水稻分蘖调控基因HTD3的克隆与功能研究

doi:10.16819/j.1001-7216.2021. 210205

中国水稻科学 ›› 2021, Vol. 35 ›› Issue (6): 535-542.DOI: 10.16819/j.1001-7216.2021. 210205

水稻分蘖调控基因HTD3的克隆与功能研究

吴先美¹^,^#, 李三峰¹^,^#, 胡萍¹, 何瑞¹, 焦然², 毛一剑¹, 鲁草林¹, 胡娟², 林晗², 吴荣梁¹, 朱旭东¹, 饶玉春^2,^*(), 王跃星^1,^*()

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

收稿日期:2021-02-16 修回日期:2021-03-23 出版日期:2021-11-10 发布日期:2021-11-10
通讯作者: 饶玉春,王跃星
作者简介:
^#共同第一作者
基金资助:
浙江省自然科学杰出青年基金资助项目(LR20C130001);国家自然科学基金面上资助项目 (31971921);浙江省万人计划青年拔尖人才资助项目(ZJWR0108023)

Cloning and Functional Analysis of Rice Tillering Regulatory Gene HTD3

Xianmei WU¹^,^#, Sanfeng LI¹^,^#, Ping HU¹, Rui HE¹, Ran JIAO², Yijian MAO¹, Caolin LU¹, Juan HU², Han LIN², Rongliang WU¹, Xudong ZHU¹, Yuchun RAO^2,^*(), Yuexing WANG^1,^*()

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

Received:2021-02-16 Revised:2021-03-23 Online:2021-11-10 Published:2021-11-10
Contact: Yuchun RAO, Yuexing WANG
About author:
^#These authors contributed equally to this work

摘要/Abstract

摘要：

【目的】克隆水稻分蘖相关基因,为构建理想株型水稻,提高粮食产量提供理论基础及有利基因资源。【方法】在常规大田种植条件下分别比较突变体htd3（high-tillering dwarf 3）与野生型在幼苗期、抽穗期和成熟期表型及主要农艺性状差异,利用图位克隆方法克隆候选基因,利用荧光定量PCR方法分析HTD3及独脚金内酯和脱落酸相关基因的表达水平,测序比对分析HTD3在147份种质资源中的自然变异情况。【结果】与野生型相比,突变体htd3的分蘖芽生长较快,分蘖数和有效穗数显著增多,株高、一次枝梗数和每穗粒数显著降低,结实率和千粒重没有显著变化。遗传分析表明,htd3多分蘖的性状受一对隐性核基因控制。图位克隆将HTD3基因定位在第12染色体CM8和CM10之间约63.5 kb的物理区间内,互补转基因实验证明该区间内LOC_Os12g21710为控制突变体多分蘖表型的基因。HTD3在野生型和突变体中呈组成型表达,该基因突变会引起部分独脚金内酯和脱落酸相关基因的表达水平上调。水稻品种中HTD3编码区G2674A自然变异使得分蘖数显著增多。【结论】HTD3是最近报道的T20/MIT1基因的一个新的等位基因,HTD3突变导致水稻出现分蘖适度增加,株高略矮的表型,在培育理想株型水稻和高产育种上具有较大的应用潜力。

关键词: 水稻, 多分蘖, 图位克隆, 生物学功能

Abstract:

