Abstract
Wheat (Triticum aestivum) is one of the most important food crops worldwide, providing up to 20% of the caloric intake per day. Developing high-yielding wheat cultivars with tolerance against abiotic and biotic stresses is important to keep up with the increasing human population. Tiller number is one of the major yield-related traits, directly affecting the number of grains produced per plant; however, only a small number of QTL and underlining genes have been identified for this important factor. Identification of novel genetic variation underlying contrasting traits and their precise genetic mapping in wheat is considered difficult due to the complexity and size of the genome; however, advancements in genomic resources have made efficient gene localization more possible. In this study, we report the characterization of a novel tillering number gene using a mutant identified in the forward genetic screen of an ethyl methane sulfonate (EMS)-treated population of cv. “Jagger.” By crossing the low tillering mutant with the Jagger wild-type plant, we generated an F2 population and used the MutMap approach to identify a novel physical interval on 11 Mb on chromosome 2DS. Using an F2 population of 442 gametes and polymorphic SNP markers, we were able to delineate the tin6 locus to a 2.1 Mb region containing 22 candidate genes.
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Data availability
DNA raw sequencing reads are available under the NCBI BioProject ID: PRJNA954413.
References
Abe A, Kosugi S, Yoshida K et al (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30:174–178. https://doi.org/10.1038/nbt.2095
An J, Niu H, Ni Y et al (2019) The miRNA-mRNA networks involving abnormal energy and hormone metabolisms restrict tillering in a wheat mutant dmc. Int J Mol Sci Article. https://doi.org/10.3390/ijms20184586
Appels R, Eversole K, Feuillet C et al (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science (1979) 361. https://doi.org/10.1126/science.aar7191
Broman KW, Wu H, Sen Ś, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890. https://doi.org/10.1093/bioinformatics/btg112
Danguy des Déserts A, Bouchet S, Sourdille P, Servin B (2021) Evolution of recombination landscapes in diverging populations of bread wheat. Genome Biol Evol. https://doi.org/10.1093/gbe/evab152
Donald CM, (1968) The breeding of crop ideotypes. Euphytica 17:385–403. https://doi.org/10.1007/BF00056241
Dong C, Zhang L, Chen Z 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. https://doi.org/10.3389/fpls.2020.01249
Dong C, Zhang L, Zhang Q et al (2023) Tiller number1 encodes an ankyrin repeat protein that controls tillering in bread wheat. Nat Commun 14:836. https://doi.org/10.1038/s41467-023-36271-z
Emms DM, Kelly S (2015) OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 16(1):157. https://doi.org/10.1186/s13059-015-0721-2
Fekih R, Takagi H, Tamiru M et al (2013) MutMap+: genetic mapping and mutant identification without crossing in rice. PLoS One 8:e68529. https://doi.org/10.1371/journal.pone.0068529
Food and Agriculture Organization of the United Nations (2020) FAOSTAT statistical database
Godfray HCJ, Beddington JR, Crute IR et al (2010) (2010) Food security: the challenge of feeding 9 billion people. Science (1979) 327:812–818. https://doi.org/10.1126/science.1185383
Haenel Q, Laurentino TG, Roesti M, Berner D (2018) Meta-analysis of chromosome-scale crossover rate variation in eukaryotes and its significance to evolutionary genomics. Mol Ecol 27:2477–2497. https://doi.org/10.1111/mec.14699
Hawkesford MJ, Araus JL, Park R et al (2013) Prospects of doubling global wheat yields. Food Energy Secur 2:34–48
He F, Pasam R, Shi F et al (2019) Exome sequencing highlights the role of wild-relative introgression in shaping the adaptive landscape of the wheat genome. Nat Genet 51:896–904. https://doi.org/10.1038/s41588-019-0382-2
Hickey LT, Hafeez AN, Robinson H et al (2019) Breeding crops to feed 10 billion. Nat Biotechnol 37:744–754. https://doi.org/10.1038/s41587-019-0152-9
