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TaMADS29 interacts with TaNF-YB1 to synergistically regulate early grain development in bread wheat

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Abstract

Grain development is a crucial determinant of yield and quality in bread wheat (Triticum aestivum L.). However, the regulatory mechanisms underlying wheat grain development remain elusive. Here we report how TaMADS29 interacts with TaNF-YB1 to synergistically regulate early grain development in bread wheat. The tamads29 mutants generated by CRISPR/Cas9 exhibited severe grain filling deficiency, coupled with excessive accumulation of reactive oxygen species (ROS) and abnormal programmed cell death that occurred in early developing grains, while overexpression of TaMADS29 increased grain width and 1,000-kernel weight. Further analysis revealed that TaMADS29 interacted directly with TaNF-YB1; null mutation in TaNF-YB1 caused grain developmental deficiency similar to tamads29 mutants. The regulatory complex composed of TaMADS29 and TaNF-YB1 exercises its possible function that inhibits the excessive accumulation of ROS by regulating the genes involved in chloroplast development and photosynthesis in early developing wheat grains and prevents nucellar projection degradation and endosperm cell death, facilitating transportation of nutrients into the endosperm and wholly filling of developing grains. Collectively, our work not only discloses the molecular mechanism of MADS-box and NF-Y TFs in facilitating bread wheat grain development, but also indicates that caryopsis chloroplast might be a central regulator of grain development rather than merely a photosynthesis organelle. More importantly, our work offers an innovative way to breed high-yield wheat cultivars by controlling the ROS level in developing grains.

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Data availability

Sequence data from this article are available at the EnsemblPlants website, http://plants.ensembl.org/index.html (TraesCS6A02G158100 (TaMADS29-A); TraesCS6B02-G186700 (TaMADS29-B); TraesCS6D01G147400 (Ta-MADS29-D); TraesCS6A02G287500 (TaNF-YB1-A); TraesCS6B02G316800 (TaNF-YB1-B); TraesCS6D02-G268200 (TaNF-YB1-D)). RNA-seq data were deposited in the NCBI with accession numbers PRJNA791126 and PRJNA790694. All other study data are included in the article and Supporting Information.

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Acknowledgements

This work was supported by the National Key Research and Development Program of China (2022YFF1002902, 2016YFD0100803). The authors are grateful to Dr.s Lubin Tan and Jinsheng Lai (China Agricultural University) for their helpful discussions and comments on the text. We thank Dr. Na Song (China Agricultural University) for helping with tissue culture and wheat transformation and Dr. Jian Chen (China Agricultural University) for suggestions about ChIP optimization.

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Liu, G., Zhang, R., Li, S. et al. TaMADS29 interacts with TaNF-YB1 to synergistically regulate early grain development in bread wheat. Sci. China Life Sci. 66, 1647–1664 (2023). https://doi.org/10.1007/s11427-022-2286-0

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