【Objective】Cloning of rice tiller-related genes lays a theoretical basis and provides beneficial genetic resources for constructing ideal plant-type rice and increasing grain yield.【Method】We compared phenotypes and main agronomic traits between the mutant htd3 (high-tillering dwarf 3) and its wild type under conventional field planting conditions, used map-based cloning method to clone candidate genes, analyzed the expression levels of HTD3, SL and ABA-related genes by fluorescence quantitative real-time PCR. Sequencing comparison was performed to analyze the natural variation of HTD3 in 147 germplasm resources.【Result】Compared with the wild type, the axillay bud of the mutant htd3 grow faster, the number of tillers and effective panicles were significantly increased, the plant height, the number of primary rachis branches and grains per panicle were significantly decreased, and the seed setting rate and 1000-grain weight were not significantly changed. Genetic analysis indicated that the high-tillering trait of htd3 was controlled by single recessive nuclear gene, which was mapped to a 63.5 kb region between the marker CM8 and CM10 on chromosome 12, and the complementary transgenic experiment proved that LOC_Os12g21710 was the gene controlling the high-tillering phenotype. HTD3 is constitutively expressed in wild-type and mutant, and the mutation of this gene could up-regulate the expression level of some stratolactones and ABA-related genes. The natural variation of G2674A in the HTD3 coding region in rice varieties significantly increase the number of tillers.【Conclusion】HTD3 is a new allele of the recently reported T20/MIT1 gene. The HTD3 mutation leads to the phenotype of moderate increase in tillers and slightly shorter plant height in rice, which has great application potential in cultivating ideal plant type rice and high-yield breeding.

Key words: rice, high-tillering, gene cloning, biological function

吴先美, 李三峰, 胡萍, 何瑞, 焦然, 毛一剑, 鲁草林, 胡娟, 林晗, 吴荣梁, 朱旭东, 饶玉春, 王跃星. 水稻分蘖调控基因HTD3的克隆与功能研究[J]. 中国水稻科学, 2021, 35(6): 535-542.

Xianmei WU, Sanfeng LI, Ping HU, Rui HE, Ran JIAO, Yijian MAO, Caolin LU, Juan HU, Han LIN, Rongliang WU, Xudong ZHU, Yuchun RAO, Yuexing WANG. Cloning and Functional Analysis of Rice Tillering Regulatory Gene HTD3[J]. Chinese Journal OF Rice Science, 2021, 35(6): 535-542.

图/表 9

表1 HTD3精细定位所用分子标记

Table 1 Sequences of markers for HTD3 mapping.

标记 Marker	正向引物 Forward primer (5′→3′)	反向引物 Reverse primer (5′→3′)
B12-6	TGAAGCGGTTTGACTTTGACC	GGGGTGAAAACTGGTAGGGT
B12-9	TCCTTCTCGTTTATGAACTTATGG	TAGAGCAAAGCAGAGCCCAG
M9	TAATCCCCTGCACTCCATCC	GTGAACAACCAGCCGAGAAT
M17	GACTTTCTAGCATTGCCCACA	GCATTAACTGGGGCCATTGT
M25	GAGACGGCCAGCTTAGGTAG	CAGTGCTACAGAAACAGGGC
M29	CCGAACTCCAGTTTGTGAGG	CGGAAATCTGACGCTGGTAT
M35	AAAAGAACAACACAGCCCCT	ACAAGGAGCAATCTGGACCA
CM5	TTGTGAACAAGAGCCAACGG	CGCTGTTGGGCATTCTTTAAAG
CM8	GTGTGATCCATGGGTAGCCT	CAGAGCCCTATTAGTCTATTGCT
CM10	TCACATGATACCTCGCGAGT	CAGACGATTCTACACAACAGGA
CM13	AGCAGCCAAGATTAAGGAGGA	CGTCAGAGTGATTAGCAAAAGGA

表2 扩增HTD3完整表达单元的引物

Table 2 Primers for amplifying the complete expression unit of HTD3.

引物名称 Primer name	引物序列 Primer sequences (5′→3′)
HTD3-CPT-EcoRⅠ-F	ACGAATTCGAGCTCGGTACCTGGTTCTGTGACTAAAGCGC
HTD3-CPT-HindⅢ-R	GGCCAGTGCCAAGCTTTCTCCGGGGCCCTGAATATTCCTCT

图1 野生型和htd3的形态性状比较 A~C-野生型和htd3在苗期（A）,分蘖期（B）和成熟期（C）的植株表型,标尺为6 cm;D,E-野生型和htd3的分蘖数（D）和株高（E）随播种后日期的动态变化。数据为平均值±标准差（n=15）;采用t测验,**表示在0.01水平上差异显著,*表示在0.05水平上差异显著。

Fig. 1. Morphological characterization of WT and htd3. A~C, Plant phenotypes of wild-type (WT) and htd3 in the seedling stage (A), tillering stage (B) , and mature stage (C) , bar= 6 cm; D~E, Tiller number (D) and plant height (E) of WT and htd3 after sowing. Values are means ± SD (n=15), t-test, *, ** indicate significant difference at P<0.05 and P<0.01, respectively.

