Kelch f-box protein positively influences arabidopsis seed germination by targeting phytochrome-interacting factor1

Manoj Majee; Santosh Kumar; Praveen Kumar Kathare; Shuiqin Wu; Derek Gingerich; Nihar R. Nayak; Louai Salaita; Randy Dinkins; Kathleen Martin; Michael Goodin; Lynnette M.A. Dirk; Taylor D. Lloyd; Ling Zhu; Joseph Chappell; Arthur G. Hunt; Richard Vierstra; Enamul Huq; A. Bruce Downie

doi:10.1073/pnas.1711919115

Kelch f-box protein positively influences arabidopsis seed germination by targeting phytochrome-interacting factor1

Manoj Majee
, Santosh Kumar
, Praveen Kumar Kathare
, Shuiqin Wu
, Derek Gingerich
, Nihar R. Nayak
, Louai Salaita
, Randy Dinkins
, Kathleen Martin
, Michael Goodin
, Lynnette M.A. Dirk
, Taylor D. Lloyd
, Ling Zhu
, Joseph Chappell
, Arthur G. Hunt
, Richard Vierstra
, Enamul Huq
, A. Bruce Downie

Producción científica: Article › revisión exhaustiva

71 Citas (Scopus)

Resumen

Seeds employ sensory systems that assess various environmental cues over time to maximize the successful transition from embryo to seedling. Here we show that the Arabidopsis F-BOX protein COLD TEMPERATURE-GERMINATING (CTG)-10, identified by activation tagging, is a positive regulator of this process. When overex-pressed (OE), CTG10 hastens aspects of seed germination. CTG10 is expressed predominantly in the hypocotyl, and the protein is localized to the nucleus. CTG10 interacts with PHYTOCHROME-INTERACTING FACTOR 1 (PIF1) and helps regulate its abundance in planta. CTG10-OE accelerates the loss of PIF1 in light, increasing germination efficiency, while PIF1-OE lines fail to complete germination in darkness, which is reversed by concurrent CTG10-OE. Double-mutant (pif1 ctg10) lines demonstrated that PIF1 is epi-static to CTG10. Both CTG10 and PIF1 amounts decline during seed germination in the light but reaccumulate in the dark. PIF1 in turn down-regulates CTG10 transcription, suggesting a feedback loop of CTG10/PIF1 control. The genetic, physiological, and biochemical evidence, when taken together, leads us to propose that PIF1 and CTG10 coexist, and even accumulate, in the nucleus in darkness, but that, following illumination, CTG10 assists in reducing PIF1 amounts, thus promoting the completion of seed germination and subsequent seedling development.

Idioma original	English
Páginas (desde-hasta)	E4120-E4129
Publicación	Proceedings of the National Academy of Sciences of the United States of America
Volumen	115
N.º	17
DOI	https://doi.org/10.1073/pnas.1711919115
Estado	Published - abr 24 2018

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Publisher Copyright:
© 2018 National Academy of Sciences. All Rights Reserved.

Financiación

ACKNOWLEDGMENTS. Ms. Amy Crume provided the tobacco plants used for BiFC experiments. Prof. Giltsu Choi (Korea Advanced Institute of Science and Technology) kindly provided the pil5-1 and PIF1-OE lines. A modified pRTL2 vector (double CaMV35S promoter, Tobacco etch virus translational enhancer, NotI sites introduced 5′ and 3′ to the cassette) was the kind gift of Gulvadee Chaiyaprasithi. Prof. Rup K. Kar (Visva-Bharati University) provided useful ideas and encouragement at the inception of this project. Dr. Sharyn Perry (Plant Science Department, University of Kentucky) permitted the use of her growth chamber, and Dr. Tomokazu Kawashima (Plant Science Department, University of Kentucky) allowed the use of his imaging system. Mr. David N. Martin and Mr. Kim Schäfermeyer provided excellent technical assistance in aspects of the project. Funding support included a pilot project and research grant from the Kentucky Tobacco Research and Development Center at the University of Kentucky (to A.B.D.), National Science Foundation Division of Integrative Organismal Systems Collaborative Research Grant 0849230 (to A.B.D. and E.H.), NIH Grant 1R01 GM-114297 (to E.H.), National Science Foundation Supplement 0849230 (to T.D.L. and A.B.D.), an American Society of Plant Biologists Summer Undergraduate Research Fellowship (to T.D.L.), US Department of Agriculture–National Institute of Food and Agriculture Seed Grant 2011-04375 (to A.B.D.), and Kentucky Agricultural Experiment Station Grant KY011038 (to A.B.D. and L.M.A.D.). Ms. Amy Crume provided the tobacco plants used for BiFC experiments. Prof. Giltsu Choi (Korea Advanced Institute of Science and Technology) kindly provided the pil5-1 and PIF1-OE lines. A modified pRTL2 vector (double CaMV35S promoter, Tobacco etch virus translational enhancer, NotI sites introduced 5′ and 3′ to the cassette) was the kind gift of Gulvadee Chaiyaprasithi. Prof. Rup K. Kar (Visva-Bharati University) provided useful ideas and encouragement at the inception of this project. Dr. Sharyn Perry (Plant Science Department, University of Kentucky) permitted the use of her growth chamber, and Dr. Tomokazu Kawashima (Plant Science Department, University of Kentucky) allowed the use of his imaging system. Mr. David N. Martin and Mr. Kim Schäfermeyer provided excellent technical assistance in aspects of the project. Funding support included a pilot project and research grant from the Kentucky Tobacco Research and Development Center at the University of Kentucky (to A.B.D.), National Science Foundation Division of Integrative Organismal Systems Collaborative Research Grant 0849230 (to A.B.D. and E.H.), NIH Grant 1R01 GM-114297 (to E.H.), National Science Foundation Supplement 0849230 (to T.D.L. and A.B.D.), an American Society of Plant Biologists Summer Undergraduate Research Fellowship (to T.D.L.), US Department of Agriculture–National Institute of Food and Agriculture Seed Grant 2011-04375 (to A.B.D.), and Kentucky Agricultural Experiment Station Grant KY011038 (to A.B.D. and L.M.A.D.).

