水稻黄绿叶调控基因YGL18的克隆与功能解析

doi:10.11983/CBB22018

植物学报 ›› 2022, Vol. 57 ›› Issue (3): 276-287.DOI: 10.11983/CBB22018

水稻黄绿叶调控基因YGL18的克隆与功能解析

杨凯如¹, 贾绮玮¹, 金佳怡¹, 叶涵斐¹, 王盛¹, 陈芊羽¹, 管易安¹, 潘晨阳¹, 辛德东¹, 方媛¹^,^*(), 王跃星²^,^*(), 饶玉春¹^,^*()

¹浙江师范大学化学与生命科学学院, 金华 321004
²中国水稻研究所水稻生物学国家重点实验室, 杭州 310006

收稿日期:2022-01-19 接受日期:2022-03-18 出版日期:2022-05-01 发布日期:2022-05-18
通讯作者: 方媛,王跃星,饶玉春
作者简介:ryc@zjnu.cn
wangyuexing@caas.cn;
* E-mail: fy0579@zjnu.cn;
基金资助:
国家级大学生创新创业训练计划(202010345067);国家级大学生创新创业训练计划(202110345011);国家自然科学基金(31971921);广西水稻遗传育种重点实验室开放基金(2018-15-Z06-KF12);中国水稻生物学国家重点实验室开放项目(20200102)

Cloning and Functional Analysis of Rice Yellow Green Leaf Regulatory Gene YGL18

Kairu Yang¹, Qiwei Jia¹, Jiayi Jin¹, Hanfei Ye¹, Sheng Wang¹, Qianyu Chen¹, Yian Guan¹, Chenyang Pan¹, Dedong Xin¹, Yuan Fang¹^,^*(), Yuexing Wang²^,^*(), Yuchun Rao¹^,^*()

¹College of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua 321004, China
²State Key Laboratory of Rice Biology, China National Rice Research Institute, Hangzhou 310006, China

Received:2022-01-19 Accepted:2022-03-18 Online:2022-05-01 Published:2022-05-18
Contact: Yuan Fang,Yuexing Wang,Yuchun Rao

摘要/Abstract

摘要： 叶色突变体往往伴随着叶绿素含量变化及叶绿体结构异常, 是研究叶绿体发育与光合作用相关基因功能的重要材料。该研究通过甲基磺酸乙酯(EMS)诱变籼稻(Oryza sativa subsp. indica)品种华占(HZ)获得黄绿叶突变体, 将其命名为ygl18 (yellow-green leaf 18)。与野生型相比, 黄绿叶突变体ygl18自三叶期起叶片开始变黄且程度不断加深, 同时伴随着光合速率与叶绿素含量下降, 且结实率、千粒重及有效穗数均显著降低。透射电镜观察结果显示, ygl18的叶绿体结构紊乱, 基质片层疏松, 发育受到抑制, 与叶片出现黄绿色表型一致。遗传分析表明, ygl18突变性状受1对隐性等位核基因控制, 这对等位基因位于水稻第3号染色体长臂标记InDel2和InDel3之间115.2 kb范围内。进一步研究发现该突变体表型是编码铁氧还蛋白FdC2的基因LOC_Os03g48040的5'UTR发生突变所致。通过CRISPR转基因实验验证了该基因对表型的控制作用。研究结果揭示了叶色调控网络的遗传基础, 可为今后选育高光效水稻品种提供新线索。

