Identification and Gene Mapping of Male Sterile Mutant gamyb5 in Rice

doi:10.16819/j.1001-7216.2016.5154

Chinese Journal OF Rice Science ›› 2016, Vol. 30 ›› Issue (2): 143-151.DOI: 10.16819/j.1001-7216.2016.5154

• Orginal Article • Previous Articles Next Articles

Identification and Gene Mapping of Male Sterile Mutant gamyb5 in Rice

Zheng-fu YANG¹, Ying-xin ZHANG¹, Lian-ping SUN^1,², Pei-pei ZHANG¹, Dan-dan XUAN¹, Ling LIU^1,³, Xia HU¹, Zi-he LI¹, Xiao-deng ZHAN¹, Wei-xun WU¹, Li-yong CAO^1,^*(), Shi-hua CHENG^1,^*()

¹National Center for Rice Improvement/ Key Laboratory for Zhejiang Super Rice Research, China National Rice Research Institute, Hangzhou 311401, China
²College of Agronomy,Shenyang Agricultural University, Shenyang 110866, China
³College of Agronomy, He'nan Agricultural University, Zhengzhou 450002, China

Received:2015-10-19 Revised:2015-12-11 Online:2016-03-10 Published:2016-03-10
Contact: Li-yong CAO, Shi-hua CHENG
About author:
# These authors contributed equally to this work;

水稻雄性不育突变体gamyb5的鉴定与基因定位

杨正福¹, 张迎信¹, 孙廉平^1,², 张沛沛¹, 轩丹丹¹, 刘嶺^1,³, 胡霞¹, 李紫荷¹, 占小登¹, 吴玮勋¹, 曹立勇^1,^*(), 程式华^1,^*()

¹中国水稻研究所/国家水稻改良中心/浙江省超级稻研究重点实验室, 杭州 311401
²沈阳农业大学农学院, 沈阳 110866
³河南农业大学农学院, 郑州 450002

通讯作者: 曹立勇,程式华
作者简介:
# 共同第一作者;
基金资助:
农业部农业公益性行业科技专项(20140302, 20150308);国家转基因重大专项(2014ZX08001-002);浙江省自然科学基金资助项目(Q13C130009);中国农业科学院创新工程超级稻育种创新团队、水稻杂种优势机理研究创新团队项目(CAAS-ASTIP-2013-CNRRI);国家自然科学基金资助项目(31501290)

Abstract

Abstract:

The gamyb5, a pollen-free male sterile mutant was identified from the mutant library of ⁶⁰Co-γ-treated indica cultivar Zhonghui 8015. There was no significant difference in agronomic traits such as plant type, plant height and tiller number between gamyb5 and the wild-type. But gamyb5 exhibited slender and white anthers without mature pollen grains. Observation results of anther cross-sections exhibited that the microspore mother cells failed to form functional tetrads and microspores in gamyb5. Moreover, tapetal cells of gamyb5 abnormally enlarged and the tapetum programmed cell death (PCD) was delayed. gamyb5, as the pollen acceptor, was crossed with the wild type Zhonghui 8015 and a japonica cultivar 02428, respectively. Genetic analysis of all hybridization populations indicated that gamyb5 was controlled by a single recessive nuclear gene which was mapped on the long arm of chromosome 1. With developed SSR, Indel markers and F₂ mapping population of gamyb5/02428, the gene was fine mapped to a region of 16-kb on the long arm of chromosome 1 between markers ZF-29 and ZF-31. Sequence analysis of the two open reading frames in this region revealed that the LOC_Os01g0812000, which encodes a gibberellin-induced MYB transcription factor, had an 8 nucleotides bases deletion in the second extron probably responsible for the male sterility phenotype. Additionally, real-time fluorescent quantitative PCR analysis showed that the expression level of the important regulators UDT1, TDR, CYP703A3 and CYP704B2 in anther decreased significantly in gamyb5. Together, these results suggest GAMYB plays key roles in anther meiosis and tapetum PCD.

