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Identification and functional analysis of a chromosome 2D fragment harboring TaFPF1 gene with the potential for yield improvement using a late heading wheat mutant

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Abstract

Key message

A chromosome fragment influencing wheat heading and grain size was identified using mapping of m406 mutant. The study of TaFPF1 in this fragment provides more insights into wheat yield improvement.

Abstract

In recent years, wheat production has faced formidable challenges driven by rapid population growth and climate change, emphasizing the importance of improving specific agronomic traits such as heading date, spike length, and grain size. To identify potential genes for improving these traits, we screened a wheat EMS mutant library and identified a mutant, designated m406, which exhibited a significantly delayed heading date compared to the wild-type. Intriguingly, the mutant also displayed significantly longer spike and larger grain size. Genetic analysis revealed that a single recessive gene was responsible for the delayed heading. Surprisingly, a large 46.58 Mb deletion at the terminal region of chromosome arm 2DS in the mutant was identified through fine mapping and fluorescence in situ hybridization. Thus, the phenotypes of the mutant m406 are controlled by a group of linked genes. This deletion encompassed 917 annotated high-confidence genes, including the previously studied wheat genes Ppd1 and TaDA1, which could affect heading date and grain size. Multiple genes in this region probably contribute to the phenotypes of m406. We further investigated the function of TaFPF1 using gene editing. TaFPF1 knockout mutants showed delayed heading and increased grain size. Moreover, we identified the direct upstream gene of TaFPF1 and investigated its relationship with other important flowering genes. Our study not only identified more genes affecting heading and grain development within this deleted region but also highlighted the potential of combining these genes for improvement of wheat traits.

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Data availability

The RNA-seq data have been uploaded to Genome Sequence Archive (https://bigd.ac.cn/gsa) under accession number CRA012428.

References

  • Beales J, Turner A, Griffiths S, Snape JW, Laurie DA (2007) A pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.). Theor Appl Genet 115:721–733

    Article  CAS  PubMed  Google Scholar 

  • Boden SA, Cavanagh C, Cullis BR, Ramm K, Greenwood J, Jean FE et al (2015) Ppd-1 is a key regulator of inflorescence architecture and paired spikelet development in wheat. Nat Plants 1:14016

    Article  CAS  PubMed  Google Scholar 

  • Chai L, Chen Z, Bian R, Zhai H, Cheng X, Peng H et al (2018) Dissection of two quantitative trait loci with pleiotropic effects on plant height and spike length linked in coupling phase on the short arm of chromosome 2D of common wheat (Triticum aestivum L.). Theor Appl Genet 131:2621–2637

    Article  CAS  PubMed  Google Scholar 

  • Chai L, Xin M, Dong C, Chen Z, Zhai H, Zhuang J et al (2022) A natural variation in ribonuclease H-like gene underlies Rht8 to confer “green revolution” trait in wheat. Mol Plant 15:377–380

    Article  CAS  PubMed  Google Scholar 

  • Chatterjee A, Moulik SP, Majhi PR, Sanyal SK (2002) Studies on surfactant-biopolymer interaction. I. Microcalorimetric investigation on the interaction of cetyltrimethylammonium bromide (CTAB) and sodium dodecylsulfate (SDS) with gelatin (Gn), lysozyme (Lz) and deoxyribonucleic acid (DNA). Biophys Chem 98:313–327

    Article  CAS  PubMed  Google Scholar 

  • Chen A, Dubcovsky J (2012) Wheat TILLING mutants show that the vernalization gene VRN1 down-regulates the flowering repressor VRN2 in leaves but is not essential for flowering. PLoS Genet 8:e1003134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui G, Li D, Zhang L, Xia C, Kong X, Liu X (2023) GSK3 regulates VRN1 to control flowering time in wheat. J Integr Plant Biol 65:1605–1608

    Article  CAS  PubMed  Google Scholar 

  • Daba SD, Tyagi P, Brown-Guedira G, Mohammadi M (2018) Genome-wide association studies to identify loci and candidate genes controlling kernel weight and length in a historical United States wheat population. Front Plant Sci 9:1045

    Article  PubMed  PubMed Central  Google Scholar 

  • Deng W, Casao MC, Wang P, Sato K, Hayes PM, Finnegan EJ et al (2015) Direct links between the vernalization response and other key traits of cereal crops. Nat Commun 6:5882

    Article  PubMed  Google Scholar 

  • Dong C, Zhang L, Chen Z, Xia C, Gu Y, Wang J et al (2020) Combining a new exome capture panel with an effective varBScore algorithm accelerates BSA-Based gene cloning in wheat. Front Plant Sci 11:1249

