Agave REVEILLE1 regulates the onset and release of seasonal dormancy in Populus

Degao Liu; Dan Tang; Meng Xie; Jin Zhang; Longmei Zhai; Jiangping Mao; Chao Luo; Anna Lipzen; Yu Zhang; Emily Savage; Guoliang Yuan; Hao Bo Guo; Dimiru Tadesse; Rongbin Hu; Sara Jawdy; Hua Cheng; Linling Li; Huseyin Yer; Miranda M. Clark; Huayu Sun; Jiyuan Shi; Roshani Budhathoki; Rahul Kumar; Troy Kamuda; Yanjun Li; Christa Pennacchio; Kerrie Barry; Jeremy Schmutz; Rajiv Berry; Wellington Muchero; Jin Gui Chen; Yi Li; Gerald A. Tuskan; Xiaohan Yang

doi:10.1093/plphys/kiac588

Agave REVEILLE1 regulates the onset and release of seasonal dormancy in Populus

Degao Liu, Dan Tang, Meng Xie, Jin Zhang, Longmei Zhai, Jiangping Mao, Chao Luo, Anna Lipzen, Yu Zhang, Emily Savage, Guoliang Yuan, Hao Bo Guo, Dimiru Tadesse, Rongbin Hu, Sara Jawdy, Hua Cheng, Linling Li, Huseyin Yer, Miranda M. Clark, Huayu SunJiyuan Shi, Roshani Budhathoki, Rahul Kumar, Troy Kamuda, Yanjun Li, Christa Pennacchio, Kerrie Barry, Jeremy Schmutz, Rajiv Berry, Wellington Muchero, Jin Gui Chen, Yi Li, Gerald A. Tuskan, Xiaohan Yang

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

6 Scopus citations

Abstract

Deciduous woody plants like poplar (Populus spp.) have seasonal bud dormancy. It has been challenging to simultaneously delay the onset of bud dormancy in the fall and advance bud break in the spring, as bud dormancy, and bud break were thought to be controlled by different genetic factors. Here, we demonstrate that heterologous expression of the REVEILLE1 gene (named AaRVE1) from Agave (Agave americana) not only delays the onset of bud dormancy but also accelerates bud break in poplar in field trials. AaRVE1 heterologous expression increases poplar biomass yield by 166% in the greenhouse. Furthermore, we reveal that heterologous expression of AaRVE1 increases cytokinin contents, represses multiple dormancy-related genes, and up-regulates bud break-related genes, and that AaRVE1 functions as a transcriptional repressor and regulates the activity of the DORMANCY-ASSOCIATED PROTEIN 1 (DRM1) promoter. Our findings demonstrate that AaRVE1 appears to function as a regulator of bud dormancy and bud break, which has important implications for extending the growing season of deciduous trees in frost-free temperate and subtropical regions to increase crop yield.

Original language	English
Pages (from-to)	1492-1504
Number of pages	13
Journal	Plant Physiology
Volume	191
Issue number	3
DOIs	https://doi.org/10.1093/plphys/kiac588
State	Published - Mar 2023

Funding

This research is supported by the Department of Energy (DOE), Office of Science, Genomic Science Program under Award Number DE-SC0008834, and the Center for Bioenergy Innovation (CBI), which is a U.S. Department of Energy Bioenergy Research Center supported by the Office of Biological and Environmental Research in the DOE Office of Science. Oak Ridge National Laboratory is managed by UT-Battelle, LLC for the US DOE under Contract Number DE-AC05-00OR22725. Meng Xie and Dimiru Tadesse are supported by the U.S. DOE, Office of Science, Office of Biological and Environmental Research, as part of the Quantitative Plant Science Initiative (QPSI) at Brookhaven National Laboratory. The work (proposal: 10.46936/10.25585/ 60000780) conducted by the U.S. Department of Energy Joint Genome Institute (https://ror.org/04xm1d337), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. DOE operated under Contract No. DE-AC02-05CH11231.

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Liu, D., Tang, D., Xie, M., Zhang, J., Zhai, L., Mao, J., Luo, C., Lipzen, A., Zhang, Y., Savage, E., Yuan, G., Guo, H. B., Tadesse, D., Hu, R., Jawdy, S., Cheng, H., Li, L., Yer, H., Clark, M. M., ... Yang, X. (2023). Agave REVEILLE1 regulates the onset and release of seasonal dormancy in Populus. Plant Physiology, 191(3), 1492-1504. https://doi.org/10.1093/plphys/kiac588

@article{496be07533214d52a4b8b04aa0a7f36f,

title = "Agave REVEILLE1 regulates the onset and release of seasonal dormancy in Populus",

abstract = "Deciduous woody plants like poplar (Populus spp.) have seasonal bud dormancy. It has been challenging to simultaneously delay the onset of bud dormancy in the fall and advance bud break in the spring, as bud dormancy, and bud break were thought to be controlled by different genetic factors. Here, we demonstrate that heterologous expression of the REVEILLE1 gene (named AaRVE1) from Agave (Agave americana) not only delays the onset of bud dormancy but also accelerates bud break in poplar in field trials. AaRVE1 heterologous expression increases poplar biomass yield by 166% in the greenhouse. Furthermore, we reveal that heterologous expression of AaRVE1 increases cytokinin contents, represses multiple dormancy-related genes, and up-regulates bud break-related genes, and that AaRVE1 functions as a transcriptional repressor and regulates the activity of the DORMANCY-ASSOCIATED PROTEIN 1 (DRM1) promoter. Our findings demonstrate that AaRVE1 appears to function as a regulator of bud dormancy and bud break, which has important implications for extending the growing season of deciduous trees in frost-free temperate and subtropical regions to increase crop yield.",

