Genome-wide analysis of Q binding reveals a regulatory network that coordinates wheat grain yield and grain protein content

Jing Zhu; Qing Chen; Zhenru Guo; Yan Wang; Qingcheng Li; Yang Li; Lu Lei; Caihong Liu; Yue Li; Rui Tang; Jie Tang; Ziyi Zhang; Shijing Peng; Mi Zhang; Zhongxu Chen; Li Kong; Mei Deng; Qiang Xu; Yazhou Zhang; Qiantao Jiang; Jirui Wang; Guoyue Chen; Yunfeng Jiang; Yuming Wei; Youliang Zheng; Pengfei Qi

doi:10.1016/j.jgg.2025.02.011

Volume 52 Issue 12

Dec. 2025

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2025 > 52(12): 1576-1587

PDF( 0 KB)

Genome-wide analysis of Q binding reveals a regulatory network that coordinates wheat grain yield and grain protein content

doi: 10.1016/j.jgg.2025.02.011

a State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Chengdu, Sichuan 611130, China;
b Triticeae Research Institute, Sichuan Agricultural University, Chengdu, Sichuan 611130, China

Funds:

This study was supported by the National Key Research and Development Program of China (2023YFD1200404), the Science and Technology Department of Sichuan Province (2024ZYD0160), and the National Natural Science Foundation of China (32072054).

Received Date: 2024-11-05
Accepted Date: 2025-02-20
Rev Recd Date: 2025-02-19
Publish Date: 2025-12-31

Abstract

Abstract

Wheat is an important cereal crop used to produce diverse and popular food worldwide because of its high grain yield (GY) and grain protein content (GPC). However, GY and GPC are usually negatively correlated. We previously reported that favorable alleles of the wheat domestication gene Q can synchronously increase GY and GPC, but the underlying mechanisms remain largely unknown. In this study, we investigate the regulatory network involving Q associated with GY and GPC in young grains through DNA affinity purification sequencing and transcriptome sequencing analyses, electrophoretic mobility shift and dual-luciferase assays, and transgenic approaches. Three Q-binding motifs, namely TTAAGG, AAACA[A/T]A, and GTAC[T/G]A, are identified. Notably, genes related to photosynthesis or carbon and nitrogen metabolism are enriched and regulated by Q. Moreover, Q is revealed to bind directly to its own gene and the glutamine synthetase gene GSr-4D to increase expression, thereby influencing nitrogen assimilation during the grain filling stage and increasing GPC. Considered together, our findings provide molecular evidence of the positive regulatory effects of Q on wheat GY and GPC.
- Grain yield,
- Grain protein content,
- Q gene,
- Glutamine synthetase,
- Mechanism,
- Wheat

FullText(HTML)

References(103)

References

Abbas, N., Maurya, J.P., Senapati, D., Gangappa, S.N., Chattopadhyay, S., 2014. Arabidopsis CAM7 and HY5 physically interact and directly bind to the HY5 promoter to regulate its expression and thereby promote photomorphogenesis. Plant Cell 26, 1036-1052.

Bahaji, A., Li, J., Angela Maria, S.L., Baroja-Fernandez, E., Francisco Jose, M., Ovecka, M., Almagro, G., Montero, M., Ezquer, I., Etxeberria, E., et al., 2014. Starch biosynthesis, its regulation and biotechnological approaches to improve crop yields. Biotechnol. Adv. 32, 87-106.

Baslam, M., Mitsui, T., Sueyoshi, K., Ohyama, T., 2021. Recent advances in carbon and nitrogen metabolism in C3 plants. Int. J. Mol. Sci. 22, 318.

Bernard, S.M., Habash, D.Z., 2009. The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytol. 182, 608-620.

Bernard, S.M., Moller, A.L., Dionisio, G., Kichey, T., Jahn, T.P., Dubois, F., Baudo, M., Lopes, M.S., Terce-Laforgue, T., Foyer, C.H., et al., 2008. Gene expression, cellular localisation and function of glutamine synthetase isozymes in wheat (Triticum aestivum L.). Plant Mol. Biol. 67, 89-105.

