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Improving bread wheat yield through modulating an unselected AP2/ERF gene

Nature Plants volume 8, pages 930–939 (2022)Cite this article

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An Author Correction to this article was published on 17 January 2023

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Abstract

Crop breeding heavily relies on natural genetic variation. However, additional new variations are desired to meet the increasing human demand. Inflorescence architecture determines grain number per spike, a major determinant of bread wheat (Triticum aestivum L.) yield. Here, using Brachypodium distachyon as a wheat proxy, we identified DUO-B1, encoding an APETALA2/ethylene response factor (AP2/ERF) transcription factor, regulating spike inflorescence architecture in bread wheat. Mutations of DUO-B1 lead to mild supernumerary spikelets, increased grain number per spike and, importantly, increased yield under field conditions without affecting other major agronomic traits. DUO-B1 suppresses cell division and promotes the expression of BHt/WFZP, whose mutations could lead to branched ‘miracle-wheat’. Pan-genome analysis indicated that DUO-B1 has not been utilized in breeding, and holds promise to increase wheat yield further.

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Fig. 1: Characterization of BdDUO1 in B. distachyon.
Fig. 2: Expression of DUO1 in wheat.
Fig. 3: Spike architecture of bread wheat cv. Fielder and duo-B1 mutants.
Fig. 4: Yield of duo-B1 mutant lines in the field grown in Zhaoxian in 2019/20 at a sowing density of 180 grains m−2 and selection sweeps around the DUO-B1 locus.
Fig. 5: DUO-B1 inhibits cell division and meristematic gene expression.
Fig. 6: WFZP mediates the function of DUO-B1 in spike development.

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Data availability

The raw sequencing data for the RNA-seq analysis in this paper have been deposited in the Genome Sequence Archive database at the National Genomics Data Center (https://ngdc.cncb.ac.cn/) (accession nos. CRA009320-009325 and CRA009431-009433). Source data are provided with this paper.

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Acknowledgements

This work was supported by National Natural Science Foundation of China (grant no. 31921005) and Strategic Priority Research Programme of the Chinese Academy of Sciences (grant no. XDA24020203) to Y.J. We thank Y. Tian for assistance with scanning electron microscopy.

Author information

Author notes

  1. These authors contributed equally: Yuange Wang, Fei Du.

Authors and Affiliations

  1. State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, China

    Yuange Wang, Fei Du, Jian Wang, Caihuan Tian & Yuling Jiao

  2. National Key Facility of Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China

    Ke Wang & Xingguo Ye

  3. Key Laboratory of Plant Molecular Physiology, Institute of Botany, The Innovation Academy of Seed Design, Chinese Academy of Sciences, Beijing, China

    Xiaoquan Qi

  4. College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, China

    Xiaoquan Qi, Fei Lu & Yuling Jiao

  5. State Key Laboratory of Plant Cell and Chromosome Engineering, CAS-JIC Centre of Excellence for Plant and Microbial Science (CEPAMS), Institute of Genetics and Developmental Biology, The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, China

    Fei Lu

  6. Ministry of Education Key Laboratory of Molecular and Cellular Biology, Hebei Collaboration Innovation Center for Cell Signaling, Hebei Key Laboratory of Molecular and Cellular Biology, College of Life Sciences, Hebei Normal University, Shijiazhuang, China

    Xigang Liu

  7. State Key Laboratory of Protein and Plant Gene Research, Peking-Tsinghua Center for Life Sciences, Center for Quantitative Biology, School of Life Sciences, Peking University, Beijing, China

    Yuling Jiao

  8. Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences at Weifang, Weifang, China

    Yuling Jiao

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Contributions

Y.W. and F.D. performed experiments, analysed the data and wrote the manuscript. J.W., K.W., X.L. and X.Y. performed the genetic transformation. C.T. performed experiments in Arabidopsis. F.L. conducted population genetic analysis. X.Q. provided key resources. Y.J. designed research, wrote the manuscript and supervised the project.

