MADS1 maintains barley spike morphology at high ambient temperatures

Gang Li; Hendrik N.J. Kuijer; Xiujuan Yang; Huiran Liu; Chaoqun Shen; Jin Shi; Natalie Betts; Matthew R. Tucker; Wanqi Liang; Robbie Waugh; Rachel A. Burton; Dabing Zhang

doi:10.1038/s41477-021-00957-3

MADS1 maintains barley spike morphology at high ambient temperatures

Gang Li^*, Hendrik N.J. Kuijer, Xiujuan Yang, Huiran Liu, Chaoqun Shen, Jin Shi, Natalie Betts, Matthew R. Tucker, Wanqi Liang, Robbie Waugh, Rachel A. Burton, Dabing Zhang^*

^*Corresponding author for this work

Biological, Environmental Sciences and Engineering

Research output: Contribution to journal › Article › peer-review

41 Scopus citations

Abstract

Temperature stresses affect plant phenotypic diversity. The developmental stability of the inflorescence, required for reproductive success, is tightly regulated by the interplay of genetic and environmental factors. However, the mechanisms underpinning how plant inflorescence architecture responds to temperature are largely unknown. We demonstrate that the barley SEPALLATA MADS-box protein HvMADS1 is responsible for maintaining an unbranched spike architecture at high temperatures, while the loss-of-function mutant forms a branched inflorescence-like structure. HvMADS1 exhibits increased binding to target promoters via A-tract CArG-box motifs, which change conformation with temperature. Target genes for high-temperature-dependent HvMADS1 activation are predominantly associated with inflorescence differentiation and phytohormone signalling. HvMADS1 directly regulates the cytokinin-degrading enzyme HvCKX3 to integrate temperature response and cytokinin homeostasis, which is required to repress meristem cell cycle/division. Our findings reveal a mechanism by which genetic factors direct plant thermomorphogenesis, extending the recognized role of plant MADS-box proteins in floral development.

Original language	English (US)
Pages (from-to)	1093-1107
Number of pages	15
Journal	Nature Plants
Volume	7
Issue number	8
DOIs	https://doi.org/10.1038/s41477-021-00957-3
State	Published - Aug 2021

Bibliographical note

Funding Information:
We thank L. Dreni (Instituto de Biología Molecular y Celular de Plantas, Spain), M. Kater (University of Milan, Italy) and M. Bennett (University of Nottingham, UK) for the discussion on the Australian Research Council Discovery Project (grant no. DP170103352 to D.Z. and R.A.B.) and Y. Liu (South China Agricultural University) for providing vectors pYLsgRNA–OsU6a, pYLsgRNA–OsU6b and pYLCRISPR– Cas9Pubi–H for CRISPR–Cas9 editing. We thank J. Chu (Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China) for help with the CK measurements, G. Mayo (Adelaide Microscopy) for assistance in the microscopy work, D. Peet (University of Adelaide) for guidance with dual-luciferase measurement, A. Chieng and H. Zhou (University of Adelaide) for managing the plant materials, and G. Coupland (Max Planck Institute for Plant Breeding Research, Germany), E. A. Kellogg (Donald Danforth Plant Science Center, USA), D. Smyth (Monash University, Australia), C. Beveridge (University of Queensland, Australia), M. Byrne (University of Sydney, Australia) and S. Boden (University of Adelaide, Australia) for comments on the manuscript. This work was financially supported by the Australian Research Council (grant no. DP170103352 to D.Z. and R.A.B.); an Australia–China Science and Research Fund Joint Research Centre grant (no. ACSRF48187) to D.Z. and G.L.; the Waite Research Institute (WRI) of the University of Adelaide; the National Key Technologies Research and Development Program of China, Ministry of Science and Technology (grant nos. 2016YFD0100804 and 2016YFE0101000 to D.Z.); the National Natural Science Foundation of China (grant nos. 31970803 and 31861163002 to D.Z.) and the Science and Research grant of Southwest University of Science and Technology (no. 19zx7146 to G.L.).

Publisher Copyright:
© 2021, The Author(s), under exclusive licence to Springer Nature Limited.