Binkert, M., Kozma-Bognar, L., Terecskei, K., De Veylder, L., Nagy, F., Ulm, R., 2014. UV-B-responsive association of the Arabidopsis bZIP transcription factor ELONGATED HYPOCOTYL5 with target genes, including its own promoter. Plant Cell 26, 4200-4213.

Burgess, A.J., Masclaux-Daubresse, C., Strittmatter, G., Weber, A.P.M., Taylor, S.H., Harbinson, J., Yin, X.Y., Long, S., Paul, M.J., Westhoff, P., et al., 2023. Improving crop yield potential: underlying biological processes and future prospects. Food Energy Secur. 12, e435.

Chen, C.J., Chen, H., Zhang, Y., Thomas, H.R., Frank, M.H., He, Y.H., Xia, R., 2020a. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol. Plant 13, 1194-1202.

Chen, J.N., Cao, F.B., Li, H.L., Shan, S.L., Tao, Z., Lei, T., Liu, Y., Xiao, Z.W., Zou, Y.B., Huang, M., et al., 2020b. Genotypic variation in the grain photosynthetic contribution to grain filling in rice. J. Plant Physiol. 253, 153269.

Chen, L.Q., Cheung, L.S., Feng, L., Tanner, W., Frommer, W.B., 2015. Transport of sugars. Annu. Rev. Biochem. 84, 865-894.

Chen, Q., Guo, Z.R., Shi, X.L., Wei, M.Q., Fan, Y.Z., Zhu, J., Zheng, T., Wang, Y., Kong, L., Deng, M., et al., 2022. Increasing the grain yield and grain protein content of common wheat (Triticum aestivum) by introducing missense mutations in the Q gene. Int. J. Mol. Sci. 23, 10772.

Dai, S.F., Chen, H.X., Li, H.Y., Yang, W.J., Zhai, Z., Liu, Q.Y., Li, J., Yan, Z.H., 2022. Variations in the quality parameters and gluten proteins in synthetic hexaploid wheats solely expressing the Glu-D1 locus. J. Integr. Agric. 21, 1877-1885.

Debernardi, J.M., Greenwood, J.R., Jean Finnegan, E., Jernstedt, J., Dubcovsky, J., 2020. APETALA 2-like genes AP2L2 and Q specify lemma identity and axillary floral meristem development in wheat. Plant J. 101, 171-187.

Debernardi, J.M., Lin, H.Q., Chuck, G., Faris, J.D., Dubcovsky, J., 2017. microRNA172 plays a crucial role in wheat spike morphogenesis and grain threshability. Development 144, 1966-1975.

Delcour, J.A., Joye, I.J., Pareyt, B., Wilderjans, E., Brijs, K., Lagrain, B., 2012. Wheat gluten functionality as a quality determinant in cereal-based food products. Annu. Rev. Food Sci. Technol. 3, 469-492.

Dinh, T.T., Girke, T., Liu, X.G., Yant, L., Schmid, M., Chen, X.M., 2012. The floral homeotic protein APETALA2 recognizes and acts through an AT-rich sequence element. Development 139, 1978-1986.

Dobin, A., Davis, C.A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., Gingeras, T.R., 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21.

FAOSTAT. 2021. Food and Agricultural Organization of the United Nations Agriculture Databases. https://www.fao.org/faostat/en/#data/QCL.

Forde, B.G., Lea, P.J., 2007. Glutamate in plants: metabolism, regulation, and signalling. J. Exp. Bot. 58, 2339-2358.

Fu, Y.X., Guo, X.J., Cheng, M.P., Li, H.G., Liu, Z.H., Li, M.L., Chen, Q., Dong, H.X., Zhong, Z.W., Jiang Q., et al., 2024. Spatial transcriptomics uncover coordinated cellular responses to heat stress in developing wheat grains. Research Square, Preprint, DOI: 10.21203/rs.3.rs-4253930/v1.

Gadaleta, A., Nigro, D., Giancaspro, A., Blanco, A., 2011. The glutamine synthetase (GS2) genes in relation to grain protein content of durum wheat. Funct. Integr. Genomics. 11, 665-670.

Gadaleta, A., Nigro, D., Marcotuli, I., Giancaspro, A., Giove, S.L., Blanco, A., 2014. Isolation and characterisation of cytosolic glutamine synthetase (GSe) genes and association with grain protein content in durum wheat. Crop Pasture Sci. 65, 38-45.