Key words: rice, male sterility, gene mapping, gamyb5

摘要：

在⁶⁰Co-γ射线辐射诱变籼稻中恢8015的突变体库内发现了一个无花粉型雄性不育突变体gamyb5。gamyb5 的株型、株高、分蘖数等农艺性状与野生型中恢8015无差异,而其花药细长且呈白色半透明状,花药中无花粉粒。花药半薄切片观察结果表明,gamyb5的小孢子母细胞减数分裂异常,没有形成正常的四分体和小孢子,并且绒毡层异常伸长,细胞程序性死亡延迟。对以gamyb5 为母本,与野生型中恢8015 和广亲和粳稻品种02428分别配制的杂交组合遗传分析表明,gamyb5 突变性状受一个隐性核基因控制。利用gamyb5 和02428 杂交的F₂定位群体,最终将突变基因精细定位于第1染色体长臂的ZF-29和ZF-31两个标记之间,物理距离约16.9 kb。对该区域内2个完整的开放阅读框测序分析发现,编码受赤霉素诱导的MYB转录因子基因LOC_Os01g0812000的第2外显子存在8个碱基的缺失,导致翻译提前终止。qRT-PCR检测到影响花药发育的调控因子UDT1、TDR、CYP703A3和CYP704B2的表达量在突变体中比野生型中极显著降低。进一步证明GAMYB在花药减数分裂和绒毡层细胞程序性死亡过程中起关键作用。

关键词: 水稻, 雄性不育, 基因定位, gamyb5

CLC Number:

Zheng-fu YANG, Ying-xin ZHANG, Lian-ping SUN, Pei-pei ZHANG, Dan-dan XUAN, Ling LIU, Xia HU, Zi-he LI, Xiao-deng ZHAN, Wei-xun WU, Li-yong CAO, Shi-hua CHENG. Identification and Gene Mapping of Male Sterile Mutant gamyb5 in Rice[J]. Chinese Journal OF Rice Science, 2016, 30(2): 143-151.

杨正福, 张迎信, 孙廉平, 张沛沛, 轩丹丹, 刘嶺, 胡霞, 李紫荷, 占小登, 吴玮勋, 曹立勇, 程式华. 水稻雄性不育突变体gamyb5的鉴定与基因定位[J]. 中国水稻科学, 2016, 30(2): 143-151.

Figures/Tables 6

Table 1 Makers used for fine mapping and sequencing.

引物名称 Primer name	上游引物 Forward primer (5'-3')	下游引物 Reverse primer (5'-3')	实验目的 Purpose
RD0114	GCTTGTGGCAATTGGG	CGCCTGATGGATGTCG	精细定位Fine mapping
ZF-26	GATCATACCATCATCAGAAGCAGT	CAAGCAGCCCACATCACAGC	精细定位Fine mapping
ZF-28	TCTCGCTCCTCTTCGCCCAAAC	ACCCGCACCAGTACGTGACCC	精细定位Fine mapping
ZF-29	GGCAGCAGCAATCACAACAC	TCGGCACTTTCTTTACTCAACT	精细定位Fine mapping
ZF-31	CAGCCAGGCACCGCAGCAAA	AAGAAAGGCAGAGCAAGAAGG	精细定位Fine mapping
ZF-32	GCACGCTTCTCGCTACGCTAT	GCTCCAGGAACACCACCAACTC	精细定位Fine mapping
ZF-38	TGGGTGCGAGGTTTCTGTGA	AATGAATGCGTGTTTCCTGT	精细定位Fine mapping
InDel15	CAACCCCTCCAAATACCTGA	ACCGTGTTCATGCCTTTCAC	精细定位Fine mapping
GAMYB5	ACTGGAGCACTGCTGATCTTC	GCACATCTTCTCAGTTGCCAG	gamyb5位点检测gamyb5 deletion site detection
cDNA	CCCCTGCGAGTCCAATCTAC	ACCGGCTTATCTCCATGCAC	cDNA测序cDNA sequencing

Fig. 1. Phenotypic comparison of wild type Zhonghui 8015(WT)and gamyb5 . A, Plant of Zhonghui 8015 and the gamyb5 mutant at the heading stage; B, Panicle of Zhonghui 8015 and the gamyb5 mutant; C, Spikelet of the wild type Zhonghui 8015 and gamyb5 ; D, Anther of Zhonghui 8015 and gamyb5 mutant; E, Pollen fertility of Zhonghui 8015 and gamyb5.

Table 2 Genetic analysis of the gamyb5 mutant.

