTT GGTGAAAGGATTGCTCTGAG 序列分析 Sequence analysis
WRI3-3 CCCATCTGCCATTCTTCCTA GCTTTGTTGTTCGGCACAAG 序列分析 Sequence analysis

Fig. 1

Measurement methods and evaluation of seed shattering A: measurement instruments used in this study; B: sample fixation method used in the measurement process of this study; C: measurement method of the pulling method; D: measurement method of the bending method; E: plant morphology of YZX (Bar: 20 cm); F: plant morphology of 02428 (Bar: 20 cm); G-J: abscission zone structures of YZX and 02428 in the early stage of flowering, YZX exhibits obvious abscission layer, whereas 02428 abscission layer does not exist (Bar: 100 μm); K-N: scanning electron microscopy of the fracture surfaces of YZX and 02428 at 30 days after flowering, the fracture surface of YZX is smooth and complete, while 02428 is rough and incomplete (Bar: 50 μm); O: frequency distribution histogram of the pulling method in 2021; P: frequency distribution histogram of the bending method in 2021; Q: frequency distribution histogram of the pulling method in 2023; R: frequency distribution histogram of the bending method in 2023."

Fig. 2

Seed shattering QTL identified by the pulling and the bending methods in 2021 and 2023 The figure illustrates the co-location of QTL in different years (red), different methods (green), and those that are not co-located (black), black interval indicates QTL that researchers have previously identified on rice chromosome 5. Figure shows the physical distances (100 kb) of QTL on chromosomes."

Table S2

QTL located in this study"

QTL名称
QTL name		 物理位置
Physical location (Mb)		 标记区间
Marker interval		 加性效应
Additive effect		 LOD值
LOD value		 贡献率
Contribution rate (%)
qBSH1.1 3.95-4.05 mk26-mk27 4.56 2.59 6.25
qBSH1.5 28.50-28.75 mk200-mk201 7.09 4.23 10.20
qBSH1.2 29.05-29.25 mk204-mk205 5.97 3.90 9.26
qPSH1.3 34.90-35.05 mk236-mk237 23.40 7.49 17.22
qBSH1.3 36.85-36.95 mk249-mk250 10.97 17.74 35.72
qPSH1.1 38.25-38.45 mk256-mk257 26.60 18.91 39.16
qPSH1.1 38.25-38.45 mk256-mk257 10.90 16.91 36.08
qPSH1.1 38.25-38.45 mk256-mk257 28.72 12.38 27.12
qPSH1.1 38.25-38.45 mk256-mk257 11.40 15.02 31.54
qBSH1.4 39.95-40.05 mk266-mk267 8.29 10.48 23.05
qPSH1.4 42.55-42.65 mk289-mk290 14.44 3.26 7.74
qPSH1.2 42.75-42.85 mk291-mk292 11.91 3.70 8.94
qPSH1.2 42.75-42.85 mk291-mk292 5.03 3.60 8.57
qBSH2 0.85-0.95 mk304-mk305 -4.75 3.15 7.54
qPSH3.1 1.10-1.25 mk559-mk560 11.11 2.98 7.35
qPSH3.2 2.75-2.95 mk574-mk575 12.87 3.94 9.71
qBSH3 28.40-28.55 mk792-mk793 4.81 2.51 5.99
qPSH4 19.25-19.35 mk1003-mk1004 10.95 3.01 7.49
qPSH4 19.25-19.35 mk1003-mk1004 4.53 2.73 6.83
qBSH4 20.55-20.65 mk1016-mk1017 4.55 2.86 6.87
qBSH5.1 21.80-21.95 mk1268-mk1269 4.44 2.67 6.53
qBSH5.2 26.50-26.65 mk1301-mk1302 4.38 2.55 6.17
qBSH5.2 26.50-26.65 mk1301-mk1302 4.81 2.51 5.95
qBSH7 25.35-25.45 mk1748-mk1749 -4.48 2.87 6.92
qBSH9 13.30-13.55 mk2062-mk2063 5.42 3.95 9.70

Fig. 3

Candidate gene database analysis and gene expression analysis in the abscission zone A: spatio-temporal gene expression profiles of different tissues/organs in rice; B: gene expression profile during reproductive organ development in rice; C: differences in the expression levels of candidate genes in the abscission zone between YZX and 02428 in the early stage of flowering; D: differences in the expression levels of candidate genes in the abscission zone between YZX and 02428 at 30 days after flowering. ns indicates no significant difference, * indicates a significant difference at P < 0.05, and ** indicates a significant difference at P < 0.01."

Fig. 4

RNA sequencing and gene sequence analysis A: there are 24 genes in qBSH5.2, excluding genes encoding transposons and retrotransposons, for a total of 21 genes. Red fonts indicate genes with differences in RNA sequencing. (+) indicates that the expression level of W517 is upregulated compared with that of DZ129 in the abscission zone, and (-) indicates that the expression level of W517 is downregulated compared with that of DZ129 in the abscission zone. The green curve indicates the LOD value of the bending method, and the red curve indicates the LOD value of the pulling method. B: comparison of the gene sequences of Os05g0536250 in YZX and 02428."

Fig. 5

Functional verification of ZH11-OsWRI3 A: two different knockout homozygous mutant lines of OsWRI3, ZH11-OsWRI3-1 with T insertion and ZH11-OsWRI3-2 with AT deletion, both mutations lead to premature termination of translation; B: comparison of ZH11-OsWRI3-1, ZH11-OsWRI3-2 and ZH11-WT plants (Bar: 20 cm); C: BTS values of ZH11-OsWRI3-1 and ZH11-OsWRI3-2 on 30 days after flowering were significantly higher than ZH11-WT; D: scanning electron micrographs of fracture surfaces of ZH11-WT, ZH11-OsWRI3-1, and ZH11-OsWRI3-2 at 30 days after flowering (Bar: 50 μm); E: expression pattern of OsWRI3 in various plant tissues, including leaves, roots, stems, leaf sheaths, pulvinus, internodes, 1-5 cm panicles, 5-10 cm panicles, the abscission zone in the early stage of flowering (0 d), and the abscission zone on 30 days after flowering of ZH11; F: differences in expression levels of pivotal genes involved in ACC synthesis between the WT and mutants. ## indicates no gene expression, * indicates a significant difference at P < 0.05, and ** indicates a significant difference at P < 0.01. BTS: breaking tensile strength."

Fig. 6

Haplotype analysis of OsWRI3 A: CDS haplotype analysis of OsWRI3; B: promoter haplotype analysis of OsWRI3; C: distribution of OsWRI3 CDS haplotypes and the differences in BTS values between the various haplotypes; D: distribution of OsWRI3 promoter haplotypes and the differences in BTS values between the various haplotypes; E: distribution of different haplotypes among seven major rice groups in MBKbase; F: joint analysis of OsWRI3 and qSH1 functional SNP. * indicates a significant difference at P < 0.05, and ** indicates a significant difference at P < 0.01. Different lowercase letters mean significant difference at P < 0.05. - represents the missing bases, D1 represents the bases AATGTAG. BTS: breaking tensile strength."

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