Suppressing ASPARTIC PROTEASE 1 prolongs photosynthesis and increases wheat grain weight

Nature Plants (2023)Cite

Nature Plants (2023)Cite this article

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The elongation of photosynthesis, or functional staygreen, represents a feasible strategy to propel metabolite flux towards cereal kernels. However, achieving this goal remains a challenge in food crops. Here we report the cloning of wheat CO2 assimilation and kernel enhanced 2 (cake2), the mechanism underlying the photosynthesis advantages and natural alleles amenable to breeding elite varieties. A premature stop mutation in the A-genome copy of the ASPARTIC PROTEASE 1 (APP-A1) gene increased the photosynthesis rate and yield. APP1 bound and degraded PsbO, the protective extrinsic member of photosystem II critical for increasing photosynthesis and yield. Furthermore, a natural polymorphism of the APP-A1 gene in common wheat reduced APP-A1's activity and promoted photosynthesis and grain size and weight. This work demonstrates that the modification of APP1 increases photosynthesis, grain size and yield potentials. The genetic resources could propel photosynthesis and high-yield potentials in elite varieties of tetraploid and hexaploid wheat.

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We deposited the raw sequencing data in the Gene Expression Omnibus Database under the accession code PRJNA861409. Correspondence and requests for other related information or materials should be addressed to the corresponding author. Source data are provided with this paper.

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This study was supported by the National Key Research and Development Program of China (grant no. 2022YFF1002902) and the National Natural Science Foundation of China (grant no. 31972350). We thank C. Hao, X. Zhang at the Chinese Academy of Agricultural Sciences and Y. Jiao at Peking University for sharing the hexaploid wheat varieties. We thank J. Dubcovsky at the University of California, Davis, for constructive suggestions.

MOE Engineering Research Center of Gene Technology, School of Life Sciences, Fudan University, Shanghai, China

Ke-Xin Niu, Chao-Yan Chang, Mei-Qi Zhang, Yue-Ting Guo, Yan Yan, Hao-Jie Sun, Guo-Liang Zhang, Xiao-Ming Li, Yi-Lin Gong, Ci-Hang Ding & Jin-Ying Gou

Key Laboratory of Crop Heterosis and Utilization (MOE), Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing, China

Ke-Xin Niu, Chao-Yan Chang, Mei-Qi Zhang, Yue-Ting Guo, Yan Yan, Xiao-Ming Li, Yi-Lin Gong, Ci-Hang Ding, Meng-Lu Wang, Zhongfu Ni, Qixin Sun & Jin-Ying Gou

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J.-Y.G. designed the research, interpreted the data and wrote the manuscript. K.-X.N. performed most of the experiments with help from C.-Y.C., M.-Q.Z., Y.-T.G., Y.Y., H.-J.S., G.-L.Z., X.-M.L., Y.-L.G., C.-H.D. and M.-L.W. Z.N. and Q.S. contributed to the discussion and analysis of the data.

Correspondence to Jin-Ying Gou.

The authors declare no competing interests.

Nature Plants thanks Lin Li and Thorsten Schnurbusch for their contribution to the peer review of this work.

Publisher's note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Note that we extracted the data from GSE12508 in NCBI.

Source data

a,b, Sequence of the app-B1 gene at the mutation site and its effect on the coding sequence.

a. Comparison of the endogenous PsbO protein levels in the dysfunction mutants. b, c. Grain sizes of WT and psbo-A1 mutant. Bars= 1 cm. d–f. Phenotypic data of grains from WT and psbo-A1 mutants, including grain length (n = 10), grain width (n = 10), grain thickness (n = 20), 1000-grain weight (n = 15), Grain roundness (n = 4), and Tons/HA (n = 3). Data represented mean ± SD; the two-tailed unpaired Student's t-test indicates p-values.

Source data

The specific enzymatic activity of APP1 on a synthetic substrate and PsbO. a. The specific enzymatic activity of APP1 on an artificial substrate. n = 4, Data represented mean ± SD, and the two-tailed unpaired Student's t-test indicates p-values. b. The specific enzymatic activity of APP1 on PsbO.

Source data

a. Venn diagram representation of up-regulated expression genes between the app-A1 backcrossed mutant and WT. b. Venn diagram representation of down-regulated expression genes between the app-A1 backcrossed mutant and WT. c. The APP-A1 expression in app-A1 mutant and WT through RNA-seq. n = 3, Data represented mean ± SD, and the two-tailed unpaired Student's t-test indicates p-values. d. The PsbO-A1 expression in app-A1 mutant and WT through RNA-seq. n = 3, Data represented mean ± SD, and the two-tailed unpaired Student's t-test indicates p-values. GO (e) and KEGG (f) analysis in the app-A1 mutant. n = 3.

Source data

Supplementary Figs. 1 and 2 and Data 1 and 2.

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Niu, KX., Chang, CY., Zhang, MQ. et al. Suppressing ASPARTIC PROTEASE 1 prolongs photosynthesis and increases wheat grain weight. Nat. Plants (2023). https://doi.org/10.1038/s41477-023-01432-x

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Received: 13 September 2022

Accepted: 09 May 2023

Published: 05 June 2023

DOI: https://doi.org/10.1038/s41477-023-01432-x

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Suppressing ASPARTIC PROTEASE 1 prolongs photosynthesis and increases wheat grain weight