Genome-editing of a circadian clock gene <i>TaPRR95</i> facilitates wheat peduncle growth and heading date

Mingxue Fu; Shaoshuai Liu; Yuqing Che; Dada Cui; Zhongyin Deng; Yang Li; Xinyu Zou; Xingchen Kong; Guoliang Chen; Min Zhang; Yifan Liu; Xiang Wang; Wei Liu; Danmei Liu; Shuaifeng Geng; Aili Li; Long Mao

doi:10.1016/j.jgg.2024.05.011

Volume 51 Issue 10

Oct. 2024

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Article Navigation > Journal of Genetics and Genomics > 2024 > 51(10): 1101-1110

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Genome-editing of a circadian clock gene TaPRR95 facilitates wheat peduncle growth and heading date

doi: 10.1016/j.jgg.2024.05.011

a. State Key Laboratory of Crop Gene Resources and Breeding and National Key Facility for Crop Resources and Genetic Improvement, Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing 100081, China;
b. College of Life Sciences, Henan Normal University, Xinxiang, Henan 453007, China;
c. College of Agronomy, Sichuan Agricultural University, Chengdu, Sichuan 610106, China;
d. College of Agronomy, Henan Agricultural University, Zhengzhou, Henan 450002, China;
e. School of Life Science, Shanxi University, Taiyuan, Shanxi 030006, China

Funds:

We are grateful for the funding from STI 2030－Major Projects (2023ZD0406802), the National Natural Science Foundation of China (32072066, 32172050, 3220151460), Hainan Yazhou Bay Seed Lab (B21HJ0215), CAAS Agricultural Science and Technology Innovation Program (CAAS-ZDRW202002, CAAS-ZDRW202201), and Hebei Natural Science Foundation (C2021205013).

Received Date: 2024-02-13
Accepted Date: 2024-05-28
Rev Recd Date: 2024-05-27

Available Online: 2025-06-06

Publish Date: 2024-06-06

Abstract

Abstract

Plant height and heading date are important agronomic traits in wheat (Triticum aestivum L.) that affect final grain yield. In wheat, knowledge of pseudo-response regulator (PRR) genes on agronomic traits is limited. Here, we identify a wheat TaPRR95 gene by genome-wide association studies to be associated with plant height. Triple allele mutant plants produced by CRISPR/Cas9 show increased plant height, particularly the peduncle, with an earlier heading date. The longer peduncle is mainly caused by the increased cell elongation at its upper section, whilst the early heading date is accompanied by elevated expression of flowering genes, such as TaFT and TaCO1. A peduncle-specific transcriptome analysis reveals up-regulated photosynthesis genes and down-regulated IAA/Aux genes for auxin signaling in prr95 plants that may act as a regulatory mechanism to promote robust plant growth. A haplotype analysis identifies a TaPRR95-B haplotype (Hap2) to be closely associated with reduced plant height and increased thousand-grain weight. Moreover, the Hap2 frequency is higher in cultivars than that in landraces, suggesting the artificial selection on the allele during wheat breeding. These findings suggest that TaPRR95 is a regulator for plant height and heading date, thereby providing an important target for wheat yield improvement.
- Pseudo-response regulator (PRR),
- TaPRR95,
- CRISPR/Cas9,
- Plant height,
- Heading date,
- Photosynthesis,
- Phytohormone,
- Wheat

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References(39)

References

Appels, R., Eversole, K., Stein, N., Feuillet, C., Keller, B., Rogers, J., Pozniak, C.J., Choulet, F., Distelfeld, A., Poland, J., et al., 2018. Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science (New York, N.Y.) 361, eaar7191.

Arjona, J.M., Royo, C., Dreisigacker, S., Ammar, K., Villegas, D., 2018. Effect of Ppd-A1 and Ppd-B1 allelic variants on grain number and thousand kernel weight of durum wheat and their impact on final grain yield. Front. Plant Sci. 9, 888.

Beales, J., Turner, A., Griffiths, S., Snape, J.W., Laurie, D.A., 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.

Cui, Y., Xu, Z., and Xu, Q. (2021). Elucidation of the relationship between yield and heading date using CRISPR/Cas9 system-induced mutation in the flowering pathway across a large latitudinal gradient. Mol. Breed. 41, 23.

Farre, E.M., Liu, T., 2013. The PRR family of transcriptional regulators reflects the complexity and evolution of plant circadian clocks. Curr. Opin. Plant Biol. 16, 621-629.

