芝麻SiHEC3基因上游从5’UTR起的1049 bp序列缺失引起种子不落粒的突变

doi:10.1016/j.jia.2023.11.012

Journal of Integrative Agriculture ›› 2024, Vol. 23 ›› Issue (8): 2589-2604.DOI: 10.1016/j.jia.2023.11.012

芝麻SiHEC3基因上游从5’UTR起的1049 bp序列缺失引起种子不落粒的突变

收稿日期:2023-08-23 接受日期:2023-10-08 出版日期:2024-08-20 发布日期:2024-07-29

Deletion of a 1,049 bp sequence from the 5´ UTR upstream of the SiHEC3 gene induces a seed non-shattering mutation in sesame

Ming Ju^{1, 2, 3}, Guiting Li^{1, 2, 3}, Qiuzhen Tian^{1, 2, 3}, Hengchun Cao^{1, 2, 3}, Qin Ma^{1, 2, 3}, Yinghui Duan^{1, 2, 3}, Hui Guo^{1, 2, 3}, Zhanyou Zhang^{1, 2, 3}, Yingying Huang^{1, 2, 3}, Huili Wang^{1, 2, 3}, Haiyang Zhang^{1, 2, 3#}, Hongmei Miao^{1, 2, 3#}

¹ The Shennong Laboratory, Zhengzhou 450002, China
² Henan Sesame Research Center, Henan Academy of Agricultural Sciences, Zhengzhou 450002, China
³ Key Laboratory of Specific Oilseed Crops Genomics of Henan Province, Henan Sesame Research Center, Henan Academy of Agricultural Sciences, Zhengzhou 450002, China

Received:2023-08-23 Accepted:2023-10-08 Online:2024-08-20 Published:2024-07-29
About author:Ming Ju, Tel/Fax: +86-371-65720774, E-mail: jumingzz@163.com; #Correspondance Hongmei Miao, Tel/Fax: +86-371-65720774, E-mail: miaohongmeichina@163.com; Haiyang Zhang, Tel/Fax: +86-371-65720774, E-mail: zhanghaiyang@zzu.edu.cn
Supported by:
This work was financially supported by the earmarked funding for the China Agriculture Research System of MOF and MARA (CARS-14), the Key Project of Science and Technology of Henan Province, China (201300110600), the Henan Province Specific Professor Position Program, China (SPPP2022), the Zhongyuan Scientist Workshop Construction, China (ZSWC2019 and 214400510026), the Innovation Scientist and Technician Troop Construction Project of Henan Province, China (ISTTCPHP2016), the Shennong Laboratory First Class Program, China (SN01-2022-04), the Key Research and Development Project of Henan Province, China (221111520400), the Innovation Scientists and Technicians Troop Construction Project of Henan Academy of Agricultural Sciences, China (2023TD04), and the Henan Province Science and Technology Research and Development Plan Joint Fund, China (232301420108).

摘要/Abstract

摘要：

芝麻由于落粒性是一种机械化程度较低的劳动密集型作物。本研究以抗落粒芝麻突变体12M07为材料开展了抗落粒性状的遗传解析。与落粒型不同，12M07突变体脱落区的薄壁细胞排列松散，但紧贴在种皮上。对12M07 (抗落粒型) ×项城大籽白(落粒型) 六世代的遗传分析表明，抗落粒性状为隐性性状，受单基因对控制。对上述亲本的F₂群体的888,619个变体(snp和InDels)和31,884个结构变异(SV)的关联分析结果显示只有SV12002位点与抗落粒性状显著相关，此结构变异位于SiChr3中的Sindi0765000基因 (命名为SiHEC3)上游5'UTR区域。SiHEC3编码HLH转录因子。12M07突变体中Sihec3基因从5 ' UTR开始至上游启动子出现了1049 bp的缺失。SiHEC3基因主要在发育中的胎座组织中表达，并且在授粉后45 d达到表达高峰。在烟草中进行的双荧光素酶报告基因实验证实，Sihec3的启动子活性由于缺失1049bp的启动子序列而降低。蛋白-蛋白互作网络分析表明，HEC3与9个关键蛋白共表达，比如参与植物脱落层次生壁生物合成的SHATTERPROOF1 (SHP1)和SEEDSTICK (STK)。研究结果显示SiHEC3基因与落粒性状相对应的重要功能，为芝麻等作物宜机收新品种选育提供了基因信息。

Abstract:

Sesame is a labor intensive crop with limited mechanized harvesting mainly due to the seed shattering (SS) trait. In this study, we performed a genetic analysis of the seed-shattering resistance (SR) trait with a SR sesame mutant 12M07. Unlike the SS type, the parenchyma cells in the abscission zone of the 12M07 mutant are arranged loosely but adhere to the seed coat. Inheritance analysis of six generations derived from 12M07 (SR)×Xiangcheng Dazibai (SS) showed that the SR trait is recessive and controlled by a single gene pair. Association mapping of the F₂ population with 888,619 variants (single-nucleotide polymorphisms (SNPs) and insertion-deletion (InDels)) and 31,884 structural variations (SVs) determined that only SV12002 in the 5´ upstream region of gene Sindi0765000 (named SiHEC3) in Chr.3 was significantly associated with the SR trait. SiHEC3 encodes the bHLH transcription factor. A 1,049 bp deletion occurred in the 5´ UTR of Sihec3 in 12M07. SiHEC3 is mainly expressed in developing placental tissues, with the expression peaking in capsules at 45 days after pollination. A dual-luciferase reporter assay in tobacco confirmed that the promoter activity of Sihec3 was reduced because of the deletion of the 1,049 bp promoter sequence. Protein–protein interaction network analysis showed that HEC3 is co-expressed with nine key proteins, such as SHATTERPROOF1 (SHP1) and SEEDSTICK (STK) which participate in the secondary wall biosynthesis of the abscission layer in plants. The findings of this study show the important function of Sihec3 corresponding with the SR trait and supply the genetic information for breeding new varieties that are amenable to mechanized harvesting in sesame and other crops.

Key words: sesame (Sesamum indicum L.) , association mapping , seed shattering , structure variation , bHLH transcription factor

Ming Ju, Guiting Li, Qiuzhen Tian, Hengchun Cao, Qin Ma, Yinghui Duan, Hui Guo, Zhanyou Zhang, Yingying Huang, Huili Wang, Haiyang Zhang, Hongmei Miao. 芝麻SiHEC3基因上游从5’UTR起的1049 bp序列缺失引起种子不落粒的突变[J]. Journal of Integrative Agriculture, 2024, 23(8): 2589-2604.

Ming Ju, Guiting Li, Qiuzhen Tian, Hengchun Cao, Qin Ma, Yinghui Duan, Hui Guo, Zhanyou Zhang, Yingying Huang, Huili Wang, Haiyang Zhang, Hongmei Miao. Deletion of a 1,049 bp sequence from the 5´ UTR upstream of the SiHEC3 gene induces a seed non-shattering mutation in sesame [J]. Journal of Integrative Agriculture, 2024, 23(8): 2589-2604.

参考文献

Ahmed J, Qadir G, Ansar M, Wattoo F M, Javed T, Ali B, Marc R A, Rahimi M. 2023. Shattering and yield expression of sesame (Sesamum indicum L.) genotypes influenced by paclobutrazol concentration under rainfed conditions of Pothwar. BMC Plant Biology, 23, 137.

Baima S, Possenti M, Matteucci A, Wisman E, Altamura M M, Ruberti I, Morelli G. 2001. The Arabidopsis ATHB-8 HD-Zip protein acts as a differentiation-promoting transcription factor of the vascular meristems. Plant Physiology, 126, 643–655.

Ballester P, Martínez-Godoy M A, Ezquerro M, Navarrete-Gómez M, Trigueros M, Rodríguez-Concepción M, Ferrándiz C. 2021. A transcriptional complex of NGATHA and bHLH transcription factors directs stigma development in Arabidopsis. Plant Cell, 33, 3645–3657.

Bolger M E, Weisshaar B, Scholz U, Stein N, Bjorn U, Mayer K F. 2014. Plant genome sequencing - Applications for crop improvement. Current Opinion Biotechnology, 26, 31–37.

Bradbury P J, Zhang Z, Kroon D E, Casstevens T M, Buckler E S. 2007. TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics, 23, 2633–2635.

Cagirgan M I. 2001. Mutation techniques in sesame (Sesamum indicum L.) for intensive management: Confirmed mutant. In: Van Zanten, ed., Sesame Improvement by Induced Mutations. IAEA-TECDOC-1195, International Atomic Energy Agency, Vienna. pp. 31–40.

