Abstract
Key message
Identifying and mapping grain size candidate genes in the wheat genome greatly empowers reverse genetics approaches to improve grain yield potential of wheat.
Abstract
Grain size (GS) or grain weight is believed to be a major driving force for further improvement of wheat yield. Although the large, polyploid genome of wheat poses an obstacle to identifying GS determinants using map-based cloning, a translational genomics approach using GS regulators identified in the model plants rice and Arabidopsis as candidate genes appears to be effective and supports a hypothesis that a conserved genetic network regulates GS in rice and wheat. In this review, we summarize the progress in the studies on GS in the model plants and wheat and identify 45 GS candidate loci in the wheat genome. In silico mapping of these GS loci in the diploid wheat and barley genomes showed (1) several gene families amplified in the wheat lineage, (2) a significant number of the GS genes located in the proximal regions surrounding the centromeres, and (3) more than half of candidate genes to be negative regulators, or their expression negatively related by microRNAs. Identifying and mapping the wheat GS gene homologs will not only facilitate candidate gene analysis, but also open the door to improving wheat yield using reverse genetics approaches by mining desired alleles in landraces and wild ancestors and to developing novel germplasm by TILLING and genome editing technologies.
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References
Carroll D (2011) Genome engineering with zinc-finger nucleases. Genetics 188:773–782
Cermak T, Doyle EL, Christian M, Wang L, Zhang Y, Schmidt C, Baller JA, Somia NV, Bogdanove AJ, Voytas DF (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucl Acids Res 39:e28
Che R, Tong H, Shi B, Liu Y, Fang S, Liu D, Xiao Y, Hu B, Liu L, Wang H, Zhao M, Chu C (2016) Control of grain size and rice yield by GL2-mediated brassinosteroid responses. Nat Plants 2:15195
Clasen BM, Stoddard TJ, Luo S, Demorest ZL, Li J, Cedrone F, Tibebu R, Davison S, Ray EE, Daulhac A, Coffman A, Yabandith A, Retterath A, Haun W, Baltes NJ, Mathis L, Voytas DF, Zhang F (2015) Improving cold storage and processing traits in potato through targeted gene knockout. Plant Biotechnol J 14:169–176
Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–823
Duan P, Xu J, Zeng D, Zhang B, Geng M, Zhang G, Huang K, Huang L, Xu R, Ge S, Qian Q, Li Y (2017) Natural variation in the promoter of GSE5 contributes to grain size diversity in rice. Mol Plant 10:685–694
Fischer RA (2008) The importance of grain or kernel number in wheat: a reply to Sinclair and Jamieson. Field Crops Res 105:15–21
Gegas VC, Nazari A, Griffiths S, Simmonds J, Fish L, Orford S, Sayers L, Doonan JH, Snape JW (2010) A genetic framework for grain size and shape variation in wheat. Plant Cell 22:1046–1056
Griffiths S, Wingen L, Pietragalla J, Garcia G, Hasan A, Miralles D, Calderini DF, Ankleshwaria JB, Waite ML, Simmonds J, Snape J, Reynolds M (2015) Genetic dissection of grain size and grain number trade-offs in CIMMYT wheat germplasm. PLoS One 10:e0118847
Hanif M, Gao F, Liu J, Wen W, Zhang Y, Rasheed A, Xia X, He Z, Cao S (2016) TaTGW6-A1, an ortholog of rice TGW6, is associated with grain weight and yield in bread wheat. Mol Breed 36:1