组合 Cross	$F 1$ 结实率 Seed-setting rate of F₁ /%	F₂		$χ 3 ∶ 1 2$	$χ 0.05 2$
组合 Cross	$F 1$ 结实率 Seed-setting rate of F₁ /%	野生型植株数 Number of wild type plants		$χ 3 ∶ 1 2$	突变体植株数 Number of mutant plants
gamyb5/02428	86.8	1895	642	0.14	3.84
gamyb5/中恢8015 gamyb5/Zhonghui 8015	87.2	234	70	0.63
中恢8015/02428 Zhonghui 8015/02428	87.6	960	0	-

Table 2 Genetic analysis of the gamyb5 mutant.

组合 Cross	$F 1$ 结实率 Seed-setting rate of F₁ /%	F₂		$χ 3 ∶ 1 2$	$χ 0.05 2$
组合 Cross	$F 1$ 结实率 Seed-setting rate of F₁ /%	野生型植株数 Number of wild type plants		$χ 3 ∶ 1 2$	突变体植株数 Number of mutant plants
gamyb5/02428	86.8	1895	642	0.14	3.84
gamyb5/中恢8015 gamyb5/Zhonghui 8015	87.2	234	70	0.63
中恢8015/02428 Zhonghui 8015/02428	87.6	960	0	-

Fig.2. Positional cloning of the gamyb5 mutated gene. A, Preliminary mapping of gamyb5; B, Fine mapping of gamyb5; C, Prediction of the candidate gene within the fine-mapped region; D, The structure of candidate gene LOC_Os01g0812000 and the mutation site in gamyb5 mutant (8 bases deleted).

Fig. 3. Transverse section analyses of the wild type and gamyb5 anthers in various of developmental stages. A to E, Wild type; G to L, The gamyb5 mutant. A and G, Cross-section of anthers at the stage 7; B and H, Cross-section of anthers at the stage 8; C and I, Cross-section of anthers at the stage 9; D and J, Cross-section of anthers at the stage 10; E and K, Cross-section of anthers at the stage 11; F and L, Cross-section of anthers at the stage 12. Ep, Epidermis; En, Endothecium; ML, Middle layer; T, Tapetum; Ms, Microsporocyte; Dy, Dyad cell; Msp, Microspore; BP, Biceullar pollen; MP, Mature pollen. Bars = 20 μm.

Fig. 4. Expression analysis of male sterility-associated genes of the wild type and the mutant. **significant at P=0.01.