Cameron D L, Baber J, Shale C, Valle-Inclan J E, Besselink N, Cuppen E, Priestley P, Papenfuss A T. 2021. GRIDSS2: comprehensive characterisation of somatic structural variation using single breakend variants and structural variant phasing. Genome Biology, 22, 202.

Chen X, Schulz-Trieglaff O, Shaw R, Barnes B, Schlesinger F, Källberg M, Cox A J, Kruglyak S, Saunders C T. 2016. Manta: Rapid detection of structural variants and indels for germline and cancer sequencing applications. Bioinformatic, 32, 1220–1222.

Child R D, Summers J E, Babij J, Farrent J W, Bruce D M. 2003. Increased resistance to pod shatter is associated with changes in the vascular structure in pods of a resynthesized Brassica napus line. Journal of Experiment Botany, 54, 1919–1930.

Couch A, Gloaguen R M, Langham D R, Hochmuth G, Bennett J M, Rowland D. 2017. Non-dehiscent sesame (Sesamum indicum L.) its unique production potential and expansion into the southeastern USA. Journal of Crop Improvement, 31, 101–172.

Dong Y, Yang X, Liu J, Wang B H, Liu B L, Wang Y Z.2014. Pod shattering resistance associated with domestication is mediated by a NAC gene in soybean. Nature Communication, 5, 3352.

Dirks-Mulder A, Ahmed I, Uit Het Broek M, Krol L, Menger N, Snier J, van Winzum A, de Wolf A, Van’t Wout M, Zeegers J J, Butôt R, Heijungs R, van Heuven B J, Kruizinga J, Langelaan R, Smets E F, Star W, Bemer M, Gravendeel B. 2019. Morphological and molecular characterization of orchid fruit development. Frontiers in Plant Science, 10, 137.

Feller A, Hernandez J M, Grotewold E. 2006. An ACT-like domain participates in the dimerization of several plant basic-helix-loop-helix transcription factors. Journal of Biological Chemistry, 281, 28964–28974.

Georgiev S, Stamatov S, Deshev M. 2009. Requirements to sesame (Sesamum indicum L.) cultivars breeding for mechanized harvesting. Bulgarian Journal of Agricultural Science, 15, 26–30.

Gremski K, Ditta G, Yanofsky M F. 2007. The HECATE genes regulate female reproductive tract development in Arabidopsis thaliana. Development, 134, 3593–3601.

Harris J C, Hrmova M, Lopato S, Langridge P. 2011. Modulation of plant growth by HD-Zip class I and II transcription factors in response to environmental stimuli. New Phytologist, 190, 823–837.

Heim M A, Jakoby M, Werber M, Martin C, Weisshaar B, Bailey P C. 2003. The basic helix-loop-helix transcription factor family in plants: A genome-wide study of protein structure and functional diversity. Molecular Biology and Evolution, 20, 735–747.

Jeffares D C, Jolly C, Hoti M, Speed D, Shaw L, Rallis C, Balloux F, Dessimoz C, BäHler J, Sedlazeck F J. 2017. Transient structural variations have strong effects on quantitative traits and reproductive isolation in fission yeast. Nature Communication, 8, 14061.

Jimoh W A, Aroyehun H T. 2011. Evaluation of cooked and mechanically defatted sesame (Sesamum indicum) seed meal as a replacer for soybean meal in the diet of African catfish (Clarias gariepinus). Turkish Journal of Fisheries and Aquatic Sciences, 11, 185–190.

Ju M, Miao H M, Wang H L, Zhang H Y. 2021. Mutagenesis for creation of genetic variability in sesame. In: Miao H M, Zhang H Y, Kole C, eds., The Sesame Genome. Springer Publishing, Cham. pp. 121–129.

Langham D G. 1946. Genetics of sesame: III. “Open sesame” and mottled leaf. Journal of Heredity, 37, 149–152.

Langham D R. 2000. Method for Making Non-Dehiscent Sesame. United States Patent, Application No. 6,100,452

Langham D R. 2011. Non-Dehiscent Pygmy Sesame Variety Sesaco 70. United States Patent, Application No. 8,058,503 B1.

Langham D R. 2013. Method for Breeding Improved Non-Dehiscent Sesame. United States Patent, Application No. 8,581,028 B2.

Langham D R, Wiemers T. 2002. Progress in mechanizing sesame in the US through breeding. In: Janick J, ed., Trends in New Crops and New Uses. ASHS (American Society for Horticultural Science) Press, Alexandria, VA. pp. 157–173.