Haun W, Coffman A, Clasen BM, Demorest ZL, Lowy A, Ray E, Retterath A, Stoddard T, Juillerat A, Cedrone F, Mathis L, Voytas DF, Zhang F (2014) Improved soybean oil quality by targeted mutagenesis of the fatty acid desaturase 2 gene family. Plant Biotechnol J 12:934–940
Heang D, Sassa H (2012) An atypical bHLH protein encoded by POSITIVE REGULATOR OF GRAIN LENGTH 2 is involved in controlling grain length and weight of rice through interaction with a typical bHLH protein APG. Breed Sci 62:133–141
Hong Y, Chen L, Du LP, Su Z, Wang J, Ye X, Qi L, Zhang Z (2014) Transcript suppression of TaGW2 increased grain width and weight in bread wheat. Funct Integr Genomics 14:341–349
Hu J, Wang Y, Fang Y, Zeng L, Xu J, Yu H, Shi Z, Pan J, Zhang D, Kang S, Zhu L, Dong G, Guo L, Zeng D, Zhang G, Xie L, Xiong G, Li J, Qian Q (2015) A rare allele of GS2 enhances grain size and grain yield in rice. Mol Plant 8:1455–1465
Hu M, Zhang H, Cao J, Zhu X, Wang S, Jiang H, Wu Z, Lu J, Chang C, Sun G, Ma C (2016) Characterization of an IAA-glucose hydrolase gene TaTGW6 associated with grain weight in common wheat (Triticum aestivum L.). Mol Breed 36:25
Jaiswal V, Gahlaut V, Mathur S, Agarwal PK, Khandelwal MK, Khurana JP, Tyagi AK, Balyan HS, Gupta PK (2015) Identification of novel SNP in promoter sequence of TaGW2-6A associated with grain weight and other agronomic traits in wheat (Triticum aestivum L.). PLoS One 10:e0129400
Jia J, Zhao S, Kong X, Li Y, Zhao G, He W, Appels R, Pfeifer M, Tao Y, Zhang X, Jing R, Zhang C, Ma Y, Gao L, Gao C, Spannagl M, Mayer KF, Li D, Pan S, Zheng F, Hu Q, Xia X, Li J, Liang Q, Chen J, Wicker T, Gou C, Kuang H, He G, Luo Y, Keller B, Xia Q, Lu P, Wang J, Zou H, Zhang R, Xu J, Gao J, Middleton C, Quan Z, Liu G, Wang J, Consortium IWGS, Yang H, Liu X, He Z, Mao L, Wang J (2013) Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496:91–95
Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42:541–544
Krasileva KV, Vasquez-Gross HA, Howell T, Bailey P, Paraiso F, Clissold L, Simmonds J, Ramirez-Gonzalez RH, Wang X, Borrill P, Fosker C, Ayling S, Phillips AL, Uauy C, Dubcovsky J (2017) Uncovering hidden variation in polyploid wheat. Proc Natl Acad Sci USA 114:E913–E921
Li N, Li Y (2015) Maternal control of seed size in plants. J Exp Bot 66:1087–1097
Li W, Zhang P, Fellers JP, Friebe B, Gill BS (2004) Sequence composition, organization, and evolution of the core Triticeae genome. Plant J 40:500–511
Li T, Huang S, Jiang WZ, Wright D, Spalding MH, Weeks DP, Yang B (2011a) TAL nucleases (TALNs): hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain. Nucl Acids Res 39:359–372
Li Y, Fan C, Xing Y, Jiang Y, Luo L, Sun L, Shao D, Xu C, Li X, Xiao J, He Y, Zhang Q (2011b) Natural variation in GS5 plays an important role in regulating grain size and yield in rice. Nat Genet 43:1266–1269
Li J, Chu H, Zhang Y, Mou T, Wu C, Zhang Q, Xu J (2012a) The rice HGW gene encodes a ubiquitin-associated (UBA) domain protein that regulates heading date and grain weight. PLoS One 7:e34231
Li T, Liu B, Spalding MH, Weeks DP, Yang B (2012b) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotech 30:390–392
Ling HQ, Zhao S, Liu D, Wang J, Sun H, Zhang C, Fan H, Li D, Dong L, Tao Y, Gao C, Wu H, Li Y, Cui Y, Guo X, Zheng S, Wang B, Yu K, Liang Q, Yang W, Lou X, Chen J, Feng M, Jian J, Zhang X, Luo G, Jiang Y, Liu J, Wang Z, Sha Y, Zhang B, Wu H, Tang D, Shen Q, Xue P, Zou S, Wang X, Liu X, Wang F, Yang Y, An X, Dong Z, Zhang K, Zhang X, Luo M, Dvorak J, Tong Y, Wang J, Yang H, Li Z, Wang D, Zhang A, Wang J (2013) Draft genome of the wheat A-genome progenitor Triticum urartu. Nature 496:87–90
