Abstract
Key message
A 4.43-Kb structural variation in the sesame genome results in the deletion of the Siofp1 gene and induces the long capsule length trait.
Abstract
Capsule length (CL) has a positive effect on seed weight and yield in various agronomically important species; however, the molecular mechanism underlying long capsule trait regulation in sesame remains unknown. The inheritance analysis showed that long capsule traits (CL > 4.0 cm) were dominant over normal length (average CL = 3.0 cm) and were controlled by a single gene pair. Association mapping with a RIL population and 259 natural sesame germplasm accessions indicated that the target interval was 52,830–730,961 bp of SiChr.10 in sesame. Meanwhile, the structural variation (SV) of the association mapping revealed that only SV_414325 on chromosome 10 was significantly associated with the CL trait, with a P value of 1.1135E−19. SV_414325 represents a 4430-bp deletion from 414,325 to 418,756 bp on SiChr.10, covering Sindi_2155000 (named SiOFP1). In the normal length type, Siofp1 encodes 411 amino acids of the ovate family proteins and is highly expressed in the leaf, stem, bud, and capsule tissues of sesame. In accordance with the transcriptional repressor character, Siofp1 overexpression in transgenic Arabidopsis (T0 and T1 generations) induced a 25–39% greater shortening of silique length than the wild type (P < 0.05), as well as round cauline leaves and short carpels. These results confirm that SiOFP1 plays a key role in regulating CL trait in sesame and other flowering plants. These findings provide a theoretical and material basis for sesame capsule development and high-yield breeding research.
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Data availability
The cDNA sequence of Siofp1 gene has been submitted to NCBI dataset (NCBI accession no. MT394498). All data supporting the conclusions of this article are provided within the article (and its Supplementary Information).
Abbreviations
- CL:
-
Capsule length
- DELs:
-
Deletions
- DUPs:
-
Duplications
- EMS:
-
Ethylmethane sulfonate
- GLM:
-
General linear model
- GN:
-
Grain number per capsule
- GWAS:
-
Genome-wide association studies
- INSs:
-
Insertions
- INVs:
-
Inversions
- InDel:
-
Insertion–deletion
- KEGG:
-
Kyoto Encyclopedia of Genes and Genomes
- LD:
-
Linkage disequilibrium
- LG:
-
Linkage group
- NR:
-
Non-redundant
- PCA:
-
Principal component analysis
- OFP:
-
Ovate family protein
- QTL:
-
Quantitative trait loci
- qRT-PCR:
-
Quantitative real-time PCR
- RIL:
-
Recombinant inbred line
- SV:
-
Structural variation
- SNP:
-
Single nucleotide polymorphism
- TRAs:
-
Translocations
References
Agrawal MM, Singh S, Wawge MN, Macwana S, Sasidharan N (2017) Correlation and path analysis for seed yield and yield attributing traits in Sesame germplasm (Sesamum indicum L.). Int J Chem Stud 5:1099–1102
Akbar F, Rabbani MA, Shinwari ZK, Khan SJ (2011) Genetic divergence in sesame (Sesamum indicum L.) landraces based on qualitative and quantitative traits. Pak J Bot 43:2737–2744
Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664
Alvarez JP, Smyth DR (2002) CRABS CLAW and SPATULA genes regulate growth and pattern formation during gynoecium development in Arabidopsis thaliana. Int J Plant Sci 163:17–41
Anderson AD, Weir BS (2007) A maximum-likelihood method for the estimation of pairwise relatedness in structured populations. Genetics 176:421–440
Ashri A (2001) Induced mutations in sesame breeding. IAEA: Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, Vienna (Austria) Contract No: IAEA-TECDOC-1195 PP 13–20
Aye M, Win S, Hom NH (2018) Combining ability and heterosis studies in sesame (Sesamum indicum L.) genotypes. Int J Adv Res 6:1220–1229
Bakheit BR, Ismail AA, El-Shiemy AA, Sedek FS (2001) Triple test cross analysis in four sesame crosses (Sesamum indicum L.). J Agric Sci 137:185–193
Balasubramanian S, Schneitz K (2002) NOZZLE links proximal-distal and adaxial-abaxial pattern formation during ovule development in Arabidopsis thaliana. Development 129:4291–4300
Bolger AM, Marc L, Bjoern U (2014) Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 30:2114–2120