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Correspondence to Yuling Jiao.

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Nature Plants thanks Mohammad Pourkheirandish, Thorsten Schnurbusch and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 The phenotypes of bdduo1-1 are caused by reduced expression of Bradi2g21067.

a and b, Electron scanning microscopy images of young spikes of B. distachyon Bd21 in a and T-DNA insertion mutant bdduo1-1 in b. The experiments were repeated more than three times, with similar results. c, Comparison of spikelet number per spike between Bd21 and bdduo1-1. *** indicates P < 0.001 with significant differences compared with Bd21. Data are shown as mean ± s.d.; dots show data distribution (n = 11 biologically independent samples, P values calculated using two-tailed t-test). d, Schematic diagram of the T-DNA insertion site in bdduo1-1. e, The relative expression levels of Bradi2g21067 and Bradi2g21080 in Bd21 and bdduo1-1. The data are shown as mean ± s.d.; n = 3 biological replicates. f, CRISPR/Cas9-mediated mutations in the BdDUO1 gene. The position and sequence of target site for CRISPR/Cas9 gene editing are indicated. The symbols ‘-’ show the nucleotide deletion with the base numbers of deletion shown behind. nt, nucleotide; SM, spikelet meristem; GP, glume meristem; LP, lemma meristem; TSM, terminal spikelet meristem.

Source data

Extended Data Fig. 2 Analysis of axillary branches in Bd21 and bdduo1-1.

Schematic representation and examination of axillary branches in leaf axils in Bd21 (a) and bdduo1-1 (b) plants (n = 6). Left, schematic illustration of branches in the wild type and duo1-1. Right, analysis of branches in each leaf axil of Bd21 and bdduo1-1 plants. Each column stands for the growing order of branch, while each row represents the position of the axils. P, S, T and Q with different colors indicate primary branch, secondary branch, tertiary branch and quaternary branch, respectively. The number in the green grids represents the number of branches.

Extended Data Fig. 3 Analysis of branches in each leaf axil of Bd21 (a), bdduo1_m1 (b) and bdduo1_m2 (c) plants (n = 6).

Each column stands for the growing order of branch, while each row represents the position of the axils. P, S, T and Q with different colors indicate primary branch, secondary branch, tertiary branch and quaternary branch, respectively. The number in the green grids represents the number of branches.

Extended Data Fig. 4 Phenotypic analyses of two independent complementation lines of bdduo1, gBdDUO1/bdduo1-1#1 and gBdDUO1/bdduo1-1#2.

a, Comparisons of the flowering stage, maturity stage, spike number per spike, floret number per spike, grain number per spike and grain number per plant. ns indicates P > 0.05 with no significant differences compared with Bd21. Data are shown as mean ± s.d.; dots show data distribution (n = 40 biologically independent samples, P values calculated using two-tailed t-test). b-d, Analysis of branches in each leaf axil of Bd21 (b) gBdDUO1/bdduo1-1#1 (c) and gBdDUO1/bdduo1-1#2 (d) plants (n = 6). Each column stands for the growing order of branch, while each row represents the position of the axils. P, S, T and Q indicate primary branch, secondary branch, tertiary branch and quaternary branch, respectively. The number in the green grids represents the number of branches.

Source data

Extended Data Fig. 5 Phylogenetic analyses of DUO1 homologs in eudicots and monocots.

The Neighbor joining tree is generated by using MEGA6, and the numbers at each node shows bootstrap values obtained for 1,000 replicates. Arabidopsis thaliana (AT1G28360), Brachypodium distachyon (Bradi2g21067), Aegilops tauschii (AET3Gv20746700), Oryza sativa (LOC_Os05g41760), Zea mays (Zm00001e027350), Hordeum vulgare (HORVU1Hr1G067160), Triticum turgidum (TRITD1Bv1G217090), Triticum urartu (TuG1812G0100003530.01), Glycine max (GLYMA_13G236600), Setaria viridis (SEVIR_5G352900v2) and Triticum aestivum (TraesCS1A02G314200, TraesCS1B02G326500 and TraesCS1D02G314700) are included.

