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A regulatory network controlling developmental boundaries and meristem fates contributed to maize domestication

Nature Genetics volume 56, pages 2528–2537 (2024)Cite this article

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Abstract

During domestication, early farmers selected different vegetative and reproductive traits, but identifying the causative loci has been hampered by their epistasis and functional redundancy. Using chromatin immunoprecipitation sequencing combined with genome-wide association analysis, we uncovered a developmental regulator that controls both types of trait while acting upstream of multiple domestication loci. tasselsheath4 (tsh4) is a new maize domestication gene that establishes developmental boundaries and specifies meristem fates despite not being expressed within them. TSH4 accomplishes this by using a double-negative feedback loop that targets and represses the very same microRNAs that negatively regulate it. TSH4 functions redundantly with a pair of homologs to positively regulate a suite of domestication loci while specifying the meristem that doubled seed yield in modern maize. TSH4 has a critical role in yield gain and helped generate ideal crop plant architecture, thus explaining why it was a major domestication target.

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Fig. 1: tsh4 affects domestication traits.
Fig. 2: Identifying TSH4 direct targets using ChIP–seq.
Fig. 3: TSH4, UB2 and UB3 control auxin response.
Fig. 4: Double-negative feedback regulation between TSH4 and MIR529.
Fig. 5: TSH4 targets domestication loci.

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Data availability

All RNA-seq and ChIP–seq data generated in this study have been deposited in the National Center for Biotechnology Information Sequence Read Archive (accession code PRJNA517683). The link for the BC2S3 population can be found at http://datacommons.cyverse.org/browse/iplant/home/shared/panzea/genotypes/GBS/v23/teoW22_BC2S3_GBS_phased_genos_imputed_20110423.zip and https://figshare.com/s/0d3aa121f8393c9b4720 (ref. 46). The TeoNAM population link is located at http://datacommons.cyverse.org/browse/iplant/home/shared/panzea/genotypes/GBS/TeosinteNAM and https://doi.org/10.6084/m9.figshare.9820178, respectively. The Zea_mays.AGPv3.30 genome is available at the maize gene database (www.maizegdb.org). All other relevant data supporting the key findings of this study are available within the article, in the Supplementary Information files or are available from the corresponding authors upon reasonable request.

Code availability

No custom code was generated. All code used to analyze the sequence data is publicly available in the SAMtools section of GitHub (https://github.com/samtools/samtools).

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Acknowledgements

This work was supported by the National Key R&D Program of China (2023YFF1000400 to Z.D.) and USDA/NIFA (grant 2020-67013-31614 to G. Chuck). Z.D. was supported by the National Natural Science Foundation of China (32372144), the Pinduoduo-China Agricultural University Research Fund (PC2023B02017) and the Chinese Universities Scientific Fund (2023RC057). C.W. was supported by NSF IOS-1253421. E.S. was supported by NSF IOS (grant no. 2109190 to G. Chuck) and G. Chau was supported by NSF PGRP (grant no. 2211435 to G. Chuck). J.F. was supported by USDA CRIS (grant no. 2030-21000-048-00D). We thank C. Lunde and S. Hake for their helpful comments on the manuscript.

Author information

Authors and Affiliations

  1. State Key Laboratory of Maize Bio-breeding, National Maize Improvement Center, Frontiers Science Center for Molecular Design Breeding, China Agricultural University, Beijing, China

    Zhaobin Dong & Gaoyuan Hu

  2. University of California, Berkeley/Plant Gene Expression Center, Albany, CA, USA

    Zhaobin Dong, Elena A. Shemyakina, Geeyun Chau, Jennifer C. Fletcher & George Chuck

  3. North Carolina State University, Raleigh, NC, USA

    Qiuyue Chen

  4. Brigham Young University, Provo, UT, USA

    Clinton J. Whipple

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Contributions

Z.D. performed ChIP–seq, transcriptome sequencing, microRNA sequencing and diversity analysis and helped design the study. G.H. performed ChIP validation. Q.C. performed an association analysis. E.S. performed RT–qPCR. C.W. performed transcriptome sequencing. G. Chau and J.F. contributed confocal images. G. Chuck designed the study, performed immunolocalization and SEMs and wrote the manuscript with input from all authors.

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Correspondence to Zhaobin Dong or George Chuck.

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Dong, Z., Hu, G., Chen, Q. et al. A regulatory network controlling developmental boundaries and meristem fates contributed to maize domestication. Nat Genet 56, 2528–2537 (2024). https://doi.org/10.1038/s41588-024-01943-z

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