Bowman J, Smyth D (1999) CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 126:2387
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635
Cameron DL, Baber J, Shale C, Valle-Inclan JE, Besselink N, Cuppen E, Priestley P, Papenfuss AT (2021) GRIDSS2: comprehensive characterisation of somatic structural variation using single breakend variants and structural variant phasing. Genome Biol 22:202
Chen W, Zhang Y, Liu XP, Chen BY, Tu JX, Fu TD (2007) Detection of QTL for six yield-related traits in oilseed rape (Brassica napus) using DH and immortalized F2 populations. Theor Appl Genet 115:849–858
Chen X, Schulz-Trieglaff O, Shaw R, Barnes B, Schlesinger F, Cox AJ, Kruglyak S, Saunders CT (2015) Manta: rapid detection of structural variants and indels for clinical sequencing applications. Bioinformatics 32:1220–1222
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:736–743
Duan YH, Ju M, Miao HM, Zhang HY (2021) The sesame genome for gene discovery in sesame. In: Miao HM, Zhang HY, Kole C (eds) The sesame genome. Springer, Cham, pp 283–290
Eshed Y, Baum SF, Bowman JL (1999) Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99:199–209
Fu Y, Wei D, Dong H, He Y, Cui Y, Mei J, Wan H, Li J, Snowdon R, Friedt W, Li X, Qian W (2015) Comparative quantitative trait loci for silique length and seed weight in Brassica napus. Sci Rep 5:14407. https://doi.org/10.1038/srep14407
Hackbusch J, Richter K, Müller J, Salamini F, Uhrig JF (2005) A central role of Arabidopsis thaliana ovate family proteins in networking and subcellular localization of 3-aa loop extension homeodomain proteins. Proc Natl Acad Sci USA 102(13):4908–4912. https://doi.org/10.1073/pnas.0501181102
Jatothu J, Dangi KS, Kumar SS (2013) Evaluation of sesame crosses for heterosis of yield and yield attributing traits. J Trop Agric 51:84–91
Jeffares DC, Jolly C, Hoti M, Speed D, Shaw L, Rallis C, Balloux F, Dessimoz C, BäHler J, Sedlazeck FJ (2017) Transient structural variations have strong effects on quantitative traits and reproductive isolation in fission yeast. Nat Commun 8:14061
Jimoh WA, Aroyehun HT (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). Turk J Fish Aquat Sc 11:185–190
Langham DR (2017) VII Capsule descriptors of sesame (Sesamum indicum L.). ResearchGate, pp 263
Langham DR (2018) X Sesame seed descriptors (Sesamum indicum L.). ResearchGate, pp 14
Layer RM, Chiang C, Quinlan AR, Hall IM (2014) LUMPY: a probabilistic framework for structural variant discovery. Genome Biol 15:84
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760
Li Z, Li YG, Cai MX, Priyadarshani SVGN, Aslam M, Zhou Q, Huang XY, Wang XM, Liu YQ, Qin Y (2019) Genome-wide analysis of the YABBY transcription factor family in pineapple and functional identification of AcYABBY4 involvement in salt stress. Int J Mol Sci 20:5863
Liu YY, Douglas CJ (2015) A role for OVATE FAMILY PROTEIN1 (OFP1) and OFP4 in a BLH6-KNAT7 multi-protein complex regulating secondary cell wall formation in Arabidopsis thaliana. Plant Signal Behav 10:e1033126
Liu JP, Van Eck J, Cong B, Tanksley SD (2002) A new class of regulatory genes underlying the cause of pear-shaped tomato fruit. Proc Natl Acad Sci USA 99:13302–13306
Liu J, Hua W, Hu Z, Yang H, Zhang L, Li R, Deng L, Sun X, Wang X, Wang H (2015) Natural variation in ARF18 gene simultaneously affects seed weight and silique length in polyploid rapeseed. Proc Natl Acad Sci USA 112:E5123–E5132
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408
Makinde FM, Akinoso R (2013) Nutrient composition and effect of processing treatments on anti nutritional factors of Nigerian sesame (Sesamum indicum Linn.) cultivars. Int Food Res J 20:2293–2300
Miao HM, Langham DR, Zhang HY (2021) Botanical descriptions of sesame. In: Miao HM, Zhang HY, Kole C (eds) The sesame genome. Springer, Cham, pp 19–58
Mungala RA (2017) Study of combining ability for seed yield and its component in sesame (Sesamum indicum L.). Int J Pure Appl Biosci 5:775–785