    Article  PubMed  PubMed Central  Google Scholar 

  • Engler C, Kandzia R, Marillonnet S (2008) A one pot, one step, precision cloning method with high throughput capability. PLoS ONE 3:e3647

    Article  PubMed  PubMed Central  Google Scholar 

  • Errum A, Rehman N, Uzair M, Inam S, Ali GM, Khan MR (2023) CRISPR/Cas9 editing of wheat Ppd-1 gene homoeologs alters spike architecture and grain morphometric traits. Funct Integr Genom 23:66

    Article  CAS  Google Scholar 

  • FAO (2018) Food Outlook: Biannual Report on Global Food Markers. Rome, pp 67–74

  • Foulkes MJ, Sylvester-Bradley R, Worland AJ, Snape JW (2004) Effects of a photoperiod-response gene Ppd-D1 on yield potential and drought resistance in UK winter wheat. Euphytica 135:63–73

    Article  CAS  Google Scholar 

  • Fu S, Chen L, Wang Y, Li M, Yang Z, Qiu L et al (2015) Oligonucleotide probes for ND-FISH analysis to identify rye and wheat chromosomes. Sci Rep-Uk 5:10552

    Article  Google Scholar 

  • Garvin DF, Porter H, Blankenheim ZJ, Chao S, Dill-Macky R (2015) A spontaneous segmental deletion from chromosome arm 3DL enhances Fusarium head blight resistance in wheat. Genome 58:479–488

    Article  CAS  PubMed  Google Scholar 

  • Geng Y, Zhang P, Liu Q, Wei Z, Riaz A, Chachar S et al (2020) Rice homolog of Sin3-associated polypeptide 30, OsSFL1, mediates histone deacetylation to regulate flowering time during short days. Plant Biotechnol J 18:325–327

    Article  PubMed  Google Scholar 

  • Greenup AG, Sasani S, Oliver SN, Talbot MJ, Dennis ES, Hemming MN et al (2010) ODDSOC2 is a MADS box floral repressor that is down-regulated by vernalization in temperate cereals. Plant Physiol 153:1062–1073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu X, Wang Y, He Y (2013) Photoperiodic regulation of flowering time through periodic histone deacetylation of the florigen gene FT. PLoS Biol 11:e1001649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo Z, Song Y, Zhou R, Ren Z, Jia J (2010) Discovery, evaluation and distribution of haplotypes of the wheat Ppd-D1 gene. New Phytol 185:841–851

    Article  CAS  PubMed  Google Scholar 

  • Heigwer F, Kerr G, Boutros M (2014) E-CRISP: fast CRISPR target site identification. Nat Methods 11:122–123

    Article  CAS  PubMed  Google Scholar 

  • Hellens RP, Allan AC, Friel EN, Bolitho K, Grafton K, Templeton MD et al (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1:13

    Article  PubMed  PubMed Central  Google Scholar 

  • Ishida Y, Tsunashima M, Hiei Y, Komari T (2015) Wheat (Triticum aestivum L.) transformation using immature embryos. Methods Mol Biol 1223:189–198

    Article  CAS  PubMed  Google Scholar 

  • Jung WJ, Lee YJ, Kang CS, Seo YW (2021) Identification of genetic loci associated with major agronomic traits of wheat (Triticum aestivum L.) based on genome-wide association analysis. BMC Plant Biol 21:418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kania T, Russenberger D, Peng S, Apel K, Melzer S (1997) FPF1 promotes flowering in Arabidopsis. Plant Cell 9:1327–1338

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kippes N, Zhu J, Chen A, Vanzetti L, Lukaszewski A, Nishida H et al (2014) Fine mapping and epistatic interactions of the vernalization gene VRN-D4 in hexaploid wheat. Mol Genet Genom 289:47–62

    Article  CAS  Google Scholar 

  • Lang T, Li G, Wang H, Yu Z, Chen Q, Yang E et al (2019) Physical location of tandem repeats in the wheat genome and application for chromosome identification. Planta 249:663–675

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Zheng L, Corke F, Smith C, Bevan MW (2008) Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev 22:1331–1336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Li H, Hao C, Wang K, Wang Y, Qin L et al (2020) TaDA1, a conserved negative regulator of kernel size, has an additive effect with TaGW2 in common wheat (Triticum aestivum L.). Plant Biotechnol J 18:1330–1342

    Article  CAS  PubMed  Google Scholar 

  • Liu S, Chen S, Zhou Y, Shen Y, Qin Z, Wu L (2023) VERNALIZATION1 represses FLOWERING PROMOTING FACTOR1-LIKE1 in leaves for timely flowering in Brachypodium distachyon. Plant Cell 35:3697–3711