Liu J, Chen J, Zheng X, Wu F, Lin Q, Heng Y, Tian P, Cheng Z, Yu X, Zhou K, Zhang X, Guo X, Wang J, Wang H, Wan J (2017) GW5 acts in the brassinosteroid signalling pathway to regulate grain width and weight in rice. Nat Plants 3:17043
Lu J, Chang C, Zhang HP, Wang SX, Sun G, Xiao SH, Ma C (2015) Identification of a novel allele of TaCKX6a02 associated with grain size, filling rate and weight of common wheat. PLoS One 10:e0144765
Luo MC, Gu YQ, You FM, Deal KR, Ma Y, Hu Y, Huo N, Wang Y, Wang J, Chen S, Jorgensen CM, Zhang Y, McGuire PE, Pasternak S, Stein JC, Ware D, Kramer M, McCombie WR, Kianian SF, Martis MM, Mayer KF, Sehgal SK, Li W, Gill BS, Bevan MW, Simková H, Dolezel J, Weining S, Lazo GR, Anderson OD, Dvorak J (2013) A 4-gigabase physical map unlocks the structure and evolution of the complex genome of Aegilops tauschii, the wheat d-genome progenitor. Proc Natl Acad Sci USA 110:7940–7945
Ma L, Li T, Hao C, Wang Y, Chen X, Zhang X (2015) TaGS5-3A, a grain size gene selected during wheat improvement for larger kernel and yield. Plant Biotechnol J 14:1269–1280
Mahfouz MM, Li L, Shamimuzzaman M, Wibowo A, Fang X, Zhu J-K (2011) De novo-engineered transcription activator-like effector (TALE) hybrid nuclease with novel DNA binding specificity creates double-strand breaks. Proc Natl Acad Sci USA 108:2623–2628
Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM (2013) RNA-guided human genome engineering via Cas9. Science 339:823–826
Mao H, Sun S, Yao J, Wang C, Yu S, Xu C, Li X, Zhang Q (2010) Linking differential domain functions of the GS3 protein to natural variation of grain size in rice. Proc Natl Acad Sci USA 107:19579–19584
McCallum CM, Comai L, Greene EA, Henikoff S (2000) Targeted screening for induced mutations. Nat Biotech 18:455–457
Miura K, Ikeda M, Matsubara A, Song XJ, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42:545–549
Naranjo T, Roca A, Goicoechea PG, Giraldez R (1987) Arm homoeology of wheat and rye chromosomes. Genome 29:873–882
Orozco-Arroyo G, Paolo D, Ezquer I, Colombo L (2015) Networks controlling seed size in Arabidopsis. Plant Reprod 28:17–32
Qin L, Hao C, Hou J, Wang Y, Li T, Wang L, Ma Z, Zhang X (2014) Homologous haplotypes, expression, genetic effects and geographic distribution of the wheat yield gene TaGW2. BMC Plant Biol 14:107
Rawat N, Sehgal SK, Joshi A, Rothe N, Wilson DL, McGraw N, Vadlani PV, Li W, Gill BS (2012) A diploid wheat TILLING resource for wheat functional genomics. BMC Plant Biol 12:205
Segami S, Kono I, Ando T, Yano M, Kitano H, Miura K, Iwasaki Y (2012) Small and round seed 5 gene encodes alpha-tubulin regulating seed cell elongation in rice. Rice (N Y) 5:4
Shan Q, Zhang Y, Chen K, Zhang K, Gao C (2015) Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnol J 13:791–800
Si L, Chen J, Huang X, Gong H, Luo J, Hou Q, Zhou T, Lu T, Zhu J, Shangguan Y, Chen E, Gong C, Zhao Q, Jing Y, Zhao Y, Li Y, Cui L, Fan D, Lu Y, Weng Q, Wang Y, Zhan Q, Liu K, Wei X, An K, An G, Han B (2016) OsSPL13 controls grain size in cultivated rice. Nat Genet 48:447–456
Simmonds J, Scott P, Leverington-Waite M, Turner AS, Brinton J, Korzun V, Snape J, Uauy C (2014) Identification and independent validation of a stable yield and thousand grain weight QTL on chromosome 6A of hexaploid wheat (Triticum aestivum L.). BMC Plant Biol 14:191
