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Multiple origins of Indian dwarf wheat by mutations targeting the TREE domain of a GSK3-like kinase for drought tolerance, phosphate uptake, and grain quality

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Abstract

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Multiple origins of Indian dwarf wheat were due to two mutations targeting the same TREE domain of a GSK3-like kinase, and these mutations confer to enhanced drought tolerance and increased phosphate and nitrogen accumulation for adaptation to the dry climate of Indian and Pakistan.

Abstract

Indian dwarf wheat, featured by the short stature, erect leaves, dense spikes, and small, spherical grains, was a staple crop in India and Pakistan from the Bronze Age until the early 1900s. These morphological features are controlled by a single locus Sphaerococcum 1 (S1), but the genetic identity of the locus and molecular mechanisms underlying the selection of this wheat type are unknown. In this study, we showed that the origin of Indian dwarf wheat was due to two independent missense mutations targeting the conserved TREE domain of a GSK3-like kinase, which is homologous to the Arabidopsis BIN2 protein, a negative regulator in brassinosteroid signaling. The S1 protein is involved in brassinosteroid signaling by physical interaction with the wheat BES1/BZR1 proteins. The dwarf alleles are insensitive to brassinosteroid, upregulates brassinosteroid biosynthetic genes, significantly enhanced drought tolerance, facilitated phosphate accumulation, and increased high molecular weight glutenins. It is the enhanced drought tolerance and accumulation of nitrogen and phosphate that contributed to the adaptation of such a small-grain form of wheat to the dry climate of India and Pakistan. Thus, our research not only identified the genetic events underlying the origin of the Indian dwarf wheat, but also revealed the function of brassinosteroid in the regulation of drought tolerance, phosphate homeostasis, and grain quality.

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Acknowledgements

We thank Dr. Harold Bockelman (USDA ARS, Aberdeen, ID), Dr. Bikram Gill (Kansas State University, Manhattan, KS), Dr. Helmut Knüpffer (The Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), German), Dr. Shuhei Nasuda (Kyoto University, Japan), and Dr. N. Wanatabe (Gifu University, Japan) for providing seeds. We are grateful to Jan Vrána, Zdeňka Dubská, Romana Šperková, and Jitka Weiserová for the technical assistance with chromosome sorting and DNA amplification. This research is supported by the USDA Hatch program through the South Dakota Agricultural Experiment Station and USDA NIFA-IWYP (award number: 2017-67008-25934). IM was supported by the Marie Curie Fellowship grant award “AEGILWHEAT” (H2020-MSCA-IF-2016-746253) and the Hungarian National Research, Development, and Innovation Office (K116277). JD was supported by the ERDF project “Plants as a tool for sustainable global development” (No. CZ.02.1.01/0.0/0.0/16_019/0000827).

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  1. Ajay Gupta and Lei Hua these author contributed equally to this research.

Authors and Affiliations

  1. 252 McFadden Biostress Laboratory, Department of Biology and Microbiology, South Dakota State University, Brookings, SD, 57007, USA

    Ajay Gupta, Lei Hua & Wanlong Li

  2. Plant Pathology Department, Kansas State University, Manhattan, KS, 66502, USA

    Guifang Lin & Sanzhen Liu

  3. Institute of Experimental Botany of the Czech Academy of Sciences, 77900, Olomouc, Czech Republic

    Istváan Molnár & Jaroslav Doležel

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WL conceived the project, all authors conducted experiments and analyzed results, WL drafted the manuscript, and all authors edited and approved it.

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Gupta, A., Hua, L., Lin, G. et al. Multiple origins of Indian dwarf wheat by mutations targeting the TREE domain of a GSK3-like kinase for drought tolerance, phosphate uptake, and grain quality. Theor Appl Genet 134, 633–645 (2021). https://doi.org/10.1007/s00122-020-03719-5

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