Extended Data Fig. 6 Phenotypic analyses of duo1 mutants in the field in Zhaoxian, Hebei Province, China in 2019/20 at the sowing density of 180 grains/m2.

a, CRISPR/Cas9-based mutations in the DUO-B1 gene. The positions and sequences of target sites for CRISPR/Cas9 gene editing are shown. The symbols ‘-’ indicated the nucleotide deletion with the base numbers of deletion shown behind. nt, nucleotide. b, Comparisons of the grain width and grain length between Fielder and two independent mutant lines, duo-B1_m1 and duo-B1_m2. Bars, 1 cm. c to e, Comparisons of the spike fertility index c, harvest index d, 1000-grain weight e, between Fielder and two independent mutant lines, duo-B1_m1 and duo-B1_m2. Data are shown as mean ± s.d.; dots show data distribution (n = 20 biologically independent samples, P values calculated using two-tailed t-test).

Source data

Extended Data Fig. 7 Spike architecture analysis between WT and duo-B1 mutants.

a, Analysis of days until double ridge between WT and mutants. ns, no significant difference. b, Analysis of days until terminal spikelet stage between WT and mutants. c, Distribution of MRS along the wheat spike of mutants. Data are shown as mean ± s.d.; dots show data distribution (n = at least 15 biologically independent samples, P values calculated using two-tailed t-test).

Source data

Extended Data Fig. 8 Arabidopsis ERF12 affects axillary meristem formation in cauline leaves.

a, CRISPR/Cas9-mediated mutations in the ERF12 gene. The position and sequence of target site for CRISPR/Cas9 gene editing were indicated. The symbols ‘+’ showed the nucleotide insertion, and the base numbers of insertion were shown behind. nt, nucleotide. b, Close-up view of leaf axils in Arabidopsis Col-0 and erf12 mutants showing the presence (white arrow) and absence (red arrow) of an accessory bud, respectively. Scale bars, 5 mm. c, Schematic representation of accessory bud formation in leaf axils of Col-0 and three independent erf12 lines. Green indicates the lack of an accessory bud from an axillary branch, and red shows the presence of an accessory bud.

Extended Data Fig. 9 Phenotypic analyses of duo-B1 mutants in the greenhouse.

Comparisons of the spike number per spike (a), floret number per spike (b), grain number per spike (c), 1000-grain weight (d), grain weight per plant (e), spike fertility index (f) and grain yield per square meter (g) between Fielder and two independent mutant lines, duo-B1-1 and duo-B1-2. Data are shown as mean ± s.d.; dots show data distribution (n = 20 biologically independent samples, P values calculated using two-tailed t-test).

Source data

Extended Data Fig. 10 Phenotypic analyses of two independent complementation lines of duo-B1, gDUO-B1/duo-B1_m1#1 and gDUO-B1/duo-B1_m1#2.

Comparisons of the spike number per spike (a), floret number per spike (b), grain number per spike (c) and 1000-grain weight (d). ns indicates P > 0.05 with no significant differences compared with Fielder. Data are shown as mean ± s.d.; dots show data distribution (n = 20 biologically independent samples, P values calculated using two-tailed t-test).

Source data

Supplementary information

Supplementary Information

Supplementary Figs. 1–9, Tables 1–3 and Data 1.

Reporting Summary

Supplementary Data 1

DEGs (differential expressed genes) between Fielder and duo1-B1 mutants at young spike stage.

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Wang, Y., Du, F., Wang, J. et al. Improving bread wheat yield through modulating an unselected AP2/ERF gene. Nat. Plants 8, 930–939 (2022). https://doi.org/10.1038/s41477-022-01197-9

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