Poplin R, Ruano-Rubio V, DePristo MA, Fennell T, Carneiro MO, Van der Auwera GA, Kling DE, Gauthier LD, Levy-Moonshine A, Roazen D, Shakir K, Thibault J, Chandran S, Whelan CW, Lek M, Gabriel S, Daly MJ, Neale B, MacArthur DG, Banks E (2017) Scaling accurate genetic variant discovery to tens of thousands of samples. bioRxiv. https://doi.org/10.1101/201178
Prakash K, Naik SN (2014) Bioactive constituents as a potential agent in sesame for functional and nutritional application. J Bioresour Eng Technol 1:61–79
Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38:904–909
Raikwar R (2018) Diallel crossing for assessment of yield and its components in sesame (Sesamum indicum L.). Int J Chem Stud 6:179–183
Ramalingam A, Muralidhar V, Sheriff NM (1990) Combining ability studies in sesame. J Oilseeds Res 7:75–77
Rausch T, Zichner T, Schlattl A, Stütz AM, Beneš V, Korbel JO (2012) DELLY: structural variant discovery by integrated paired-end and split-read analysis. Bioinformatics 28:333–339
Raza MA, Feng LY, Iqbal N, Manaf A, Khalid MHB, Ur Rehman S, Wasaya A, Ansar M, Billah M, Yang F et al (2018) Effect of sulphur application on photosynthesis and biomass accumulation of sesame varieties under rainfed conditions. Agronomy 8:149. https://doi.org/10.3390/agronomy8080149
Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley JF, Kresovich S, Goodman M, Buckler E (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA 98:11479–11484
Sablowski R (2015) Control of patterning, growth, and differentiation by floral organ identity genes. J Exp Bot 66:1065–1073
Saxena K (2017) Genetic variability, heritability and genetic advance for the phenotypic traits in sesame (Sesamum indicum L.). Int J Pure Appl Biosci 5:1126–1131
Sene B, Sarr F, Sow MS, Diouf D, Niang M, Traoré D (2017) Physico-chemical composition of the sesame variety (Sesamum indicum L.) and characterization of its derived products (seeds, oil and oilcake) in Senegal. Food Sci Qual Manag 65:5–10
Shen W, Qin P, Yan M et al (2019a) Fine mapping of a silique length and seed weight-related gene in Brassica napus. Theor Appl Genet 132:2985–2996
Shen W, Qin P, Yan M, Li B, Wu Z, Wen J, Yi B, Ma C, Shen J, Fu T, Tu J (2019b) Fine mapping of a silique length- and seed weight-related gene in Brassica napus. Theor Appl Genet 132(11):2985–2996. https://doi.org/10.1007/s00122-019-03400-6
Shi L, Song J, Guo C et al (2019) A CACTA-like transposable element in the upstream region of BnaA9.CYP78A9 acts as an enhancer to increase silique length and seed weight in rapeseed. Plant J 98:524–539
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. Mol Biol Evol 28:2731–2739
Wang SC, Chang Y, Guo JJ, Chen JG (2007) Arabidopsis ovate family protein 1 is a transcriptional repressor that suppresses cell elongation. Plant J 50:858–872
Wang YK, Chang WC, Liu PF, Hsiao MK, Lin CT, Lin SM, Pan RL (2010) Ovate family protein 1 as a plant Ku70 interacting protein involving in DNA double-strand break repair. Plant Mol Biol 74(4–5):453–466. https://doi.org/10.1007/s11103-010-9685-5
Wang X, Chen L, Wang A et al (2016) Quantitative trait loci analysis and genome-wide comparison for silique related traits in Brassica napus. BMC Plant Biol 16:71
Wang H, Zaman QU, Huang W et al (2019) QTL and candidate gene identification for silique length based on high-dense genetic map in Brassica napus L. Front Plant Sci 10:1579
Wei LB, Miao HM, Li C, Duan YH, Niu JJ, Zhang TD, Zhao QY, Zhang HY (2014) Development of SNP and InDel markers via de novo transcriptome assembly in Sesamum indicum L. Mol Breeding 34:2205–2217
Wei LB, Li C, Duan YH, Qu WW, Wang HL, Miao HM, Zhang HY (2019) A SNP mutation of SiCRC regulates seed number per capsule and capsule length of cs1 mutant in sesame. Int J Mol Sci 20:4056
Wei LB, Miao HM, Duan YH, Zhang HY (2021) Classical genetics of sesame. In: Miao HM, Zhang HY, Kole C (eds) The sesame genome. Springer, Cham, pp 79–120
Wongyai W, Juttpornpong S (1992) Indirect selection for seed weight in sesame using capsule size as a criteria. Sesame Safflower Newsl 7:4–7
Wu KS, Liu HY, Yang MM, Tao Y, Ma HH, Wu WX, Zuo Y, Zhao YZ (2014) High-density genetic map construction and QTLs analysis of grain yield-related traits in Sesame (Sesamum indicum L.) based on RAD-Seq techonology. BMC Plant Biol 14:274