Galili, G., Amir, R., Fernie, A.R., 2016. The regulation of essential amino acid synthesis and accumulation in plants. Annu. Rev. Plant Biol. 67, 153-178.

Garcia, A., Gaju, O., Bowerman, A.F., Buck, S.A., Evans, J.R., Furbank, R.T., Gilliham, M., Millar, A.H., Pogson, B.J., Reynolds, M.P., et al., 2022. Enhancing crop yields through improvements in the efficiency of photosynthesis and respiration. New Phytol. 237, 60-77.

Gaufichon, L., Reisdorf-Cren, M., Rothstein, S.J., Chardon, F., Suzuki, A., 2010. Biological functions of asparagine synthetase in plants. Plant Sci. 179, 141-153.

Greenwood, J.R., Finnegan, E.J., Watanabe, N., Trevaskis, B., Swain, S.M., 2017. New alleles of the wheat domestication gene Q reveal multiple roles in growth and reproductive development. Development 144, 1959-1965.

Guo, N., Zhang, S.N., Gu, M.J., Xu, G.H., 2021. Function, transport, and regulation of amino acids: what is missing in rice? Crops J. 9, 530-542.

Guo, Z.R., Chen, Q., Zhu, J., Wang, Y., Li, Y., Li, Q.C., Zhao, K., Li, Y., Tang, R., Shi, X.L., et al., 2022. The Qc5 allele increases wheat bread-making quality by regulating SPA and SPR. Int. J. Mol. Sci. 23, 7581.

Guzman, C., Ibba, M.I., Alvarez, J.B., Sissons, M., Morris, C. 2022. Wheat quality, in: Reynolds, M.P., Braun, H.J. (Eds.), Wheat Improvement: Food Security in a Changing Climate. Springer International Publishing, Cham, pp. 177-193.

Habash, D.Z., Bernard, S., Schondelmaier, J., Weyen, J., Quarrie, S.A., 2007. The genetics of nitrogen use in hexaploid wheat: N utilisation, development and yield. Theor. Appl. Genet. 114, 403-419.

Hajheidari, M., Wang, Y., Bhatia, N., Vuolo, F., Franco-Zorrilla, J.M., Karady, M., Mentink, R.A., Wu, A., Oluwatobi, B.R., Muller, B., et al., 2019. Autoregulation of RCO by low-affinity binding modulates cytokinin action and shapes leaf diversity. Curr. Biol. 29, 4183-4192.

Hildebrandt, T.M., Nesi, A.N., Arau´jo, W.L., Braun, H.P., 2015. Amino acid catabolism in plants. Mol. Plant 8, 1563-1579.

Hu, M.Y., Zhao, X.Q., Liu, Q., Hong, X., Zhang, W., Zhang, Y.J., Sun, L.J., Li, H., Tong, Y.P., 2018. Transgenic expression of plastidic glutamine synthetase increases nitrogen uptake and yield in wheat. Plant Biotechnol. J. 16, 1858-1867.

Huang, L.C., Tan, H.Y., Zhang, C.Q., Li, Q.F., Liu, Q.Q., 2021. Starch biosynthesis in cereal endosperms: an updated review over the last decade. Plant Commun. 2, 100237.

Huang, X., Wang, C.Y., Hou, J.F., Du, C.Y., Liu, S.J., Kang, J., Lu, H.F., Xie, Y.X., Guo, T.C., Ma, D.Y., 2020. Coordination of carbon and nitrogen accumulation and translocation of winter wheat plant to improve grain yield and processing quality. Sci. Rep. 10, 10340.

Ishida, Y., Tsunashima, M., Hiei, Y., Komari, T., 2015. Wheat (Triticum aestivum L.) transformation using immature embryos, in: Wang, Kan (Ed.) Agrobacterium Protocols: Volume vol. 1. Springer New York, New York, pp. 189-198.

IWGSC, 2018. Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361, eaar7191.

Jiang, X.L., Wu, P., Tian, J.C., 2014. Genetic analysis of amino acid content in wheat grain. J. Genet. 93, 451-458.