关键词: 水稻, 叶色变异, 遗传分析, 图位克隆, 铁氧还蛋白

Abstract: Leaf color mutants are often accompanied by changes in chlorophyll content and abnormal chloroplast structure, and serve as essential materials for studying the functions of chloroplast development and photosynthesis-related genes. In this study, we obtained a yellow-green leaf mutant named yellow-green leaf 18 (ygl18) from Oryza sativa subsp. indica cv. ‘HZ’ with ethyl methanesulfonate (EMS). Compared with the wild type, the leaves of ygl18 turned yellow at three-leaf stage and the degree of yellowing increased as it grew, accompanied by decreasing photosynthetic rate and chlorophyll content. The seed-setting rate, 1 000-grain weight, and effective panicle number were significantly lower than those of the wild type. We observed disordered chloroplast structure, loose stromal lamellas, and stalled development in the mutant using transmission electron microscopy. Genetic analysis indicated that the mutant feature (or phenotype) of ygl18 is controlled by a pair of recessive nuclear alleles, which were located in a 115.2 kb region between markers InDel2 and InDel3 on the long arm of chromosome 3. We found mutations in the 5′UTR of LOC_Os03g48040 encoding FdC2 (ferredoxin C2). The gene’s function on controlling the mutant phenotype was verified using CRISPR transgenic experiments. Our results revealed a genetic basis for leaf color regulatory network and provide new clues for breeding photosynthetically efficient rice varieties in the future.

Key words: Oryza sativa (rice), leaf color variation, genetic analysis, map-based cloning, ferredoxin

杨凯如, 贾绮玮, 金佳怡, 叶涵斐, 王盛, 陈芊羽, 管易安, 潘晨阳, 辛德东, 方媛, 王跃星, 饶玉春. 水稻黄绿叶调控基因YGL18的克隆与功能解析. 植物学报, 2022, 57(3): 276-287.

Kairu Yang, Qiwei Jia, Jiayi Jin, Hanfei Ye, Sheng Wang, Qianyu Chen, Yian Guan, Chenyang Pan, Dedong Xin, Yuan Fang, Yuexing Wang, Yuchun Rao. Cloning and Functional Analysis of Rice Yellow Green Leaf Regulatory Gene YGL18. Chinese Bulletin of Botany, 2022, 57(3): 276-287.

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图/表 12

表1 精细定位所用引物序列

Table 1 Primer sequences for fine mapping

Primer name	Forward primer (5′-3′)	Reverse primer (5′-3′)
B3-14	AGGATTTGGGCTGTCAATGC	AGCCTACCACAAGACATATAATCG
B3-15	TCCAGTCCACTAAAAGTTTTC	ATTATGCTATAGGCTTTGAGC
M1	TGGAAATGGGTGGAATACCT	CCTCTGTGAGGACCATCTCC
M2	GAATTATTTTTCCTTGGTCATTGTG	GTACCAACGAGGGTCCAAAG
M3	GGAGGCAGGCTACACCAGTA	GCACAATTCTTAAAGAGATGAACC
M4	TTTGATTGGGCTCAAAGCAC	GCCAGGATTTGTTGGATTAGG
M5	AAAAACTCCCAGCGGATAGA	GCTAGAACTGGCAAAATGCTG
Indel1	TTAGGCAAATGAAACCAAGG	CCCAACCACCTAAGTAAACGA
Indel2	TCCTTTGATGACTGGTCGGC	ATGGGAAGACGGGGGAGTAA
Indel3	GTTTGGGAGAGACATGGGGG	GTTTGGCCCATTCCCTGAAG
Indel4	ATGATTTGGAGCCAGCAGTT	GGAAGTGGAATTGCAGATGG