Fornara, F., Panigrahi, K.C., Gissot, L., Sauerbrunn, N., Ruhl, M., Jarillo, J.A., Coupland, G., 2009. Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev. Cell 17, 75-86.

Gao, H., Jin, M., Zheng, X.M., Chen, J., Yuan, D., Xin, Y., Wang, M., Huang, D., Zhang, Z., Zhou, K., et al., 2014. Days to heading 7, a major quantitative locus determining photoperiod sensitivity and regional adaptation in rice. Proc. Natl. Acad. Sci. U. S. A. 111, 16337-16342.

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.

Hayama, R., Sarid-Krebs, L., Richter, R., Fernandez, V., Jang, S., Coupland, G., 2017. PSEUDO RESPONSE REGULATORs stabilize CONSTANS protein to promote flowering in response to day length. EMBO J. 36, 904-918.

Hotta, C.T. 2022. The evolution and function of the PSEUDO RESPONSE REGULATOR gene family in the plant circadian clock. Genet. Mol. Biol. 45, e20220137.

Kong, X., Wang, F., Wang, Z., Gao, X., Geng, S., Deng, Z., Zhang, S., Fu, M., Cui, D., Liu, S., et al., 2023. Grain yield improvement by genome editing of TaARF12 that decoupled peduncle and rachis development trajectories via differential regulation of gibberellin signalling in wheat. Plant Biotechnol. J. 21, 1990-2001.

Legnaioli, T., Cuevas, J., Mas, P., 2009. TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought. EMBO J. 28, 3745-3757.

Li, A., Hao, C., Wang, Z., Geng, S., Jia, M., Wang, F., Han, X., Kong, X., Yin, L., Tao, S., et al., 2022. Wheat breeding history reveals synergistic selection of pleiotropic genomic sites for plant architecture and grain yield. Mol. Plant 15, 504-519.

Li, J., Qiu, J.X., Zeng, Q.H., Yi, Z., Zhang, N., Xu, S.X., Jin, J., Dong, Z.C., Chen, L., and Huang, W. 2023. OsTOC1 plays dual roles in the regulation of plant circadian clock by functioning as a direct transcription activator or repressor. Cell Rep. 42, 112765.

Lu, S., Dong, L., Fang, C., Liu, S., Kong, L., Cheng, Q., Chen, L., Su, T., Nan, H., Zhang, D., et al., 2020. Stepwise selection on homeologous PRR genes controlling flowering and maturity during soybean domestication. Nat. Genet. 52, 428-436.

Marchler-Bauer, A., Bo, Y., Han, L., He, J., Lanczycki, C.J., Lu, S., Chitsaz, F., Derbyshire, M.K., Geer, R.C., Gonzales, N.R., et al., 2017. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 45, D200-d203.

Matsushika, A., Makino, S., Kojima, M., Mizuno, T., 2000. Circadian waves of expression of the APRR1/TOC1 family of pseudo-response regulators in Arabidopsis thaliana: insight into the plant circadian clock. Plant Cell Physiol. 41, 1002-1012.

Murakami, M., Ashikari, M., Miura, K., Yamashino, T., Mizuno, T., 2003. The evolutionarily conserved OsPRR quintet: rice pseudo-response regulators implicated in circadian rhythm. Plant Cell Physiol. 44, 1229-1236.

Murphy, R.L., Klein, R.R., Morishige, D.T., Brady, J.A., Rooney, W.L., Miller, F.R., Dugas, D.V., Klein, P.E., Mullet, J.E., 2011. Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum. Proc. Natl. Acad. Sci. U. S. A. 108, 16469-16474.

Nakamichi, N., Kiba, T., Henriques, R., Mizuno, T., Chua, N.H., Sakakibara, H., 2010. PSEUDO-RESPONSE REGULATORS 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock. The Plant cell 22 (3), 594-605.

Nakamichi, N., Kita, M., Ito, S., Yamashino, T., Mizuno, T., 2005. PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, Together Play Essential Roles Close to the Circadian Clock of Arabidopsis thaliana. Plant Cell Physiol. 46, 686-698.

Nakamichi, N., Kudo, T., Makita, N., Kiba, T., Kinoshita, T., and Sakakibara, H., 2020. Flowering time control in rice by introducing Arabidopsis clock-associated PSEUDO-RESPONSE REGULATOR 5. Biosci. Biotechnol. Biochem. 84, 970-979.