References 41

[1]	McCormick S. Male gametophyte development.Plant Cell,1993, 5: 1265-1275.
[2]	Scott R J, Spielman M, Dickinson H G.Stamen structure and function.Plant Cell, 2004,16(Suppl): 46-60.
[3]	Ma H.Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants.Annu Rev Plant Biol, 2005, 56: 393-434.
[4]	Zhang D B, Wilson Z A.Stamen specification and anther development in rice.Chin Sci Bull, 2009, 54: 2342-2353.
[5]	Zhang D B, Luo X, Zhu L, et al.Cytological analysis and genetic control of rice anther development.J Genet Genom, 2011, 38: 379-390.
[6]	Zhang D B, Yang L.Specification of tapetum and microsporocyte cells within the anther.Curr Opin Plant Biol, 2014, 17C: 49-55.
[7]	马西青, 方才臣, 邓联武, 等. 水稻隐性核雄性不育基因研究进展及育种应用探讨. 中国水稻科学, 2012, 26(5): 511-520.
	Ma X Q, Fang C C, Deng L W, et al.Research progress and breeding application of recessive genic male sterility genes in rice.Chin J Rice Sci, 2012, 26(5): 511-520. (in Chinese with English abstract)
[8]	Nonomura K, Miyoshi K.The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice.Plant Cell, 2003, 15(8): 1728-1739.
[9]	Ken-Ichi N, Mutsuko N, Toshiyuki F, et al.The novel gene HOMOLOGOUS PAIRING ABERRATION IN RICE MEIOSIS1 of rice encodes a putative coiled-coil protein required for homologous chromosome pairing in meiosis.Plant J, 2004, 16(4): 1008-1020.
[10]	Nonomura K I, Nakano M, Murata K, et al.An insertional mutation in the rice PAIR2 gene, the ortholog of Arabidopsis ASY1, results in a defect in homologous chromosome pairing during meiosis.Mol Genet Genom, 2004, 271(2): 121-129.
[11]	Yuan W Y, Li X W, Chang Y X, et al.Mutation of the rice gene PAIR3 results in lack of bivalent formation in meiosis.Plant J, 2009, 59(2): 303-315.
[12]	Sandra N Ol, Elizabeth S D, Rudy D.ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice.Plant Cell Physiol, 2007, 48(9): 1319-1330.
[13]	Ken-Ichi N, Akane M, Mutsuko N, et al.A germ cell-specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice.Plant Cell, 2007, 19(8): 2583-2594.
[14]	Wang C, Huang W, Ying Y H, et al.Functional characterization of the rice SPX-MFS family reveals a key role of OsSPX-MFS1 in controlling phosphate homeostasis in leaves.New Phytol, 2012, 196(1): 139-148.
[15]	Li L, Li Y X, Song S F.An anther development F-box (ADF) protein regulated by tapetum degeneration retardation (TDR) controls rice anther development.Planta, 2015, 241(1): 157-166.
[16]	Jung K H, Han M J, Lee Y S.Rice undeveloped tapetum1 is a major regulator of early tapetum development.Plant Cell, 2005, 17(10): 2705-2722.
[17]	Liu Z H, Bao W J.Identification of gamyb-4 and analysis of the regulatory role of GAMYB in rice anther development.J Integ Plant Biol, 2010, 52(7): 670-678.
[18]	Li H, Yuan Z.PERSISTENT TAPETAL CELL1 Encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice.Plant Physiol, 2011, 156(2): 615-630.
[19]	Li X W, Gao X Q.Rice APOPTOSIS INHIBITOR5 coupled with two DEAD-box adenosine 5'-triphosphate-dependent RNA helicases regulates tapetum degeneration.Plant Cell, 2011, 23(4): 1416-1434.
[20]	Jung K H, Han M J.Wax-deficient anther1 is involved in cuticle and wax production in rice anther walls and is required for pollen development.Plant Cell, 2006, 18(11): 3015-3032.
[21]	Shi J, Tan H X.Defective pollen wall is required for anther and microspore development in rice and encodes a fatty acyl carrier protein reductase.Plant Cell, 2011, 23(6): 2225-2246.
[22]	Li H, Pinot F.Cytochrome P450 family member CYP704B2 catalyzes the ω -Hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice.Plant Cell, 2010, 22(1): 173-190.