Jiang, Y.F., Chen, Q., Wang, Y., Guo, Z.R., Xu, B.J., Zhu, J., Zhang, Y.Z., Gong, X., Luo, C.H., Wu, W., et al., 2019. Re-acquisition of the brittle rachis trait via a transposon insertion in domestication gene Q during wheat de-domestication. New Phytol. 224, 961-973.

Julius, B.T., Leach, K.A., Tran, T.M., Mertz, R.A., Braun, D.M., 2017. Sugar transporters in plants: new insights and discoveries. Plant Cell Physiol. 58, 1442-1460.

Kasemsap, P., Bloom, A.J., 2023. Breeding for higher yields of wheat and rice through modifying nitrogen metabolism. Plants 12, 85.

Kichey, T., Heumez, E., Pocholle, D., Pageau, K., Vanacker, H., Dubois, F., Gouis, J.L., Hirel, B., 2006. Combined agronomic and physiological aspects of nitrogen management in wheat highlight a central role for glutamine synthetase. New Phytol. 169, 265-278.

Kolberg, L., Raudvere, U., Kuzmin, I., Adler, P., Vilo, J., Peterson, H., 2023. g:Profiler-interoperable web service for functional enrichment analysis and gene identifier mapping (2023 update). Nucleic Acids Res. 51, W207-W212.

Laidig, F., Piepho, H.P., Rentel, D., Drobek, T., Meyer, U., Huesken, A., 2017. Breeding progress, environmental variation and correlation of winter wheat yield and quality traits in German official variety trials and on-farm during 1983-2014. Theor. Appl. Genet. 130, 223-245.

Li, B., Dewey, C.N., 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinf. 12, 323.

Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., Subgroup, G.P.D.P., 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078-2079.

Li, M.J., Wang, T., Zhang, H., Liu, S., Li, W.H., Abou Elwafa, S.F., Tian, H., 2022. TaNRT2.1-6B is a dual-affinity nitrate transporter contributing to nitrogen uptake in bread wheat under both nitrogen deficiency and sufficiency. Crops J. 10, 993-1005.

Li, Q.H., Brown, J.B., Huang, H., Bickel, P.J., 2011. Measuring reproducibility of high-throughput experiments. Ann. Appl. Stat. 5, 1752-1779.

Li, W.T., Zhu, Z.W., Chern, M., Yin, J.J., Yan, C., Ra, L., Cheng, M.P., He, M., Wang, K., Wang, J., et al., 2017. A natural allele of a transcription factor in rice confers broad-spectrum blast resistance. Cell 170, 114-126.

Liu, H.Y., Wang, K., Tang, H.L., Gong, Q., Du, L.P., Pei, X.W., Ye, X.G., 2020. CRISPR/Cas9 editing of wheat TaQ genes alters spike morphogenesis and grain threshability. J. Genet. Genomics 47, 563-575.

Liu, J., Cheng, X.L., Liu, P., Sun, J.Q., 2017a. miR156-targeted SBP-Box transcription factors interact with DWARF53 to regulate TEOSINTE BRANCHED1 and BARREN STALK1 expression in bread wheat. Plant Physiol. 174, 1931-1948.

Liu, P., Liu, J., Dong, H.X., Sun, J.Q., 2017b. Functional regulation of Q by microRNA172 and transcriptional co-repressor TOPLESS in controlling bread wheat spikelet density. Plant Biotechnol. J. 16, 495-506.

Liu, X.J., Hu, B., Chu, C.C., 2022. Nitrogen assimilation in plants: current status and future prospects. J. Genet. Genomics 49, 394-404.

Livak, K.J., Schmittgen, T.D., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402-408.

Long, X.Y., Wang, J.R., Ouellet, T., Rocheleau, H., Wei, Y.M., Pu, Z.E., Jiang, Q.T., Lan, X.J., Zheng, Y.L., 2010. Genome-wide identification and evaluation of novel internal control genes for Q-PCR based transcript normalization in wheat. Plant Mol. Biol. 74, 307-311.

Love, M.I., Huber, W., Anders, S., 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550.