Xiao Y, Liu D, Zhang G, Tong H, Chu C (2017) Brassinosteroids regulate OFP1, a DLT interacting protein, to modulate plant architecture and grain morphology in rice. Front Plant Sci 8:1698. https://doi.org/10.3389/fpls.2017.01698
Yamanura KM, Nadaf HL (2009) Combining ability and gene action for yield and yield components in sesame (Sesamum indicum L.). Karnataka J Agric Sci 22:255–260
Yang P, Shu C, Chen L, Xu J, Wu J, Liu K (2012) Identification of a major QTL for silique length and seed weight in oilseed rape (Brassica napus L.). Theor Appl Genet 125:285–296
Yang M, Yang WJ, Gao Y, Zhang YY, Zhu XD, Zhou R, Li DH, Zhang XR, Wu WH, Wang LH (2017a) Quantitative trait locus mapping for sesame capsule size. Chin J Oil Crop Sci 39:785–793
Yang Y, Shen Y, Li S, Ge X, Li Z (2017b) High density linkage map construction and QTL detection for three silique-related traits in Orychophragmus violaceus derived Brassica napus population. Front Plant Sci 8:1512
Yol E (2017) Inheritance of long and dense capsule characteristics in sesame. Turk J Field Crops 22:8–13
Zhang LW, Yang GS, Liu PW, Hong DF, Li SP, He QB (2011) Genetic and correlation analysis of silique-traits in Brassica napus L. by quantitative trait locus mapping. Theor Appl Genet 122:21–31
Zhang HY, Miao HM, Wang L, Qu LB, Liu HY, Wang Q, Yue MW (2013) Genome sequencing of the important oilseed crop Sesamum indicum L. Genome Biol 14:401
Zhang HY, Miao HM, Li C, Wei LB, Duan YH, Ma Q, Kong JJ, Xu FF, Chang SX (2016) Ultra-dense SNP genetic map construction and identification of SiDt gene controlling the determinate growth habit in Sesamum indicum L. Sci Rep 6:31556
Zhang HY, Miao HM, Wei LB, Li C, Duan YH, Xu FF, Qu WW, Zhao RH, Ju M, Chang SX (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 Biol 18:296
Zhang HY, Miao HM, Ju M (2019) Potential for adaptation to climate change through genomic breeding in sesame. In: Miao HM, Zhang HY, Kole C (eds) The sesame genome. Springer, Cham, pp 374–376
Zhang HY, Langham DR, Miao HM (2021) Economic and academic importance of sesame. In: Miao HM, Zhang HY, Kole C (eds) The sesame genome. Springer, Cham, pp 1–18
Zhao RH, Miao HM, Song WQ, Chen CB, Zhang HY (2018) Identification of sesame (Sesamum indicum L.) chromosomes using the BAC-FISH system. Plant Biol 20:85–92
Zhou X, Zhang H, Wang P, Liu Y, Zhang X, Song Y, Wang Z, Ali A, Wan L, Yang G, Hong D (2022) BnaC7.ROT3, the causal gene of cqSL-C7, mediates silique length by affecting cell elongation in Brassica napus. J Exp Bot 73(1):154–167. https://doi.org/10.1093/jxb/erab407
Acknowledgements
This work was supported by the earmarked fund of China Agriculture Research System of MOF and MARA (CARS-14-1-04), the Key Project of Science and Technology in Henan Province (201300110600), the Shennong Laboratory First Class Program (SN01-2022-04), the National Natural Science Foundation of China (No. 32172094), the Henan Province Specific Professor Position Program (SPPP2022), the Innovation Scientists and Technicians Troop Construction Projects of Henan Province (2023TD04), Key Research and Development Project of Henan Province (221111520400) and Science and Technology Foundation for The Excellent Youth Scholars of Henan Academy of Agricultural Sciences (2022YQ14).
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ZH conceived the technical route and guided the manuscript for publishing. MH, WL and WC guided the experiments, performed the data analysis and drafted the manuscript. LC, LG, CH, NJ and GH conducted the main data analysis and experiments. TQ, JM and MQ performed the genetic experiments and participated in result validation. All authors read and approved the final manuscript.
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Wang, C., Niu, J., Wei, L. et al. A 4.43-Kb deletion of chromosomal segment containing an ovate family protein confers long capsule in sesame (Sesamum indicum L.). Theor Appl Genet 136, 221 (2023). https://doi.org/10.1007/s00122-023-04465-0
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DOI: https://doi.org/10.1007/s00122-023-04465-0