Hill JT, Demarest BL, Bisgrove BW et al (2013) MMAPPR: mutation mapping analysis pipeline for pooled RNA-seq. Genome Res 23:687–697. https://doi.org/10.1101/gr.146936.112
Hubbard L, Mcsteen P, Doebley J, Hake S (2002) Expression patterns and mutant phenotype of teosinte branched1 correlate with growth suppression in maize and teosinte. Genetics 162:1927–1935
Hussien A, Tavakol E, Horner DS et al (2014) Genetics of tillering in rice and barley; genetics of tillering in rice and barley. Plant Genome 7. https://doi.org/10.3835/plantgenome2013.10.0032
Kang J, Li J, Gao S et al (2017) Overexpression of the leucine-rich receptor-like kinase gene LRK2 increases drought tolerance and tiller number in rice. Plant Biotechnol J 15:1175–1185. https://doi.org/10.1111/pbi.12707
Krasileva KV, Vasquez-Gross HA, Howell T et al (2017) Uncovering hidden variation in polyploid wheat. Proc Natl Acad Sci USA 114:E913–E921. https://doi.org/10.1073/pnas.1619268114
Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19(9):1639–1645. https://doi.org/10.1101/gr.092759.109
Kuraparthy V, Sood S, Dhaliwal HS et al (2007) Identification and mapping of a tiller inhibition gene (tin3) in wheat. Theor Appl Genet 114:285–294. https://doi.org/10.1007/s00122-006-0431-y
Ma Z, Zhao D, Zhang C et al (2007) Molecular genetic analysis of five spike-related traits in wheat using RIL and immortalized F2 populations. Mol Genet Genomics 277:31–42. https://doi.org/10.1007/s00438-006-0166-0
Manchikatla PK, Kalavikatte D, Mallikarjuna BP et al (2021) MutMap approach enables rapid identification of candidate genes and development of markers associated with early flowering and enhanced seed size in chickpea (Cicer arietinum L.). Front Plant Sci 12. https://doi.org/10.3389/fpls.2021.688694
Mo Y, Howell T, Vasquez-Gross H et al (2018) Mapping causal mutations by exome sequencing in a wheat TILLING population: a tall mutant case study. Mol Genet Genomics 293:463–477. https://doi.org/10.1007/s00438-017-1401-6
Na J-K, Huh S-M, Yoon I-S et al (2014) Rice LIM protein OsPLIM2a is involved in rice seed and tiller development. Mol Breed 34:569–581. https://doi.org/10.1007/s11032-014-0058-7
Peng Z, Yen C, Yang JL (1998) Genetic control of oligo-culms in common wheat. Wheat Information Service 26:19–24
Ramírez-González RH, Borrill P, Lang D et al (2018) The transcriptional landscape of polyploid wheat. Science (1979) 361. https://doi.org/10.1126/science.aar6089
Rawat N, Joshi A, Pumphrey M et al (2019) A TILLING resource for hard red winter wheat variety Jagger. Crop Sci 59:1666–1671. https://doi.org/10.2135/cropsci2019.01.0011
Ren T, Hu Y, Tang Y et al (2018) Utilization of a wheat55K SNP array for mapping of major QTL for temporal expression of the tiller number. Front Plant Sci 9. https://doi.org/10.3389/fpls.2018.00333
Richards R (1988) A tiller inhibitor gene in wheat and its effect on plant growth. Aust J Agric Res 39:749. https://doi.org/10.1071/AR9880749
Schneeberger K, Ossowski S, Lanz C et al (2009) SHOREmap: simultaneous mapping and mutation identification by deep sequencing. Nat Methods 6:550–551
Schoen A, Joshi A, Tiwari V et al (2021) Triple null mutations in starch synthase SSIIa gene homoeologs lead to high amylose and resistant starch in hexaploid wheat. BMC Plant Biol 21. https://doi.org/10.1186/s12870-020-02822-5
Sears ER, (1966) Nullisomic-Tetrasomic Combinations in Hexaploid Wheat. In: Riley R, Lewis KR, (eds) Chromosome Manipulations and Plant Genetics, Boston, MA: Springer. https://doi.org/10.1007/978-1-4899-6561-5_4
Sears RG, Moffatt JM, Martin TJ et al (1997) Registration of ‘Jagger’ wheat. Crop Sci. https://doi.org/10.2135/cropsci1997.0011183x003700030062x
Si Y, Lu Q, Tian S et al (2022) Fine mapping of the tiller inhibition gene TIN5 in Triticum urartu. Theor Appl Genet. https://doi.org/10.1007/S00122-022-04140-W
Sugihara Y, Young L, Yaegashi H et al (2022) High-performance pipeline for MutMap and QTL-seq. PeerJ 10:e13170. https://doi.org/10.7717/peerj.13170