[23]	Yang X J, Wu D. rice CYP703A3, a cytochrome P450 hydroxylase, is essential for development of anther cuticle and pollen exine.J Integ Plant Biol, 2014, 56(10): 979-994.
[24]	Zhu Q H, Ramm K, Shivakkumar R, et al.The ANTHER INDEHISCENCE1 gene encoding a single MYB domain protein is involved in anther development in rice.Plant Physiol, 2004, 135(3): 1514-1525.
[25]	初明光, 李双成, 王世全, 等. 一个水稻雄性不育突变体的遗传分析和基因定位. 作物学报, 2009, 35(6): 1151-1155.
	Chu G M, Li S C, Wang S Q, et al.Genetic analysis and molecular mapping of a male sterile mutant in rice.Crop J, 2004, 135(3): 1514-1525. (in Chinese with English abstract)
[26]	卢扬江, 郑康乐. 提取水稻DNA 的一种简易方法. 中国水稻科学, 1992, 6(1): 47-48.
	Lu Y J, Zheng K L.A simple method for isolation of rice DNA.Chin J Rice Sci, 1992, 6(1): 47-48. (in Chinese with English abstract)
[27]	Orjuela J, Garavito A, Bouniol M.A universal core genetic map for rice.Theor Appl Genet, 2010,120,563-572.
[28]	Rychlik W.Oligo primer analysis software version 7.0. 2nd ed. Molecular Biology Insights, Inc, Cascade, Co, 2008.
[29]	Aya K, Miyako Ueguchi-Tanaka M. Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB.Plant Cell, 2009, 21(5): 1453-1472.
[30]	Gocal, Sheldon G F. GAMYB-like genes, flowering and gibberellin signaling in Arabidopsis. Plant Physiol, 2001,127, 1682-1693.
[31]	Gubler F, Kalla R, Roberts J K, et al.Gibberellin-regulated expression of a MYB gene in barley aleurone cells: Evidence for Myb transactivation of a high-pI α-amylase gene promoter.Plant Cell, 1995, 7: 1879-1891.
[32]	Fiona J, Woodger A M, Murray F, et al.The role of GAMYB transcription factors in GA-regulated gene expression.J Plant Growth Regul, 2003, 22, 176-184.
[33]	Kaneko M, Inukai Y, Ueguchi-Tanaka M. loss-of-function mutations of the rice GAMYB gene impair α-amylase expression in aleurone and flower development.Plant Cell, 2004,16:1473-1487.
[34]	Aya K, Ueguchi-Tanaka M, Kondo M, et al.Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB.Plant Cell, 2009, 21:1453-1472.
[35]	Wang Y, Wang Y F, Zhang D B.Identification of the rice (Oryza sativa L.) mutant msp1-4 and expression analysis of its UDT1 and GAMYB genes.J Plant Physiol Mol Biol, 2006 , 32: 527-534.
[36]	Morant M, Jorgensen K, Schaller H.CYP703 is an ancient cytochrome P450 in land plants catalyzing in-chain hydroxylation of lauric acid to provide building blocks for sporopollenin synthesis in pollen.Plant Cell, 2007, 19:1473-1487.
[37]	Dobritsa A A, Shrestha J, Morant M.CYP704B1 is a long-chain fatty acid ω-hydroxylase essential for sporopollenin synthesis in pollen of Arabidopsis.Plant Physiol, 2009, 151: 574-589.
[38]	Bouquin L, Pinot R, Benveniste F, et al.Cloning and functional characterization of CYP94A2, a medium chain fatty acid hydroxylase from Vicia sativa. Biochem. Biophys.Res Commun, 1999, 261: 156-162.
[39]	Kurdyukov S, Faust A, Trenkamp S.Genetic and biochemical evidence for involvement of HOTHEAD in the biosynthesis of long-chain alpha-omega-dicarboxylic fatty acids and formation of extracellular matrix.Planta, 2006, 224: 315-329.
[40]	Kandel S, Sauveplane V, Compagnon V.Characterization of a methyl jasmonate and wounding-responsive cytochrome P450 of Arabidopsis thaliana catalyzing dicarboxylic fatty acid formation in vitro.FEBS J, 2007, 274: 5116-5127.
[41]	Sauveplane V, Kandel S, Kastner P E.Arabidopsis thaliana CYP77A4 is the first cytochrome P450 able to catalyze the epoxidation of free fatty acids in plants.FEBS J, 2009, 276: 719-735.