author = "Degao Liu and Dan Tang and Meng Xie and Jin Zhang and Longmei Zhai and Jiangping Mao and Chao Luo and Anna Lipzen and Yu Zhang and Emily Savage and Guoliang Yuan and Guo, {Hao Bo} and Dimiru Tadesse and Rongbin Hu and Sara Jawdy and Hua Cheng and Linling Li and Huseyin Yer and Clark, {Miranda M.} and Huayu Sun and Jiyuan Shi and Roshani Budhathoki and Rahul Kumar and Troy Kamuda and Yanjun Li and Christa Pennacchio and Kerrie Barry and Jeremy Schmutz and Rajiv Berry and Wellington Muchero and Chen, {Jin Gui} and Yi Li and Tuskan, {Gerald A.} and Xiaohan Yang",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2022.",

year = "2023",

month = mar,

doi = "10.1093/plphys/kiac588",

language = "English",

volume = "191",

pages = "1492--1504",

journal = "Plant Physiology",

issn = "0032-0889",

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Liu, D, Tang, D, Xie, M, Zhang, J, Zhai, L, Mao, J, Luo, C, Lipzen, A, Zhang, Y, Savage, E, Yuan, G, Guo, HB, Tadesse, D, Hu, R, Jawdy, S, Cheng, H, Li, L, Yer, H, Clark, MM, Sun, H, Shi, J, Budhathoki, R, Kumar, R, Kamuda, T, Li, Y, Pennacchio, C, Barry, K, Schmutz, J, Berry, R, Muchero, W, Chen, JG, Li, Y, Tuskan, GA & Yang, X 2023, 'Agave REVEILLE1 regulates the onset and release of seasonal dormancy in Populus', Plant Physiology, vol. 191, no. 3, pp. 1492-1504. https://doi.org/10.1093/plphys/kiac588

TY - JOUR

T1 - Agave REVEILLE1 regulates the onset and release of seasonal dormancy in Populus

AU - Liu, Degao

AU - Tang, Dan

AU - Xie, Meng

AU - Zhang, Jin

AU - Zhai, Longmei

AU - Mao, Jiangping

AU - Luo, Chao

AU - Lipzen, Anna

AU - Zhang, Yu

AU - Savage, Emily

AU - Yuan, Guoliang

AU - Guo, Hao Bo

AU - Tadesse, Dimiru

AU - Hu, Rongbin

AU - Jawdy, Sara

AU - Cheng, Hua

AU - Li, Linling

AU - Yer, Huseyin

AU - Clark, Miranda M.

AU - Sun, Huayu

AU - Shi, Jiyuan

AU - Budhathoki, Roshani

AU - Kumar, Rahul

AU - Kamuda, Troy

AU - Li, Yanjun

AU - Pennacchio, Christa

AU - Barry, Kerrie

AU - Schmutz, Jeremy

AU - Berry, Rajiv

AU - Muchero, Wellington

AU - Chen, Jin Gui

AU - Li, Yi

AU - Tuskan, Gerald A.

AU - Yang, Xiaohan

PY - 2023/3

Y1 - 2023/3

N2 - Deciduous woody plants like poplar (Populus spp.) have seasonal bud dormancy. It has been challenging to simultaneously delay the onset of bud dormancy in the fall and advance bud break in the spring, as bud dormancy, and bud break were thought to be controlled by different genetic factors. Here, we demonstrate that heterologous expression of the REVEILLE1 gene (named AaRVE1) from Agave (Agave americana) not only delays the onset of bud dormancy but also accelerates bud break in poplar in field trials. AaRVE1 heterologous expression increases poplar biomass yield by 166% in the greenhouse. Furthermore, we reveal that heterologous expression of AaRVE1 increases cytokinin contents, represses multiple dormancy-related genes, and up-regulates bud break-related genes, and that AaRVE1 functions as a transcriptional repressor and regulates the activity of the DORMANCY-ASSOCIATED PROTEIN 1 (DRM1) promoter. Our findings demonstrate that AaRVE1 appears to function as a regulator of bud dormancy and bud break, which has important implications for extending the growing season of deciduous trees in frost-free temperate and subtropical regions to increase crop yield.

AB - Deciduous woody plants like poplar (Populus spp.) have seasonal bud dormancy. It has been challenging to simultaneously delay the onset of bud dormancy in the fall and advance bud break in the spring, as bud dormancy, and bud break were thought to be controlled by different genetic factors. Here, we demonstrate that heterologous expression of the REVEILLE1 gene (named AaRVE1) from Agave (Agave americana) not only delays the onset of bud dormancy but also accelerates bud break in poplar in field trials. AaRVE1 heterologous expression increases poplar biomass yield by 166% in the greenhouse. Furthermore, we reveal that heterologous expression of AaRVE1 increases cytokinin contents, represses multiple dormancy-related genes, and up-regulates bud break-related genes, and that AaRVE1 functions as a transcriptional repressor and regulates the activity of the DORMANCY-ASSOCIATED PROTEIN 1 (DRM1) promoter. Our findings demonstrate that AaRVE1 appears to function as a regulator of bud dormancy and bud break, which has important implications for extending the growing season of deciduous trees in frost-free temperate and subtropical regions to increase crop yield.

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U2 - 10.1093/plphys/kiac588

DO - 10.1093/plphys/kiac588

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AN - SCOPUS:85150234751

SN - 0032-0889

VL - 191

SP - 1492

EP - 1504

JO - Plant Physiology

JF - Plant Physiology

IS - 3

ER -

Agave REVEILLE1 regulates the onset and release of seasonal dormancy in Populus

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