Layer R M, Chiang C, Quinlan A R, Hall I M. 2014. LUMPY: A probabilistic framework for structural variant discovery. Genome Biology, 15, R84.

Li F, Numa H, Hara N, Sentoku N, Ishii T, Fukuta Y, Nishimura N, Kato H. 2019. Identification of a locus for seed shattering in rice (Oryza sativa L.) by combining bulked segregant analysis with whole-genome sequencing. Molecular Breeding, 39, 36.

Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754–1760.

Liljegren S J, Ditta G S, Eshed Y, Savidge B, Bowman J L, Yanofsky M F. 2000. SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature, 404, 766.

Liljegren S J, Roeder A H, Kempin S A, Gremski K, Østergaard L, Guimil S, Reyes D K, Yanofsky M F. 2004. Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell, 116, 843–853.

Lin Z, Griffith M E, Li X, Zhu Z, Tan L, Fu Y, Zhang W, Wang X, Xie D, Sun C. 2007. Origin of seed shattering in rice (Oryza sativa L.). Planta, 226, 11–20.

Lin Z, Hong Y, Yin M, Li C, Zhang K, Grierson D. 2008. A tomato HD-Zip homeobox protein, LeHB-1, plays an important role in floral organogenesis and ripening. Plant Journal, 55, 301–310.

Lin Z, Li X, Shannon L M, Yeh C T, Wang M L, Bai G, Peng Z, Li J, Trick H N, Clemente T E, Doebley J, Schnable P S, Tuinstra M R, Tesso T T, White F, Yu J. 2012. Parallel domestication of the Shattering1 genes in cereals. Nature Genetics, 44, 720–724.

Liu Y Y, Wu K, Mei H X, Du Z W, Cui C Q, Jiang X L, Zheng Y Z. 2020. Cloning and prokaryotic expression of capsule indehiscent gene SiIND1 from sesame. Journal of Henan Agricultural Science, 49, 63–68. (in Chinese)

Maity A, Lamichaney A, Joshi D C, Bajwa A, Subramanian N, Walsh M, Bagavathiannan M. 2021. Seed shattering: A trait of evolutionary importance in plants. Frontiers in Plant Science, 12, 657773.

Makinde F M, Akinoso R. 2013. Nutrient composition and effect of processing treatments on anti nutritional factors of Nigerian sesame (Sesamum indicum Linn) cultivars. International Food Research Journal, 20, 2293–2300.

Miao H, Wang L, Qu L, Liu H, Sun Y, Le M, Wang Q, Wei S, Zheng Y, Lin W, Duan Y, Cao H, Xiong S, Wang X, Wei L, Li C, Ma Q, Ju M, Zhao R, Li G, et al. 2024. Genomic evolution and insights into agronomic trait innovations of Sesamum species. Plant Communications, 5, 100729.

Miao H M, Langham D R, Zhang H Y. 2021. Botanical descriptions of sesame. In: Miao H M, Zhang H Y, Kole C, eds., The Sesame Genome. Springer Publishing, Cham. pp. 19–57.

Miao H M, Li C, Duan Y H, Wei L B, Ju M, Zhang H Y. 2020. Identification of a Sidwf1 gene controlling short internode length trait in the sesame dwarf mutant dw607. Theoretical and Applied Genetics, 133, 73–86.

Phumichai C, Matthayatthaworn W, Chuenpom N, Wongkaew A, Kaveeta R. 2017. Identification of a scar marker linked to a shattering resistance trait in sesame. Turkish Journal of Field Crops, 22, 258–265.

Pinyopich A, Ditta G S, Savidge B, Liljegren S J, Baumann E, Wisman E, Yanofsky M F. 2003. Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature, 424, 85.

Uzun B, Çağırgan M İ. 2009. Identification of molecular markers linked to determinate growth habit in sesame. Euphytica, 166, 379–384.

Rausch T, Zichner T, Schlattl A, Stütz A M, Beneš V, Korbel J O. 2012. DELLY: Structural variant discovery by integrated paired-end and split-read analysis. Bioinformatics, 28, 333–339.

Rieu P, Turchi L, Thévenon E, Zarkadas E, Nanao M, Chahtane H, Tichtinsky G, Lucas J, Blanc-Mathieu R, Zubieta C, Schoehn G, Parcy F. 2023. The F-box protein UFO controls flower development by redirecting the master transcription factor LEAFY to new cis-elements. Nature Plants, 9, 315–329.

