Scientia Agricultura Sinica ›› 2025, Vol. 58 ›› Issue (6): 1052-1064.doi: 10.3864/j.issn.0578-1752.2025.06.002

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

Generation of Low-Glutelin Rice (Oryza sativa L.) Germplasm Through Long Fragment Deletion Using CRISPR/Cas9-Mediated Targeted Mutagenesis

JIN YaRu1,2(), CHEN Bin1,2, WANG XinKai1,2, ZHOU TianTian2, LI Xiao2, DENG JingJing2, YANG YuWen2, GUO DongShu2, ZHANG BaoLong1,2()   

  1. 1 School of Tropical Agriculture and Forestry, Hainan University, Haikou 570228
    2 Institute of Germplasm Resources and Biotechnology, Jiangsu Academy of Agricultural Sciences, Nanjing 210014
  • Received:2024-09-25 Accepted:2024-11-18 Online:2025-03-16 Published:2025-03-25
  • Contact: ZHANG BaoLong

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Abstract:

【Objective】 Rice (Oryza sativa L.) is a staple cereal crop for about half of the global population, with protein being the second-most significant nutritional component in rice grains. The storage proteins in rice grains mostly consist of glutelin, prolamin, globulin, and albumin, among which the content of easy-to-digest glutelin is the highest. Consequently, common rice increases the burden of kidney and accelerates the progression of renal disorders. The method of generating low-glutelin rice germplasm will provide novel genetic material for the cultivation of functional rice cultivars suitable for individuals with kidney diseases. 【Method】 We utilized Suxiu 867 (SX867), an elite japonica rice cultivar appropriate for cultivation in Jiangsu province, as a transgenic recipient to delete a fragment of approximately 3 500 bp between the B subfamily glutelin-coding genes GluB4 and GluB5 using CRISPR/Cas9-mediated gene editing technology. The large fragment deletion was identified by PCR using the primers corresponding to the flanking sequence of gene editing target sites, while sequence-specific primers for Cas9 and hygromycin resistance gene cassettes were used to identify the low-glutelin rice mutant absent of transgenic elements. The protein component contents of homozygous low-glutelin mutants were analyzed qualitatively and quantitatively, and the expression levels of glutelin-coding genes in rice grains were detected by quantitative PCR. The agronomic traits and quality traits of homozygous low-glutelin mutants and recipient cultivar cultivated under the same cultivation conditions were measured. 【Result】 Homozygous mutants with a 3 448 bp deletion between GluB4 and GluB5 genes were generated successfully. In the mutants, the relative proportion of glutelin decreased significantly, while that of prolamin and globulin increased significantly. The glutelin content of homozygous mutants decreased to 45.54%-49.75% compared to recipient cultivar, and the reduction level is comparable to LGC-1, a low-glutelin rice germplasm commonly used as a donor of low-glutelin trait in commercialized rice cultivars. The expression levels of B subfamily glutelin-coding genes in homozygous mutant were decreased significantly, and the changing trends was consistent with that of LGC-1 derived rice cultivar. Except that plant height decreased and grain length increased significantly, other measured agronomic and quality traits of homozygous mutants were not changed significantly compared to recipient cultivar. 【Conclusion】 Using CRISPR/Cas9-mediated gene editing technology, rice mutants with significant lower glutelin content free from transgenic elements were obtained successfully providing a convenient and quick method to generate low-glutelin germplasm.

Key words: rice, glutelin, gene editing, GluB4, GluB5, low-glutelin rice

Fig. 1

Schematic diagrams of gene editing strategy and T-DNA region of CRISPR vector A: Gene structures and target sites of GluB4 and GluB5. Green boxes represent the exons of GluB4 and GluB5 genes, short black lines between exons represent introns or intergenic region; Red lines in green boxes indicate the location of spacer1, while yellow line in intergenic region indicates the location of spacer2; The sequences of two spacers and flanking regions are shown below the diagram of genes; Underlined red and blue letters indicate the sequences of target sites, and underlined black letters indicate the protospacer adjacent motif (PAM) sequence; Black arrows indicate the locations of the primers labeled above or below the arrows. B: Diagram of gene editing vector T-DNA segment. ZmpUBI: Promoter of maize Ubiquitin1 gene. SpCas9: Cas9 gene derived from Streptococcus pyogenes after codon optimization for rice; NOST: NOS terminator; 3: Rice U3b promoter; 35S Promoter: Cauliflower mosaic virus 35S promoter; HygR: Hygromycin resistance gene; 35ST: 35S terminator; LB: T-DNA left boundary; RB: T-DNA right boundary"