表2 qRT-PCR所用引物序列

Table 2 Primer sequences for qRT-PCR

Primer name	Forward primer (5′-3′)	Reverse primer (5′-3′)
CAO1-qrt	GCTGCTCTACCGGATGTCTC	ACAACCGATACCGGATACCA
DVR-qrt	TTCACCTACAGCATCGTCCG	AACAGCATCTCCCCTTGCTC
YGL1-qrt	TGTTGGTGGGTCCTTGCTTT	ACTGAAGCCCCAGAGCTCTA
PORA-qrt	CATGCTCGACGACCTCAAGA	TCCTGCATCGTCAGCATGTT
PORB-qrt	CATCATCGTCGGCTCCATCA	TCCTGCATCGTCAGCATGTT
ChlH-qrt	GGGAACTTGGCGTTTCATTA	TCAAATGTCTTGCGTTGCTC
ChlD-qrt	TCCTTTAGCTCACGGCCTTA	GTCCAACATCACCGCTCTTT
NOL-qrt	TCACAAGCCTTACGACCCAC	GCTCCCTCTCCATCATCTGC
NYC1-qrt	TAGTTGGCTCGGGGGAGTAA	AAGGACTGATTCAGGGCTGC
OsFdC2-qrt	AGCTGTGCGGTTCGGATAAA	AACAGGTCCTCGTGCGAAAT
rpoA-qrt	CCATTCCCACAAGCAAAAAT	TCTTACCGCCTTCCGTAGAA
rpoB-qrt	TGGTACATATCCCTTATCTCAA	CTCCAGGACCCAAACAACTC
rbcL-qrt	CTTGGCAGCATTCCGAGTAA	ACAACGGGCTCGATGTGATA
rbcS-qrt	GCTTGGAGTTCAGCAAGGTC	AACGAAGGCATCAGGGTATG
PsaA-qrt	TTAGAAATCCGCCAATCCA	TGCTAGGCTCTACAACCATT
PsaD-qrt	CCGCTCCAAGTACAAGATCA	AAGAGCAGCCTGACAGATGA
PsbA-qrt	ACCCTCATTAGCAGATTCGT	GATTGTATTCCAGGCAGAGC
PsbD-qrt	AAGACAGATTCCGAGGGTGG	TGATTCGCTAGGGATTAAAGAG

表3 CRISPR/Cas9载体所用引物

Table 3 Primer sequences for CRISPR/Cas9

Primer name	Forward primer (5′-3′)	Reverse primer (5′-3′)
CRISPR/Cas9	CTCCCTCTCTCGATCGTCAG	GCTACTGCTGCTTGAGACGG

图1 水稻野生型HZ与突变体ygl18的表型 (A) 分蘖期植株(bar=6 cm); (B) 成熟期植株(bar=10 cm)

Figure 1 Phenotypic of wild-type HZ and mutant ygl18 of rice (A) Phenotype of plant at tillering stage (bar=6 cm); (B) Phenotype of plant at maturity stage (bar=10 cm)

图2 水稻野生型HZ与突变体ygl18的农艺性状 (A) 穗长; (B) 有效穗数; (C) 二次枝梗数; (D) 分蘖数; (E) 结实率; (F) 千粒重。*和**分别表示在0.05和0.01水平差异显著。

Figure 2 Agronomic characters of wild-type HZ and mutant ygl18 of rice (A) Panicle length; (B) Effective number of panicle; (C) Secondary branch number; (D) Tiller number; (E) Seed-setting rate; (F) 1000-grain weight. * and ** indicate significant differences at 0.05 and 0.01 levels, respectively.

图3 水稻野生型HZ和突变体ygl18叶片光合色素含量和净光合速率 (A) 分蘖期叶片光合色素含量; (B) 抽穗期叶片光合色素含量; (C) 叶片净光合速率。*和**分别表示在0.05和0.01水平差异显著。

Figure 3 Photosynthetic pigment contents and net photosynthetic rate in leaves of wild-type HZ and mutant ygl18 of rice (A) Photosynthetic pigment content of leaves at tillering stage; (B) Photosynthetic pigment content of leaves at heading stage; (C) Net photosynthetic rate of leaves. * and ** indicate significant differences at 0.05 and 0.01 levels, respectively.