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

Seki, M., Chono, M., Matsunaka, H., Fujita, M., Oda, S., Kubo, K., Kiribuchi-Otobe, C., Kojima, H., Nishida, H., Kato, K., 2011. Distribution of photoperiod-insensitive alleles Ppd-B1a and Ppd-D1a and their effect on heading time in Japanese wheat cultivars. Breed Sci. 61, 405-412.

Sun, H., Guo, Z., Gao, L., Zhao, G., Zhang, W., Zhou, R., Wu, Y., Wang, H., An, H., Jia, J., 2014. DNA methylation pattern of Photoperiod-B1 is associated with photoperiod insensitivity in wheat (Triticum aestivum). New Phytol. 204, 682-692.

Sun, H., Zhang, W., Wu, Y., Gao, L., Cui, F., Zhao, C., Guo, Z., Jia, J., 2020. The circadian clock gene, TaPRR1, is associated with yield-related traits in wheat (Triticum aestivum L.). Front. Plant Sci. 11.

Sun, K., Zong, W., Xiao, D., Wu, Z., Guo, X., Li, F., Song, Y., Li, S., Wei, G., Hao, Y., et al., 2023. Effects of the core heading date genes Hd1, Ghd7, DTH8, and PRR37 on yield-related traits in rice. Theor. Appl. Genet. 136, 227.

Turner, A., Beales, J., Faure, S., Dunford, R.P., Laurie, D.A., 2005. The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science (New York, N.Y.) 310, 1031-1034.

Waddington, S., Cartwright, P., Wall, P., 1983. A quantitative scale of spike initial and pistil development in barley and wheat. Annals of Botany 51, 119-130.

Wang, T., Su, N., Lu, J., Zhang, R., Sun, X., Weining, S., 2023. Genome-wide association studies of peduncle length in wheat under rain-fed and irrigating field conditions. J. Plant Physiol. 280, 153854.

Wang, L., Sun, S., Wu, T., Liu, L., Sun, X., Cai, Y., Li, J., Jia, H., Yuan, S., Chen, L., et al., 2020. Natural variation and CRISPR/Cas9-mediated mutation in GmPRR37 affect photoperiodic flowering and contribute to regional adaptation of soybean. Plant Biotechnol. J. 18, 1869-1881.

Wang, Y., Wu, F., Zhou, S., Chen, W., Li, C., Duan, E., Wang, J., Cheng, Z., Zhang, X., Lin, Q., et al., 2022. Clock component OsPRR59 delays heading date by repressing transcription of Ehd3 in rice. The Crop J. 10, 1570-1579.

Wei, H., Wang, X., He, Y., Xu, H., Wang, L., 2021. Clock component OsPRR73 positively regulates rice salt tolerance by modulating OsHKT2;1-mediated sodium homeostasis. Embo J. 40(3), e105086.

Wilhelm, E.P., Turner, A.S., Laurie, D.A., 2009. Photoperiod insensitive Ppd-A1a mutations in tetraploid wheat (Triticum durum Desf.). Theor. Appl. Genet. 118, 285-294.

Yang, M., Han, X., Yang, J., Jiang, Y., Hu, Y., 2021. The Arabidopsis circadian clock protein PRR5 interacts with and stimulates ABI5 to modulate abscisic acid signaling during seed germination. The Plant cell 33, 3022-3041.

Zhang, W., Zhao, G., Gao, L., Kong, X., Guo, Z., Wu, B., Jia, J., 2016. Functional studies of heading date-related gene TaPRR73, a paralog of Ppd1 in common wheat. Front. Plant Sci. 7.

Zhao, X.Y., Hong, P., Wu, J.Y., Chen, X.B., Ye, X.G., Pan, Y.Y., Wang, J., Zhang, X.S., 2016. The tae-miR408-mediated control of TaTOC1 genes transcription is required for the regulation of heading time in wheat. Plant Physiol. 170, 1578-1594.

Zhou, Y., Chen, Z., Cheng, M., Chen, J., Zhu, T., Wang, R., Liu, Y., Qi, P., Chen, G., Jiang, Q., et al., 2018. Uncovering the dispersion history, adaptive evolution and selection of wheat in China. Plant Biotechnol. J. 16, 280-291.

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

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