表3 野生型和htd3的主要农艺性状比较

Table 3 Comparison of agronomic traits between WT and htd3.

农艺性状Agronomic trait	野生型WT	突变体htd3
株高Plant height /cm	97.08±2.78	83.76±1.54^*
有效穗数Effective panicles	11.0±1.0	28.0±2.0^**
穗长Panicle length/cm	21.52±0.98	20.82±0.62
一次枝梗数 Primary branches	12.0±2.0	9.0±1.0^*
二次枝梗数Secondary branches	26.0±3.0	23.0±4.0
每穗粒数Grains per panicle	121.0±11.0	104.0±16.0^*
每株总粒数Total grains per plant	1331±28	2018±36^**
千粒重1000-grain weight/g	23.7±2.1	23.9±1.3
结实率Seed setting rate/%	87.2±5.8	90.0±2.4

图2 野生型和htd3分蘖芽表型观察 A~F-野生型和突变体htd3在5叶期、6叶期、7叶期的分蘖芽表型, A~C为野生型, D~F为突变体, 标尺为1 cm;G-野生型和突变体htd3在各叶期的分蘖长度, n/0中n表示叶位, 0表示主茎, 即1/0表示主茎第一片叶对应的分蘖芽, 2/0表示主茎第2片叶对应的分蘖芽, 以此类推。

Fig. 2. Phenotypic observation of tillering buds of WT and htd3. A~F, Phenotype of tillering buds of WT and htd3 at five-, six- and seven-leaf stage; A-C represents WT; D-F represents htd3; bars=1 cm; G, Tillering bud length of WT and htd3 at each leaf stage, in n/0, n represents the leaf position, 0 represents the main stem, 1/0 represents the tiller bud corresponding to the first leaf of the main stem, 2/0 represents the tiller bud corresponding to the second leaf of the main stem, and so on.

表4 水稻矮秆多分蘖突变体htd3的遗传分析

Table 4 Genetic analysis of rice high-tillering mutant htd3.

组合Cross	F₁表型 Phenotype of F₁ plants	F₂群体 F₂ population			χ² _(3:1)	χ²_{0. 05}
组合Cross	F₁表型 Phenotype of F₁ plants	总株数 No. of plants	正常分蘖株数 No. of normal plants	多分蘖株数 No. of high-tillering plants	χ² _(3:1)	χ²_{0. 05}
中花11/ TN1 Zhonghua 11/TN1	正常分蘖Normal tiller	864	666	198	2	3. 84

图3 HTD3的图位克隆和互补转基因验证 A-HTD3的初定位;B-HTD3的精细定位;C-定位区间内预测的ORF;D-候选基因LOC_Os12g21710的基因结构及在野生型和htd3中的序列差异,黑色方框代表外显子,白色方框代表UTR,黑色线条代表内含子;E-野生型、htd3和互补转基因T2代植株分蘖期表型,标尺为6 cm;F~G-野生型、htd3和互补转基因T2代植株分蘖期的分蘖数(F)和株高(G)统计,数据为平均值±标准差(n=5)。用新复极差法进行多重比较,相同小写字母表示在0.05水平上无显著差异。

Fig. 3. Map-based cloning of HTD3 and verification of complementary transgene. A, Initial location of HTD3; B, Fine mapping of HTD3; C, Predicted ORFs in the location interval; D, Gene structure of the candidate gene LOC_Os12g21710 and the sequence difference between WT and htd3, in which black boxes, white boxes, black lines represent exons, UTR and introns, respectively; E, Phenotype of WT, htd3 and complementary transgenic T2 generation plants in the tilling stage, bar=6 cm; F~G, Number of tillers (F) and plant height (G) of WT, htd3 and complementary transgenic T2 generation plants in the tillering stage, the data are means ± standard deviation (n=5). Significant difference by Duncan’s multiple range test. The same letters indicate no significant difference at P<0.05.