Takagi H, Tamiru M, Abe A et al (2015) MutMap accelerates breeding of a salt-tolerant rice cultivar. Nat Biotechnol 33:445–449. https://doi.org/10.1038/nbt.3188
Takagi H, Uemura A, Yaegashi H et al (2013) MutMap-Gap: whole-genome resequencing of mutant F2 progeny bulk combined with de novo assembly of gap regions identifies the rice blast resistance gene Pii. New Phytol 200:276–283. https://doi.org/10.1111/nph.12369
Tavakol E, Okagaki R, Verderio G et al (2015) The barley Uniculme4 gene encodes a BLADE-ON-PETIOLE-like protein that controls tillering and leaf patterning. Plant Physiol 168:164–174. https://doi.org/10.1104/pp.114.252882
Tilman D, Balzer C, Hill J, Befort BL (2011) Global food demand and the sustainable intensification of agriculture. Proc Natl Acad Sci USA 108:20260–20264. https://doi.org/10.1073/pnas.1116437108
Walkowiak S, Gao L, Monat C et al (2020) Multiple wheat genomes reveal global variation in modern breeding. Nature 588:277–283. https://doi.org/10.1038/s41586-020-2961-x
Wang Z, Li J, Chen S et al (2017) Poaceae-specific MS1 encodes a phospholipid-binding protein for male fertility in bread wheat. Proc Natl Acad Sci 114:12614–12619. https://doi.org/10.1073/pnas.1715570114
Wang Z, Wu F, Chen X et al (2022) Fine mapping of the tiller inhibition gene TIN4 contributing to ideal plant architecture in common wheat. Theor Appl Genet 135:527–535. https://doi.org/10.1007/s00122-021-03981-1
Watson A, Ghosh S, Williams MJ et al (2018) Speed breeding is a powerful tool to accelerate crop research and breeding. Nat Plants 4:23–29. https://doi.org/10.1038/s41477-017-0083-8
Yang R, Wu Z, Bai C et al (2021) Overexpression of PvWOX3a in switchgrass promotes stem development and increases plant height. Hortic Res 8:252. https://doi.org/10.1038/s41438-021-00678-w
Zhang L, Dong C, Chen Z et al (2021) WheatGmap: a comprehensive platform for wheat gene mapping and genomic studies. Mol Plant 14:187–190
Zhang X, Jia H, Li T et al (2022) TaCol-B5 modifies spike architecture and enhances grain yield in wheat. Sci 376:180–183. https://doi.org/10.1126/science.abm0717
Funding
Authors thankfully acknowledge financial support from the United States Department of Agriculture—National Institute of Food and Agriculture (award # 2020–67013-31460).
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VT and JP conceived the idea of the project and designed the experiments. AS and SW performed experiments. AS and ISY performed data analysis. JP and NR provided resources for experiments. AS, VT, and ISY wrote the manuscript with inputs from the co-authors. All co-authors read and approved the manuscript.
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Key message
This work reports an integrated forward genetic approach that combines whole genome sequencing of mutant bulk to identify a novel tiller number gene in hexaploid wheat.
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Supplementary file1 Supplementary Figure 1: Linear plot showing average SNP indexes across all chromosomes. (PNG 690 kb)
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Supplementary file2 Supplementary Figure 2: Example of 10 recombinants and Jagger and tin6 control using the tin6_18.3 marker. (PNG 519 kb)
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Supplementary file4 Supplementary Figure 4: Circos plot showing synteny between Jagger (blue) and Chinese Spring (green). Blue lines show Jagger homologs on Chinese Spring whereas red lines show where one chromosome of Jagger is having match on another nonhomologous chromosome of Chinese Spring. (PNG 3246 kb)
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Schoen, A., Yadav, I., Wu, S. et al. Identification and high-resolution mapping of a novel tiller number gene (tin6) by combining forward genetics screen and MutMap approach in bread wheat. Funct Integr Genomics 23, 157 (2023). https://doi.org/10.1007/s10142-023-01084-2
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DOI: https://doi.org/10.1007/s10142-023-01084-2