图4 水稻野生型HZ和突变体ygl18叶肉细胞超微结构观察 (A) HZ叶肉细胞(bar=2 μm); (B) HZ叶肉细胞(bar=1 μm); (C) ygl18叶肉细胞(bar=2 μm); (D) ygl18叶肉细胞(bar=1 μm)。G: 类囊体片层; Sg: 淀粉粒; O: 嗜锇粒

Figure 4 Ultrastructural observation of mesophyll cells in wild-type HZ and mutant ygl18 of rice (A) HZ mesophyll cells (bar=2 μm); (B) HZ mesophyll cells (bar=1 μm); (C) ygl18 mesophyll cells (bar=2 μm); (D) ygl18 mesophyll cells (bar=1 μm). G: Grana lamella; Sg: Starch granule; O: Ophilic granule

图5 水稻野生型HZ和突变体ygl18分蘖期叶绿素合成、叶绿体发育及光合作用相关基因的表达量 (A) 叶绿素合成相关基因的表达量; (B) 叶绿体发育及光合作用相关基因的表达量

Figure 5 Expression levels of chlorophyll synthesis, chloroplast development and photosynthesis related genes in wild-type HZ and mutant ygl18 of rice at tillering stage (A) Expression of genes related to chlorophyll synthesis; (B) Expression of genes related to chloroplast development and photosynthesis

表4 水稻突变体F2代群体的遗传分析

Table 4 Genetic analysis of F2 population of rice mutant

Cross	No. of F₂ individuals			χ²_0.05<3.841
Cross	Normal	yellow-green leaf	Total	χ²_0.05<3.841
ygl18 × NIP	836	331	1167	0.833

图6 水稻YGL18的精细定位 (A) YGL18定位于水稻3号染色体长臂B3-14与B3-15之间; (B) 使用148个F2代突变个体将其缩小至M3与M4之间; (C) 使用504个F2代突变个体将其限定在InDel2和InDel3之间约115.2 kb的区域中, 共15个开放阅读框(ORFs), 其中绿色部分表示突变基因所在ORF; (D) YGL18基因结构模型(绿色方框表示外显子, 白色方框表示UTRs, 黑线表示内含子); (E) YGL18在野生型和突变体间的测序结果峰图

Figure 6 Fine mapping of YGL18 in rice (A) YGL18 was located between B3-14 and B3-15 on long arm of rice chromosome 3; (B) Then it was narrowed to a region between M3 and M4 using 148 F2 mutants; (C) Then it was limited to an area of about 115.2 kb between InDel2 and InDel3 with a total of 15 open reading frames (ORFs), using 504 F2 mutants; (D) YGL18 gene structure modeling (green boxes indicate exons, white boxes indicate UTRs, and black lines between boxes indicate introns); (E) Peak sequencing result of YGL18 gene between wild type and mutant

图7 水稻YGL18基因的CRISPR/Cas9敲除验证 (A) 2个分离的敲除靶点位置(黑色方框表示外显子, 灰色方框表示UTRs, 黑线表示内含子, Target 1和Target 2为2个分离的靶点); (B) 基因敲除株的测序验证; (C) 野生型(WT)、突变体ygl18、敲除1及敲除2株系表型(bar=2 cm)。PAM: 原间隔序列邻近基序

Figure 7 CRISPR/Cas9 knockout verification of YGL18 in rice (A) The position of two separate knockout targets (black boxes represent exons, gray boxes represent UTRs, black lines represent introns, and Target 1 and Target 2 are two separate targets); (B) Sequencing verification of gene knockout strains; (C) Phenotype of wild type (WT), mutant ygl18, KO1 and KO2 lines (bar=2 cm). PAM: Protospacer adjacent motif

图8 水稻野生型HZ和突变体ygl18中YGL18基因表达模式 (A) YGL18的组织特异性表达; (B) YGL18在不同发育时期的表达水平

Figure 8 Expression pattern of gene YGL18 in wild-type HZ and mutant ygl18 of rice (A) Tissue specific expression of YGL18; (B) The expression level of YGL18 in different development stage

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水稻黄绿叶调控基因YGL18的克隆与功能解析

Cloning and Functional Analysis of Rice Yellow Green Leaf Regulatory Gene YGL18

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