Lu, Z.F., Yu, H., Xiong, G.S., Wang, J., Jiao, Y.Q., Liu, G.F., Jing, Y.H., Meng, X.B., Hu, X.M., Qian, Q., et al., 2013. Genome-wide binding analysis of the transcription activator ideal plant architecture1 reveals a complex network regulating rice plant architecture. Plant Cell 25, 3743-3759.

Ma, H.L., Yang, Y.H., Wu, D.M., Xiang, G., Luo, T., Huang, X.L., Yang, H.K., Zheng, T., Fan, G.Q., 2024. Changes in free amino acid and protein polymerization in wheat caryopsis and endosperm during filling after shading. Front. Plant Sci. 15, 1344972.

Mirosavljevic, M., Momcilovic, V., Zivancev, D., Acin, V., Jockovic, B., Mikic, S., Takac, V., Dencic, S., 2020. Genetic improvement of grain yield and bread-making quality of winter wheat over the past 90 years under the Pannonian Plain conditions. Euphytica 216, 184.

Nigro, D., Gadaleta, A., Mangini, G., Colasuonno, P., Marcotuli, I., Giancaspro, A., Giove, S.L., Simeone, R., Blanco, A., 2019. Candidate genes and genome-wide association study of grain protein content and protein deviation in durum wheat. Planta 249, 1157-1175.

Oury, F.X., Godin, C., 2007. Yield and grain protein concentration in bread wheat: how to use the negative relationship between the two characters to identify favourable genotypes? Euphytica 157, 45-57.

Patil, V., McDermott, H.I., McAllister, T., Cummins, M., Silva, J.C., Mollison, E., Meikle, R., Morris, J., Hedley, P.E., Waugh, R., et al., 2019. APETALA2 control of barley internode elongation. Development 146, dev170373.

Pechanek, U., Karger, A., Groger, S., Charvat, B., Schoggl, G., Lelley, T., 1997. Effect of nitrogen fertilization on quantity of flour protein components, dough properties, and breadmaking quality of wheat. Cereal Chem. 74, 800-805.

Pei, H.C., Teng, W., Gao, L.F., Gao, H.B., Ren, X.N., Liu, Y.H., Jia, J.Z., Tong, Y.P., Wang, Y.H., Lu, Z.F., 2023. Low-affinity SPL binding sites contribute to subgenome expression divergence in allohexaploid wheat. Sci. China Life Sci. 66, 819-834.

Peng, B., Kong, H.L., Li, Y.B., Wang, L.Q., Zhong, M., Sun, L., Gao, G.J., Zhang, Q.L., Luo, L.J., Wang, G.W., et al., 2014. OsAAP6 functions as an important regulator of grain protein content and nutritional quality in rice. Nat. Commun. 5, 4857.

Peng, Y.C., Zhao, Y., Yu, Z.T., Zeng, J.B., Xu, D.G., Dong, J., Ma, W.J., 2022. Wheat quality formation and its regulatory mechanism. Front. Plant Sci. 13, 834654.

Raffan, S., Halford, N.G., 2019. Acrylamide in food: progress in and prospects for genetic and agronomic solutions. Ann. Appl. Biol. 175, 259-281.

Raffan, S., Oddy, J., Mead, A., Barker, G., Curtis, T., Usher, S., Burt, C., Halford, N.G., 2023. Field assessment of genome-edited, low asparagine wheat: europe's first CRISPR wheat field trial. Plant Biotechnol. J. 21, 1097-1099.

Ramirez, F., Ryan, D.P., Gruning, B., Bhardwaj, V., Kilpert, F., Richter, A.S., Heyne, S., Dundar, F., Manke, T., 2016. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 44, W160-W165.

Rolletschek, H., Hosein, F., Miranda, M., Heim, U., Gotz, K.P., Schlereth, A., Borisjuk, L., Saalbach, I., Wobus, U., Weber, H., 2005. Ectopic expression of an amino acid transporter (VfAAP1) in seeds of Vicia narbonensis and pea increases storage proteins. Plant Physiol. 137, 1236-1249.

Saini, P., Sheikh, I., Saini, D.K., Mir, R.R., Dhaliwal, H.S., Tyagi, V., 2022. Consensus genomic regions associated with grain protein content in hexaploid and tetraploid wheat. Front. Genet. 13, 1021180.