ASJC Scopus subject areas

Plant Science

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Cite this

@article{e6fea66f40444c19aa3738f3463464f2,

title = "MADS1 maintains barley spike morphology at high ambient temperatures",

abstract = "Temperature stresses affect plant phenotypic diversity. The developmental stability of the inflorescence, required for reproductive success, is tightly regulated by the interplay of genetic and environmental factors. However, the mechanisms underpinning how plant inflorescence architecture responds to temperature are largely unknown. We demonstrate that the barley SEPALLATA MADS-box protein HvMADS1 is responsible for maintaining an unbranched spike architecture at high temperatures, while the loss-of-function mutant forms a branched inflorescence-like structure. HvMADS1 exhibits increased binding to target promoters via A-tract CArG-box motifs, which change conformation with temperature. Target genes for high-temperature-dependent HvMADS1 activation are predominantly associated with inflorescence differentiation and phytohormone signalling. HvMADS1 directly regulates the cytokinin-degrading enzyme HvCKX3 to integrate temperature response and cytokinin homeostasis, which is required to repress meristem cell cycle/division. Our findings reveal a mechanism by which genetic factors direct plant thermomorphogenesis, extending the recognized role of plant MADS-box proteins in floral development.",

author = "Gang Li and Kuijer, {Hendrik N.J.} and Xiujuan Yang and Huiran Liu and Chaoqun Shen and Jin Shi and Natalie Betts and Tucker, {Matthew R.} and Wanqi Liang and Robbie Waugh and Burton, {Rachel A.} and Dabing Zhang",

note = "Funding Information: We thank L. Dreni (Instituto de Biolog{\'i}a Molecular y Celular de Plantas, Spain), M. Kater (University of Milan, Italy) and M. Bennett (University of Nottingham, UK) for the discussion on the Australian Research Council Discovery Project (grant no. DP170103352 to D.Z. and R.A.B.) and Y. Liu (South China Agricultural University) for providing vectors pYLsgRNA–OsU6a, pYLsgRNA–OsU6b and pYLCRISPR– Cas9Pubi–H for CRISPR–Cas9 editing. We thank J. Chu (Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China) for help with the CK measurements, G. Mayo (Adelaide Microscopy) for assistance in the microscopy work, D. Peet (University of Adelaide) for guidance with dual-luciferase measurement, A. Chieng and H. Zhou (University of Adelaide) for managing the plant materials, and G. Coupland (Max Planck Institute for Plant Breeding Research, Germany), E. A. Kellogg (Donald Danforth Plant Science Center, USA), D. Smyth (Monash University, Australia), C. Beveridge (University of Queensland, Australia), M. Byrne (University of Sydney, Australia) and S. Boden (University of Adelaide, Australia) for comments on the manuscript. This work was financially supported by the Australian Research Council (grant no. DP170103352 to D.Z. and R.A.B.); an Australia–China Science and Research Fund Joint Research Centre grant (no. ACSRF48187) to D.Z. and G.L.; the Waite Research Institute (WRI) of the University of Adelaide; the National Key Technologies Research and Development Program of China, Ministry of Science and Technology (grant nos. 2016YFD0100804 and 2016YFE0101000 to D.Z.); the National Natural Science Foundation of China (grant nos. 31970803 and 31861163002 to D.Z.) and the Science and Research grant of Southwest University of Science and Technology (no. 19zx7146 to G.L.). Publisher Copyright: {\textcopyright} 2021, The Author(s), under exclusive licence to Springer Nature Limited.",

year = "2021",

month = aug,

doi = "10.1038/s41477-021-00957-3",

language = "English (US)",

volume = "7",

pages = "1093--1107",

journal = "Nature Plants",

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T1 - MADS1 maintains barley spike morphology at high ambient temperatures

AU - Li, Gang

AU - Kuijer, Hendrik N.J.

AU - Yang, Xiujuan

AU - Liu, Huiran

AU - Shen, Chaoqun

AU - Shi, Jin

AU - Betts, Natalie

AU - Tucker, Matthew R.

AU - Liang, Wanqi

AU - Waugh, Robbie

AU - Burton, Rachel A.