Identification and Gene Mapping of Male Sterile Mutant gamyb5 in Rice

水稻雄性不育突变体gamyb5的鉴定与基因定位

RichHTML

PDF

Knowledge

Abstract

Cite this article

share this article

Figures/Tables 6

References 41

Related Articles 15

Recommended Articles

Metrics

[1]	GUO Zhan, ZHANG Yunbo. Research Progress in Physiological，Biochemical Responses of Rice to Drought Stress and Its Molecular Regulation [J]. Chinese Journal OF Rice Science, 2024, 38(4): 335-349.
[2]	WEI Huanhe, MA Weiyi, ZUO Boyuan, WANG Lulu, ZHU Wang, GENG Xiaoyu, ZHANG Xiang, MENG Tianyao, CHEN Yinglong, GAO Pinglei, XU Ke, HUO Zhongyang, DAI Qigen. Research Progress in the Effect of Salinity, Drought, and Their Combined Stresses on Rice Yield and Quality Formation [J]. Chinese Journal OF Rice Science, 2024, 38(4): 350-363.
[3]	XU Danjie, LIN Qiaoxia, LI Zhengkang, ZHUANG Xiaoqian, LING Yu, LAI Meiling, CHEN Xiaoting, LU Guodong. OsOPR10 Positively Regulates Rice Blast and Bacterial Blight Resistance [J]. Chinese Journal OF Rice Science, 2024, 38(4): 364-374.
[4]	CHEN Mingliang, ZENG Xihua, SHEN Yumin, LUO Shiyou, HU Lanxiang, XIONG Wentao, XIONG Huanjin, WU Xiaoyan, XIAO Yeqing. Typing of Inter-subspecific Fertility Loci and Fertility Locus Pattern of indica-japonica Hybrid Rice [J]. Chinese Journal OF Rice Science, 2024, 38(4): 386-396.
[5]	DING Zhengquan, PAN Yueyun, SHI Yang, HUANG Haixiang. Comprehensive Evaluation and Comparative Analysis of Jiahe Series Long-Grain japonica Rice with High Eating Quality Based on Gene Chip Technology [J]. Chinese Journal OF Rice Science, 2024, 38(4): 397-408.
[6]	HOU Xiaoqin, WANG Ying, YU Bei, FU Weimeng, FENG Baohua, SHEN Yichao, XIE Hangjun, WANG Huanran, XU Yongqiang, WU Zhihai, WANG Jianjun, TAO Longxing, FU Guanfu. Mechanisms Behind the Role of Potassium Fulvic Acid in Enhancing Salt Tolerance in Rice Seedlings [J]. Chinese Journal OF Rice Science, 2024, 38(4): 409-421.
[7]	LÜ Zhou, YI Binghuai, CHEN Pingping, ZHOU Wenxin, TANG Wenbang, YI Zhenxie. Effects of Nitrogen Application Rate and Transplanting Density on Yield Formation of Small Seed Hybrid Rice [J]. Chinese Journal OF Rice Science, 2024, 38(4): 422-436.
[8]	HU Jijie, HU Zhihua, ZHANG Junhua, CAO Xiaochuang, JIN Qianyu, ZHANG Zhiyuan, ZHU Lianfeng. Effects of Rhizosphere Saturated Dissolved Oxygen on Photosynthetic and Growth Characteristics of Rice at Tillering Stage [J]. Chinese Journal OF Rice Science, 2024, 38(4): 437-446.
[9]	WU Yue, LIANG Chengwei, ZHAO Chenfei, SUN Jian, MA Dianrong. Occurrence of Weedy Rice Disaster and Ecotype Evolution in Direct-Seeded Rice Fields [J]. Chinese Journal OF Rice Science, 2024, 38(4): 447-455.
[10]	LIU Fuxiang, ZHEN Haoyang, PENG Huan, ZHENG Liuchun, PENG Deliang, WEN Yanhua. Investigation and Species Identification of Cyst Nematode Disease on Rice in Guangdong Province [J]. Chinese Journal OF Rice Science, 2024, 38(4): 456-461.
[11]	CHEN Haotian, QIN Yuan, ZHONG Xiaohan, LIN Chenyu, QIN Jinghang, YANG Jianchang, ZHANG Weiyang. Research Progress on the Relationship Between Rice Root, Soil Properties and Methane Emissions in Paddy Fields [J]. Chinese Journal OF Rice Science, 2024, 38(3): 233-245.
[12]	MIAO Jun, RAN Jinhui, XU Mengbin, BO Liubing, WANG Ping, LIANG Guohua, ZHOU Yong. Overexpression of RGG2, a Heterotrimeric G Protein γ Subunit-Encoding Gene, Improves Drought Tolerance in Rice [J]. Chinese Journal OF Rice Science, 2024, 38(3): 246-255.
[13]	YIN Xiaoxiao, ZHANG Zhihan, YAN Xiulian, LIAO Rong, YANG Sijia, Beenish HASSAN, GUO Daiming, FAN Jing, ZHAO Zhixue, WANG Wenming. Signal Peptide Validation and Expression Analysis of Multiple Effectors from Ustilaginoidea virens [J]. Chinese Journal OF Rice Science, 2024, 38(3): 256-265.
[14]	ZHU Yujing, GUI Jinxin, GONG Chengyun, LUO Xinyang, SHI Jubin, ZHANG Haiqing, HE Jiwai. QTL Mapping for Tiller Angle in Rice by Genome-wide Association Analysis [J]. Chinese Journal OF Rice Science, 2024, 38(3): 266-276.
[15]	WEI Qianqian, WANG Yulei, KONG Haimin, XU Qingshan, YAN Yulian, PAN Lin, CHI Chunxin, KONG Yali, TIAN Wenhao, ZHU Lianfeng, CAO Xiaochuang, ZHANG Junhua, ZHU Chunqun. Mechanism of Hydrogen Sulfide, a Signaling Molecule Involved in Reducing the Inhibitory Effect of Aluminum Toxicity on Rice Growth Together with Sulfur Fertilizer [J]. Chinese Journal OF Rice Science, 2024, 38(3): 290-302.