Fig. 2

Electrophoretic results of genotyping and transgenic elements detection of T1 generaation CRISPR-GluB45 transgenic lines Marker: DNA molecular weight standards; Line 2-7: T1 generation plants; 38-2 and 38-8: Homozygous lines with long fragment deletion; 38-4 and 38-15: Heterozygous lines; 38-1 and 38-6: Wild-type segregate without long fragment deletion; T0-38: T0 generation transgenic line of No. 38; SX867: Transgenic receptor cultivar; LGC-1: Japonica rice cultivar derived from LGC-1; Control: PCR negative control"

Fig. 3

Sanger sequencing chromatograms of genotyping results of 38-2 and 38-8 A: The chromatograms of Sanger sequencing of mixed PCR productions of 38-2 and 38-8 indicating the sequences flanking the large fragment deletion region; B: The chromatograms of Sanger sequencing of mixed PCR productions of 38-2 and 38-8 indicating the sequences flanking spacer1 in GluB4. * and · under the letters represent the corresponding bases in gene sequences and Sanger sequencing chromatograms"

Table 1

Determination results of relative content of protein components"

品种或突变体
Cultivar or mutant		 基因型或品种特性
Genotype or cultivar feature		 蛋白组分Protein fraction (%) 谷蛋白相对含量/野生型4
Relative glutelin content/ Wild type (%)
谷蛋白
Glutelin		 球蛋白
Globulin		 醇溶蛋白
Prolamin		 其他
Others
SX867 转基因受体 Transgenic recipient 51.23 6.33 29.74 12.70 100.00
LGC-1 LGC-1转育品种LGC-1 derived cultivar 22.32 10.73 51.55 15.40 43.57
38-111 野生型3 Wild type 53.91 7.13 29.9 9.06 105.23
38-61 野生型3 Wild type 47.43 6.89 34.27 11.41 92.58
38-41 杂合突变体 Heterozygous mutant 36.22 10.53 41.28 11.97 70.70
38-151 杂合突变体 Heterozygous mutant 33.04 10.23 42.55 14.19 64.49
38-21 纯合突变体 Homozygous mutant 23.33 13.79 48.59 14.29 45.54
38-81 纯合突变体 Homozygous mutant 23.63 12.36 48.73 15.29 46.13
SX867 转基因受体 Transgenic recipient 52.36±0.33a 7.54±0.03a 26.47±0.93a 13.64±0.57a 100.00
LGC-1 LGC-1转育品种 LGC-1 derived cultivar 25.00±0.77b 13.01±1.28b 49.03±1.63b 12.98±0.43a 47.84
38-22 纯合突变体 Homozygous mutant 26.00±0.03b 13.18±1.84b 50.41±1.08b 10.41±0.79a 49.75
38-82 纯合突变体 Homozygous mutant 25.48±1.52b 13.62±0.28b 48.94±0.42b 11.97±1.66a 48.76

Fig. 4

SDS-PAGE results of brown rice Marker: Protein molecular weight standards; The right vertical lines indicate different components of rice storage protein; SX867: Transgenic receptor cultivar; LGC-1: Japonica rice cultivar derived from LGC-1; 38-2 and 38-8: Homozygous mutants with long fragment deletion"

Fig. 5

Gene expression levels of rice glutelin-coding genes SX867: Transgenic receptor cultivar; 38-2 and 38-8: T1 generation homozygous mutants; LGC-1: Japonica rice cultivar derived from LGC-1; GlutelinB×3: GluB1a, GluB1b, and GluB2"

Table 2

Statistical results of agronomic and quality trait"

指标Index SX867 38-2 38-8
总蛋白含量Total protein content (%) 8.52±0.45a 9.28±0.80a 8.65±0.65a
直链淀粉含量Amylose content (%) 16.82±0.29a 17.16±0.39a 16.90±0.96a
粒长Grain length (mm) 4.69±0.20a 4.86±0.34b 4.83±0.39b
粒宽Grain width (mm) 2.67±0.18a 2.64±0.21a 2.63±0.24a
株高Plant height (cm) 67.48±2.27a 64.65±2.87b 64.37±1.96b
分蘖数Tiller number 13.80±2.00a 14.73±2.07a 15.47±2.07a
每穗粒数Number of spikelets per panicle 143.13±13.45a 138.22±8.71a 133.35±10.88a
千粒重1000-grain weight (g) 27.45±0.41a 27.80±0.65a 27.08±0.24a

Fig. 6

Rice plant type, appearance phenotype and the morphology of starch grain A: The morphology of SX867, 38-2 and 38-8 mature plants, bar=10 cm; B-D: Seed appearance of SX867, 38-2 and 38-8, bar=1 cm; E-G: The appearance of SX867, 38-2 and 38-8 brown rice, bar=1 cm; H-J: The appearance of SX867, 38-2 and 38-8 milled rice, bar=1 cm; K-M: Starch particle morphology of SX867, 38-2 and 38-8 milled rice cross sections, bar=10 μm"

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