Schwager K M, Calderon-Villalobos L, Dohmann E, Willige B, Knierer S, Nill C, Schwechheimer C. 2007. Characterization of the VIER F-BOX PROTEINE genes from Arabidopsis reveals their importance for plant growth and development. The Plant Cell, 19, 1163–1178.

Sene B, Sarr F, Sow M S, Diouf D, Niang M. 2017. Physico-chemical composition of the sesame variety (Sesamum indicum L.) and characterization of its derived products (seeds, oil and oilcake) in Senegal. Food Science and Quality Management, 65, 5–10.

Szklarczyk D, Gable A L, Nastou K C, Lyon D, Kirsch R, Pyysalo S, Doncheva N T, Legeay M, Fang T, Bork P, Jensen L J, von Mering C. 2021. The STRING database in 2021: Customizable protein-protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Research, 49, D605–D612.

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.

Teboul N, Magder A, Zilberberg M, Peleg Z. 2022. Elucidating the pleiotropic effects of sesame KANADI1 locus on leaf and capsule development. Plant Journal, 110, 88–102.

Wang H L, Zhang H Y, Ma Q, Wei L B, Ju M, Li C, Duan Y H, Miao H M. 2017. Optimization of EMS mutagenesis condition and screening of mutants in sesame. Journal of Henan Agricultural Science, 46, 36–41. (in Chinese)

Wang J, Zhang Z. 2021. GAPIT version 3: Boosting power and accuracy for genomic association and prediction. Genomics Proteomics Bioinformatics, 19, 629–640.

Wei L B, Miao H M, Zhao R H, Han X H, Zhang T D, Zhang H Y. 2013. Identification and testing of reference genes for Sesame gene expression analysis by quantitative real-time PCR. Planta, 237, 873–889.

Xu Y Z, Kanagaratham C, Jancik S, Radzioch D. 2013. Promoter deletion analysis using a dual-luciferase reporter system. Methods in Molecular Biology, 977, 79–93.

Yol E, Basak M, Kızıl S, Lucas S J, Uzun B. 2021. A High-density SNP genetic map construction using ddRAD-seq and mapping of capsule shattering trait in sesame. Frontiers in Plant Science, 12, 679659.

Zhang H Y, Langham D R, Miao H M. 2021a. Economic and academic importance of sesame. In: Miao H M, Zhang H Y, Kole C, eds., The Sesame Genome. Springer Publishing, Cham. pp. 1–18.

Zhang H Y, Langham D R, Miao H M. 2021b. Prospect of designed breeding in sesame in the post-genomics era. In: Miao H M, Zhang H Y, Kole C, eds., The Sesame Genome. Springer Publishing, Cham. pp. 291–296.

Zhang H Y, Miao H M, Ju M. 2019. Potential for adaptation to climate change through genomic breeding in sesame. In: Kole C, ed., Genomic Designing of Climate-Smart Oilseed Crops. Springer Publishing, Cham, Switzerland. pp. 374–376.

Zhang H Y, Miao H M, Li C, Wei L B, Duan Y H, Ma Q, Kong J J, Xu F F, Chang S X. 2016. Ultra-dense SNP genetic map construction and identification of SiDt gene controlling the determinate growth habit in Sesamum indicum L. Scientific Reports, 6, 31556.

Zhang H Y, Miao H M, Wang L, Qu L B, Liu H Y, Wang Q, Yue M W. 2013. Genome sequencing of the important oilseed crop Sesamum indicum L. Genome Biology, 14, 401.

Zhang H Y, Miao H M, Wei L B, Li C, Duan Y H, Xu F F, Qu W W, Zhao R H, Ju M, Chang S X. 2018. Identification of a SiCL1 gene controlling leaf curling and capsule indehiscence in sesame via cross-population association mapping and genomic variants screening. BMC Plant Biology, 18, 296.

Zhao Y Q, Zhang J C, Zhang Z Y, Xie W G. 2019. Elymus nutans genes for seed shattering and candidate gene-derived EST-SSR markers for germplasm evaluation. BMC Plant Biology, 19, 10.

芝麻SiHEC3基因上游从5’UTR起的1049 bp序列缺失引起种子不落粒的突变

Deletion of a 1,049 bp sequence from the 5´ UTR upstream of the SiHEC3 gene induces a seed non-shattering mutation in sesame

PDF

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 0

编辑推荐

Metrics