    Article  PubMed  Google Scholar 

  • Luo M, Platten D, Chaudhury A, Peacock WJ, Dennis ES (2009) Expression, imprinting, and evolution of rice homologs of the polycomb group genes. Mol Plant 2:711–723

    Article  CAS  PubMed  Google Scholar 

  • Ma HX, Bai GH, Gill BS, Hart LP (2006) Deletion of a chromosome arm altered wheat resistance to fusarium head blight and deoxynivalenol accumulation in Chinese Spring. Plant Dis 90:1545–1549

    Article  CAS  PubMed  Google Scholar 

  • Ma X, Cheng Z, Qin R, Qiu Y, Heng Y, Yang H et al (2013) OsARG encodes an arginase that plays critical roles in panicle development and grain production in rice. Plant J 73:190–200

    Article  CAS  PubMed  Google Scholar 

  • Ma J, Zhang H, Li S, Zou Y, Lan X (2019) Identification of quantitative trait loci for kernel traits in a wheat cultivar Chuannong16. BMC Genet 20:77

    Article  PubMed  PubMed Central  Google Scholar 

  • Melzer S, Kampmann G, Chandler J, Apel K (1999) FPF1 modulates the competence to flowering in Arabidopsis. Plant J 18:395–405

    Article  CAS  PubMed  Google Scholar 

  • Nishida H, Yoshida T, Kawakami K, Fujita M, Long B, Akashi Y et al (2013) Structural variation in the 5’ upstream region of photoperiod-insensitive alleles Ppd-A1a and Ppd-B1a identified in hexaploid wheat (Triticum aestivum L.), and their effect on heading time. Mol Breeding 31:27–37

    Article  CAS  Google Scholar 

  • Rabbi S, Kumar A, Mohajeri NS, Simsek S, Sapkota S, Solanki S et al (2021) Genome-wide association mapping for yield and related traits under drought stressed and non-stressed environments in wheat. Front Genet 12:649988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shaw LM, Turner AS, Laurence H, Simon G, Laurie DA, Somers DE (2013) Mutant alleles of photoperiod-1 in wheat (Triticum aestivum L.) that confer a late flowering phenotype in long days. PLoS ONE 8:e79459

    Article  PubMed  PubMed Central  Google Scholar 

  • Shi C, Zhao L, Zhang X, Lv G, Pan Y, Chen F (2019) Gene regulatory network and abundant genetic variation play critical roles in heading stage of polyploidy wheat. BMC Plant Biol 19:6

    Article  PubMed  PubMed Central  Google Scholar 

  • Song L, Liu J, Cao B, Liu B, Zhang X, Chen Z et al (2023) Reducing brassinosteroid signalling enhances grain yield in semi-dwarf wheat. Nature 617:118–124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sui P, Jin J, Ye S, Mu C, Gao J, Feng H et al (2012) H3K36 methylation is critical for brassinosteroid-regulated plant growth and development in rice. Plant J 70:340–347

    Article  CAS  PubMed  Google Scholar 

  • Sui P, Shi J, Gao X, Shen WH, Dong A (2013) H3K36 methylation is involved in promoting rice flowering. Mol Plant 6:975–977

    Article  CAS  PubMed  Google Scholar 

  • Sun L, Yang W, Li Y, Shan Q, Ye X, Wang D et al (2019) A wheat dominant dwarfing line with Rht12, which reduces stem cell length and affects gibberellic acid synthesis, is a 5AL terminal deletion line. Plant J 97:887–900

    Article  CAS  PubMed  Google Scholar 

  • Tang Z, Yang Z, Fu S (2014) Oligonucleotides replacing the roles of repetitive sequences pAs1, pSc119.2, pTa-535, pTa71, CCS1, and pAWRC.1 for FISH analysis. J Appl Genet 55:313–318

    Article  CAS  PubMed  Google Scholar 

  • Trevaskis B, Bagnall DJ, Ellis MH, Peacock WJ, Dennis ES (2003) MADS box genes control vernalization-induced flowering in cereals. Proc Natl Acad Sci USA 100:13099–13104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034

    Article  CAS  PubMed  Google Scholar 

  • Wuriyanghan H, Zhang B, Cao WH, Ma B, Lei G, Liu YF et al (2009) The ethylene receptor ETR2 delays floral transition and affects starch accumulation in rice. Plant Cell 21:1473–1494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie L, Zhang Y, Wang K, Luo X, Xu D, Tian X et al (2021) TaVrt2, an SVP-like gene, cooperates with TaVrn1 to regulate vernalization-induced flowering in wheat. New Phytol 231:834–848