Simmonds J, Scott P, Brinton J, Mestre TC, Bush M, Del Blanco A, Dubcovsky J, Uauy C (2016) A splice acceptor site mutation in TaGW2-A1 increases thousand grain weight in tetraploid and hexaploid wheat through wider and longer grains. Theor Appl Genet 129:1099–1112
Slade AJ, Fuerstenberg SI, Loeffler D, Steine MN, Facciotti D (2005) A reverse genetic, nontransgenic approach to wheat crop improvement by TILLING. Nat Biotechnol 23:75–81
Su Z, Hao C, Wang L, Dong Y, Zhang X (2011) Identification and development of a functional marker of TaGW2 associated with grain weight in bread wheat (Triticum aestivum L.). Theor Appl Genet 122:211–223
Symington LS, Gautier J (2011) Double-strand break end resection and repair pathway choice. Annu Rev Genet 45:271–274
The International Wheat Genome Sequencing Consortium (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345(6194):1251788. doi:10.1126/science.1251788
Uauy C, Paraiso F, Colasuonno P, Tran RK, Tsai H, Berardi S, Comai L, Dubcovsky J (2009) A modified TILLING approach to detect induced mutations in tetraploid and hexaploid wheat. BMC Plant Biol 9:115
Wang E, Wang J, Zhu X, Hao W, Wang L, Li Q, Zhang L, He W, Lu B, Lin H, Ma H, Zhang G, He Z (2008) Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat Genet 40:1370–1374
Wang S, Wu K, Yuan Q, Liu X, Liu Z, Lin X, Zeng R, Zhu H, Dong G, Qian Q, Zhang G, Fu X (2012) Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet 44:950–954
Wang Y, Cheng X, Shan Q, Zhang Y, Liu J, Gao C, Qiu J (2014) Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nat Biotechnol 32:947–951
Wang S, Li S, Liu Q, Wu K, Zhang J, Wang S, Wang Y, Chen X, Zhang Y, Gao C, Wang F, Huang H, Fu X (2015a) The OsSPL16-GW7 regulatory module determines grain shape and simultaneously improves rice yield and grain quality. Nat Genet 47:949–954
Wang S, Zhang X, Chen F, Cui D (2015b) A single-nucleotide polymorphism of TaGS5 gene revealed its association with kernel weight in chinese bread whea. Front Plant Sci 6:1166
Weeks DP, Spalding MH, Yang B (2016) Use of designer nucleases for targeted gene and genome editing in plants. Plant Biotechnol J 14:483–495
Weng J, Gu S, Wan X, Gao H, Guo T, Su N, Lei C, Zhang X, Cheng Z, Guo X, Wang J, Jiang L, Zhai H, Wan J (2008) Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Res 18:1199–1209
Yu F, Li J, Huang Y, Liu L, Li D, Chen L, Luan S (2014) FERONIA receptor kinase controls seed size in Arabidopsis thaliana. Mol Plant 7:920–922
Zhang L, Zhao YL, Gao LF, Zhao GY, Zhou RH, Zhang BS, Jia JZ (2012) TaCKX6-D1, the ortholog of rice OsCKX2, is associated with grain weight in hexaploid wheat. N Phytol 195:574–584
Zhang Y, Liu J, Xia X, He Z (2014) TaGS-D1, an ortholog of rice OsGS3, is associated with grain weight and grain length in common wheat. Mol Breed 34:1097–1107
Zhou J, Peng Z, Long J, Sosso D, Liu B, Eom JS, Huang S, Liu S, Vera Cruz C, Frommer WB, White FF, Yang B (2015) Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J 82:632–643
Zuo J, Li J (2014) Molecular genetic dissection of quantitative trait loci regulating rice grain size. Annu Rev Genet 48:99–118
Acknowledgements
This work is supported by a USDA NIFA-IWYP project (2016-06712).
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Communicated by Rajeev K. Varshney.
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Li, W., Yang, B. Translational genomics of grain size regulation in wheat. Theor Appl Genet 130, 1765–1771 (2017). https://doi.org/10.1007/s00122-017-2953-x
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DOI: https://doi.org/10.1007/s00122-017-2953-x