Shewry, P.R., 2009. Wheat. J. Exp. Bot. 60, 1537-1553.

Shi, X.L., Cui, F., Han, X.Y., He, Y.L., Zhao, L., Zhang, N., Zhang, H., Zhu, H.D., Liu, Z.X., Ma, B., et al., 2022. Comparative genomic and transcriptomic analyses uncover the molecular basis of high nitrogen-use efficiency in the wheat cultivar Kenong 9204. Mol. Plant 15, 1440-1456.

Shiferaw, B., Smale, M., Braun, H.J., Duveiller, E., Reynolds, M., Muricho, G., 2013. Crops that feed the world 10. Past successes and future challenges to the role played by wheat in global food security. Food Secur. 5, 291-317.

Simons, K.J., Fellers, J.P., Trick, H.N., Zhang, Z.C., Gill, B.S., Faris, J.D., 2006. Molecular characterization of the major wheat domestication gene Q. Genetics 172, 547-555.

Sosso, D., Luo, D.P., Li, Q.B., Sasse, J., Yang, J.L., Gendrot, G., Suzuki, M., Koch, K.E., McCarty, D.R., Chourey, P.S., et al., 2015. Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport. Nat. Genet. 47, 1489-1493.

Tegeder, M., Masclaux-Daubresse, C., 2018. Source and sink mechanisms of nitrogen transport and use. New Phytol. 217, 35-53.

Thomsen, H.C., Eriksson, D., Moller, I.S., Schjoerring, J.K., 2014. Cytosolic glutamine synthetase: a target for improvement of crop nitrogen use efficiency? Trends Plant Sci. 19, 656-663.

Thorvaldsdottir, H., Robinson, J.T., Mesirov, J.P., 2013. Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Briefings Bioinf. 14, 178-192.

Thorwarth, P., Piepho, H.P., Zhao, Y., Ebmeyer, E., Schacht, J., Schachschneider, R., Kazman, E., Reif, J.C., Wurschum, T., Longin, C.F.H., et al., 2018. Higher grain yield and higher grain protein deviation underline the potential of hybrid wheat for a sustainable agriculture. Plant Breed. 137, 326-337.

Tian, T., Liu, Y., Yan, H.Y., You, Q., Yi, X., Du, Z., Xu, W.Y., Su, Z., 2017. agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Res. 45, W122-W129.

Wang, M.Y., Li, Z.J., Zhang, Y.E., Zhang, Y.Y., Xie, Y.L., Ye, L.H., Zhuang, Y.L., Lin, K.D., Zhao, F., Guo, J.Y., et al., 2021. An atlas of wheat epigenetic regulatory elements reveals subgenome divergence in the regulation of development and stress responses. Plant Cell 33, 865-881.

Wang, H., Wang, Z.X., Tian, H.Y., Zeng, Y.L., Xue, H., Mao, W.T., Zhang, L.Y., Chen, J.N., Lu, X., Zhu, Y., et al., 2025. The miR172a-SNB module orchestrates induced and adult resistance to multiple diseases via MYB30-mediated lignin accumulation in rice. Mol. Plant 18, 59-75.

Wickham, H. 2016. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag.

Wu, A., Hammer, G.L., Doherty, A., von Caemmerer, S., Farquhar, G.D., 2019. Quantifying impacts of enhancing photosynthesis on crop yield. Nat. Plants 5, 380-388.

Wu, D.X., Li, Y., Cao, Y.N., Hu, R.P., Wu, X., Zhang, W., Tao, W.Q., Xu, G.H., Wang, X.C., Zhang, Y.L., 2021. Increased glutamine synthetase by overexpression of TaGS1 improves grain yield and nitrogen use efficiency in rice. Plant Physiol. Biochem. 169, 259-268.

Xiao, J., Liu, B., Yao, Y.Y., Guo, Z.F., Jia, H.Y., Kong, L.R., Zhang, A.M., Ma, W.J., Ni, Z.F., Xu, S.B., et al., 2022. Wheat genomic study for genetic improvement of traits in China. Sci. China Life Sci. 65, 1718-1775.