图4 HTD3和激素相关基因的表达水平分析 A-HTD3基因在野生型和突变体htd3各组织中相对表达水平;B~C-独脚金内酯(B)和ABA(C)相关基因在野生型和突变体htd3叶片中的相对表达水平。以相应基因在野生型中的表达水平作为参考并设为1, 数据为平均值±标准差, 3次生物学重复;采用t测验, *表示在0. 05水平上差异显著, **表示在0. 01水平上差异显著。

Fig. 4. Expression analysis of HTD3 and hormone related genes. A, HTD3 relative expression level in various tissues of WT and htd3; B-C, Relative expression of SLs (B) and ABA (C) related genes in WT and htd3. RNA was isolated from WT and htd3 leaves in B and C. Expression levels are represented as relative to the corresponding genes in WT (set as reference value of 1), and data are shown as means ± SD from three biological replicates. Asterisks indicate statistical significance between the WT and the mutant, as determined by Student’s t-test (*P < 0.05; **P < 0.01).

图5 HTD3的单倍型分析 A-HTD3的基因结构及147份水稻品种中HTD3的5'-UTR和编码区上核苷酸多态性, 黑色方块代表外显子, 白色方框代表UTR, 黑色方框之间的黑色线条代表内含子, Hap代表单倍型, 数字代表相对起始密码子ATG的碱基位置;B-每种单倍型对应的分蘖数和株高。用新复极差法进行多重比较, 相同小写字母表示在0.05水平上无显著差异。

Fig. 5. Analysis of the HTD3 gene haplotypes. A, Gene structure of the HTD3, and nucleotide polymorphisms in the HTD3 5'-UTR and coding region, exons are indicated by black boxes, UTRs are indicated by white boxes, and the black lines between black boxes represent introns, hap means haplotypes, the number represents the base position relative to the start codon ATG. B, Tiller number and plant height of each haplotype. Significant difference by Duncan’s multiple range test. The same letters indicate no significant difference at P<0.05.

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水稻分蘖调控基因HTD3的克隆与功能研究

Cloning and Functional Analysis of Rice Tillering Regulatory Gene HTD3

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[1]	汪邑晨, 朱本顺, 周磊, 朱骏, 杨仲南. 光/温敏核不育系的不育机理及两系杂交稻的发展与展望 [J]. 中国水稻科学, 2024, 38(5): 463-474.
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[4]	吕阳, 刘聪聪, 杨龙波, 曹兴岚, 王月影, 童毅, Mohamed Hazman, 钱前, 商连光, 郭龙彪. 全基因组关联分析(GWAS)鉴定水稻氮素利用效率候选基因 [J]. 中国水稻科学, 2024, 38(5): 516-524.
[5]	杨好, 黄衍焱, 王剑, 易春霖, 石军, 谭楮湉, 任文芮, 王文明. 水稻中八个稻瘟病抗性基因特异分子标记的开发及应用 [J]. 中国水稻科学, 2024, 38(5): 525-534.
[6]	杨铭榆, 陈志诚, 潘美清, 张汴泓, 潘睿欣, 尤林东, 陈晓艳, 唐莉娜, 黄锦文. 烟-稻轮作下减氮配施生物炭对水稻茎鞘同化物转运和产量形成的影响 [J]. 中国水稻科学, 2024, 38(5): 555-566.
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[10]	许丹洁, 林巧霞, 李正康, 庄小倩, 凌宇, 赖美玲, 陈晓婷, 鲁国东. OsOPR10正调控水稻对稻瘟病和白叶枯病的抗性[J]. 中国水稻科学, 2024, 38(4): 364-374.
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[15]	陈浩田, 秦缘, 钟笑涵, 林晨语, 秦竞航, 杨建昌, 张伟杨. 水稻根系和土壤性状与稻田甲烷排放关系的研究进展[J]. 中国水稻科学, 2024, 38(3): 233-245.