AU - Zhang, Dabing

N1 - Funding Information: We thank L. Dreni (Instituto de Biología Molecular y Celular de Plantas, Spain), M. Kater (University of Milan, Italy) and M. Bennett (University of Nottingham, UK) for the discussion on the Australian Research Council Discovery Project (grant no. DP170103352 to D.Z. and R.A.B.) and Y. Liu (South China Agricultural University) for providing vectors pYLsgRNA–OsU6a, pYLsgRNA–OsU6b and pYLCRISPR– Cas9Pubi–H for CRISPR–Cas9 editing. We thank J. Chu (Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China) for help with the CK measurements, G. Mayo (Adelaide Microscopy) for assistance in the microscopy work, D. Peet (University of Adelaide) for guidance with dual-luciferase measurement, A. Chieng and H. Zhou (University of Adelaide) for managing the plant materials, and G. Coupland (Max Planck Institute for Plant Breeding Research, Germany), E. A. Kellogg (Donald Danforth Plant Science Center, USA), D. Smyth (Monash University, Australia), C. Beveridge (University of Queensland, Australia), M. Byrne (University of Sydney, Australia) and S. Boden (University of Adelaide, Australia) for comments on the manuscript. This work was financially supported by the Australian Research Council (grant no. DP170103352 to D.Z. and R.A.B.); an Australia–China Science and Research Fund Joint Research Centre grant (no. ACSRF48187) to D.Z. and G.L.; the Waite Research Institute (WRI) of the University of Adelaide; the National Key Technologies Research and Development Program of China, Ministry of Science and Technology (grant nos. 2016YFD0100804 and 2016YFE0101000 to D.Z.); the National Natural Science Foundation of China (grant nos. 31970803 and 31861163002 to D.Z.) and the Science and Research grant of Southwest University of Science and Technology (no. 19zx7146 to G.L.). Publisher Copyright: © 2021, The Author(s), under exclusive licence to Springer Nature Limited.

PY - 2021/8

Y1 - 2021/8

N2 - Temperature stresses affect plant phenotypic diversity. The developmental stability of the inflorescence, required for reproductive success, is tightly regulated by the interplay of genetic and environmental factors. However, the mechanisms underpinning how plant inflorescence architecture responds to temperature are largely unknown. We demonstrate that the barley SEPALLATA MADS-box protein HvMADS1 is responsible for maintaining an unbranched spike architecture at high temperatures, while the loss-of-function mutant forms a branched inflorescence-like structure. HvMADS1 exhibits increased binding to target promoters via A-tract CArG-box motifs, which change conformation with temperature. Target genes for high-temperature-dependent HvMADS1 activation are predominantly associated with inflorescence differentiation and phytohormone signalling. HvMADS1 directly regulates the cytokinin-degrading enzyme HvCKX3 to integrate temperature response and cytokinin homeostasis, which is required to repress meristem cell cycle/division. Our findings reveal a mechanism by which genetic factors direct plant thermomorphogenesis, extending the recognized role of plant MADS-box proteins in floral development.

AB - Temperature stresses affect plant phenotypic diversity. The developmental stability of the inflorescence, required for reproductive success, is tightly regulated by the interplay of genetic and environmental factors. However, the mechanisms underpinning how plant inflorescence architecture responds to temperature are largely unknown. We demonstrate that the barley SEPALLATA MADS-box protein HvMADS1 is responsible for maintaining an unbranched spike architecture at high temperatures, while the loss-of-function mutant forms a branched inflorescence-like structure. HvMADS1 exhibits increased binding to target promoters via A-tract CArG-box motifs, which change conformation with temperature. Target genes for high-temperature-dependent HvMADS1 activation are predominantly associated with inflorescence differentiation and phytohormone signalling. HvMADS1 directly regulates the cytokinin-degrading enzyme HvCKX3 to integrate temperature response and cytokinin homeostasis, which is required to repress meristem cell cycle/division. Our findings reveal a mechanism by which genetic factors direct plant thermomorphogenesis, extending the recognized role of plant MADS-box proteins in floral development.

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U2 - 10.1038/s41477-021-00957-3

DO - 10.1038/s41477-021-00957-3

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AN - SCOPUS:85112676330

SN - 2055-026X

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EP - 1107

JO - Nature Plants

JF - Nature Plants

IS - 8

ER -

MADS1 maintains barley spike morphology at high ambient temperatures

Abstract

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