    Article  CAS  PubMed  Google Scholar 

  • Xing L, Li J, Xu Y, Xu Z, Chong K (2009) Phosphorylation modification of wheat lectin VER2 is associated with vernalization-induced O-GlcNAc signaling and intracellular motility. PLoS ONE 4:e4854

    Article  PubMed  PubMed Central  Google Scholar 

  • Xing HL, Dong L, Wang ZP, Zhang HY, Han CY, Liu B et al (2014) A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol 14:327

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiong H, Zhou C, Fu M, Guo H, Xie Y, Zhao L et al (2022) Cloning and functional characterization of Rht8, a “green revolution” replacement gene in wheat. Mol Plant 15:373–376

    Article  CAS  PubMed  Google Scholar 

  • Xu S, Chong K (2018) Remembering winter through vernalisation. Nat Plants 4:997–1009

    Article  PubMed  Google Scholar 

  • Xu ML, Jiang JF, Ge L, Xu YY, Chen H, Zhao Y et al (2005) FPF1 transgene leads to altered flowering time and root development in rice. Plant Cell Rep 24:79–85

    Article  CAS  PubMed  Google Scholar 

  • Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100:6263–6268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P et al (2004) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303:1640–1644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M et al (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci USA 103:19581–19586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yong WD, Xu YY, Xu WZ, Wang X, Li N, Wu JS et al (2003) Vernalization-induced flowering in wheat is mediated by a lectin-like gene VER2. Planta 217:261–270

    Article  CAS  PubMed  Google Scholar 

  • Yoshida N, Yanai Y, Chen L, Kato Y, Hiratsuka J, Miwa T et al (2001) EMBRYONIC FLOWER2, a novel polycomb group protein homolog, mediates shoot development and flowering in Arabidopsis. Plant Cell 13:2471–2481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Zhao G, Gao L, Kong X, Guo Z, Wu B et al (2016) Functional studies of heading date-related gene TaPRR73, a paralog of Ppd1 in common wheat. Front Plant Sci 7:772

    PubMed  PubMed Central  Google Scholar 

  • Zhao J, Zhai Z, Li Y, Geng S, Song G, Guan J et al (2018) Genome-wide Identification and expression profiling of the TCP family genes in spike and grain development of wheat (Triticum aestivum L.). Front Plant Sci 9:1282

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng J, Liu H, Wang Y, Wang L, Chang X, Jing R et al (2014) TEF-7A, a transcript elongation factor gene, influences yield-related traits in bread wheat (Triticum aestivum L.). J Exp Bot 65:5351–5365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

The authors thank Prof. Qixin Sun’s group for providing the CRISPR/Cas9 vector system. This work was funded by the National Key Research and Development Program of China (2023YFF1000603), Talent Program and Innovation Program of Chinese Academy of Agricultural Sciences.

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  1. Lifen Wu and Guangrong Li have equally contributed to this work.

Authors and Affiliations

  1. State Key Laboratory of North China Crop Improvement and Regulation, Hebei Sub-Center for National Maize Improvement Center, College of Agronomy, Hebei Agricultural University, Baoding, 071001, Hebei, China

    Lifen Wu, Jingtang Chen & Xu Liu

  2. State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, 100081, China

    Lifen Wu, Danping Li, Chunhao Dong, Xueying Zhang, Lichao Zhang, Xiuying Kong, Chuan Xia & Xu Liu

  3. Center for Informational Biology, School of Life Science and Technology, University of Electronic and Technology of China, Chengdu, 611731, Sichuan, China

    Guangrong Li & Zujun Yang

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  1. Lifen Wu
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  2. Guangrong Li
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  3. Danping Li
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  4. Chunhao Dong
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Contributions

XL, XYK, CX, and JTC conceived and designed the experiments. LFW and XYZ conducted the plant material cultivation. LFW and GRL conducted laboratory experiments. LFW, CHD, and DPL participated in data analysis. ZJY provided experimental techniques for FISH. LCZ helped with the generation of transgenic wheat. LFW, CX, and XYK wrote and revised the manuscript. All authors discussed the results and provided feedback on the manuscript.

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Correspondence to Chuan Xia, Jingtang Chen or Xu Liu.

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Wu, L., Li, G., Li, D. et al. Identification and functional analysis of a chromosome 2D fragment harboring TaFPF1 gene with the potential for yield improvement using a late heading wheat mutant. Theor Appl Genet 137, 92 (2024). https://doi.org/10.1007/s00122-024-04593-1

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