Xu, B.J., Chen, Q., Zheng, T., Jiang, Y.F., Qiao, Y.Y., Guo, Z.R., Cao, Y.L., Wang, Y., Zhang, Y.Z., Zong, L.J., et al., 2018. An overexpressed Q allele leads to increased spike density and improved processing quality in common wheat (Triticum aestivum). G3: Genes, Genomes, Genet. 8, 771-778.

Xuan, W., Beeckman, T., Xu, G.H., 2017. Plant nitrogen nutrition: sensing and signaling. Curr. Opin. Plant Biol. 39, 57-65.

Yang, F., Zhang, J.J., Zhao, Y., Liu, Q.E., Islam, S., Yang, W.Y., Ma, W.J., 2022. Wheat glutamine synthetase TaGSr-4B is a candidate gene for a QTL of thousand grain weight on chromosome 4B. Theor. Appl. Genet. 135, 2369-2384.

Yang, J., Luo, D.P., Yang, B., Frommer, W.B., Eom, J.S., 2018. SWEET11 and 15 as key players in seed filling in rice. New Phytol. 218, 604-615.

Yu, G.C., Wang, L.G., He, Q.Y., 2015. ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization. Bioinformatics 31, 2382-2383.

Zadoks, J.C., Chang, T.T., Konzak C.F., 1974. A decimal code for the growth stages of cereals. Weed Res. 14, 415-421.

Zhang, C.C., Zhou, C.Z., Burnap, R.L., Peng, L., 2018. Carbon/nitrogen metabolic balance: lessons from cyanobacteria. Trends Plant Sci. 23, 1116-1130.

Zhang, J.Z., Xiong, H.C., Guo, H.J., Li, Y.T., Xie, X.M., Xie, Y.D., Zhao, L.S., Gu, J.Y., Zhao, S.R., Ding, Y.P., et al., 2022. Identification of the Q gene playing a role in spike morphology variation in wheat mutants and its regulatory network. Front. Plant Sci. 12, 807731.

Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W., et al., 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137.

Zhang, Z.C., Belcram, H., Gornicki, P., Charles, M., Just, J., Huneau, C., Magdelenat, G., Couloux, A., Samain, S., Gill, B.S., et al., 2011. Duplication and partitioning in evolution and function of homoeologous Q loci governing domestication characters in polyploid wheat. Proc. Natl. Acad. Sci. U. S. A 108, 18737-18742.

Zhang, Z.C., Li, A.L., Song, G.Y., Geng, S.F., Gill, B.S., Faris, J.D., Mao, L., 2020. Comprehensive analysis of Q gene near-isogenic lines reveals key molecular pathways for wheat domestication and improvement. Plant J. 102, 299-310.

Zhao, L., Chen, J.C., Zhang, Z.H., Wu, W.Y., Lin, X.L., Gao, M.X., Yang, Y.M., Zhao, P., Xu, S.B., Yang, C.F., et al., 2024. Deciphering the transcriptional regulatory network governing starch and storage protein biosynthesis in wheat for breeding improvement. Adv. Sci. 11, 2401383.

Zhao, Z.X., Feng, Q., Liu, P.Q., He, X.R., Zhao, J.H., Xu, Y.J., Zhang, L.L., Huang, Y.Y., Zhao, J.Q., Fan, J., et al., 2021. RPW8.1 enhances the ethylene-signaling pathway to feedback-attenuate its mediated cell death and disease resistance in Arabidopsis. New Phytol. 229, 516-531.

Zheng, T., Qi, P.F., Cao, Y.L., Han, Y.N., Ma, H.L., Guo, Z.R., Wang, Y., Qiao, Y.Y., Hua, S.Y., Yu, H.Y., et al., 2018. Mechanisms of wheat (Triticum aestivum) grain storage proteins in response to nitrogen application and its impacts on processing quality. Sci. Rep. 8, 11928.

Zhu, X.G., Long, S.P., Ort, D.R., 2010. Photosynthetic efficiency for greater yield. Annu. Rev. Plant Biol. 61, 235-261.

Zorb, C., Ludewig, U., Hawkesford, M.J., 2018. Perspective on wheat yield and quality with reduced nitrogen supply. Trends Plant Sci. 23, 1029-1037.

Relative Articles

Supplements(0)

Cited By

Proportional views