Financiadores	Número del financiador
National Science Foundation Arctic Social Science Program	0849230
National Institutes of Health (NIH)
National Institute of General Medical Sciences DP2GM119177 Sophie Dumont National Institute of General Medical Sciences	R01GM114297
U.S. Department of Agriculture
American Society of Plant Biologists
US Department of Agriculture National Institute of Food and Agriculture, Agriculture and Food Research Initiative	2011-04375
The Kentucky Tobacco Research and Development Center
University of Kentucky
Kentucky Agricultural Experiment Station	KY011038
KAIST

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10.1073/pnas.1711919115

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Majee, M., Kumar, S., Kathare, P. K., Wu, S., Gingerich, D., Nayak, N. R., Salaita, L., Dinkins, R., Martin, K., Goodin, M., Dirk, L. M. A., Lloyd, T. D., Zhu, L., Chappell, J., Hunt, A. G., Vierstra, R., Huq, E., & Bruce Downie, A. (2018). Kelch f-box protein positively influences arabidopsis seed germination by targeting phytochrome-interacting factor1. Proceedings of the National Academy of Sciences of the United States of America, 115(17), E4120-E4129. https://doi.org/10.1073/pnas.1711919115

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title = "Kelch f-box protein positively influences arabidopsis seed germination by targeting phytochrome-interacting factor1",

abstract = "Seeds employ sensory systems that assess various environmental cues over time to maximize the successful transition from embryo to seedling. Here we show that the Arabidopsis F-BOX protein COLD TEMPERATURE-GERMINATING (CTG)-10, identified by activation tagging, is a positive regulator of this process. When overex-pressed (OE), CTG10 hastens aspects of seed germination. CTG10 is expressed predominantly in the hypocotyl, and the protein is localized to the nucleus. CTG10 interacts with PHYTOCHROME-INTERACTING FACTOR 1 (PIF1) and helps regulate its abundance in planta. CTG10-OE accelerates the loss of PIF1 in light, increasing germination efficiency, while PIF1-OE lines fail to complete germination in darkness, which is reversed by concurrent CTG10-OE. Double-mutant (pif1 ctg10) lines demonstrated that PIF1 is epi-static to CTG10. Both CTG10 and PIF1 amounts decline during seed germination in the light but reaccumulate in the dark. PIF1 in turn down-regulates CTG10 transcription, suggesting a feedback loop of CTG10/PIF1 control. The genetic, physiological, and biochemical evidence, when taken together, leads us to propose that PIF1 and CTG10 coexist, and even accumulate, in the nucleus in darkness, but that, following illumination, CTG10 assists in reducing PIF1 amounts, thus promoting the completion of seed germination and subsequent seedling development.",

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author = "Manoj Majee and Santosh Kumar and Kathare, \{Praveen Kumar\} and Shuiqin Wu and Derek Gingerich and Nayak, \{Nihar R.\} and Louai Salaita and Randy Dinkins and Kathleen Martin and Michael Goodin and Dirk, \{Lynnette M.A.\} and Lloyd, \{Taylor D.\} and Ling Zhu and Joseph Chappell and Hunt, \{Arthur G.\} and Richard Vierstra and Enamul Huq and \{Bruce Downie\}, A.",

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Majee, M, Kumar, S, Kathare, PK, Wu, S, Gingerich, D, Nayak, NR, Salaita, L, Dinkins, R, Martin, K, Goodin, M, Dirk, LMA, Lloyd, TD, Zhu, L, Chappell, J , Hunt, AG, Vierstra, R, Huq, E & Bruce Downie, A 2018, 'Kelch f-box protein positively influences arabidopsis seed germination by targeting phytochrome-interacting factor1', Proceedings of the National Academy of Sciences of the United States of America, vol. 115, n.º 17, pp. E4120-E4129. https://doi.org/10.1073/pnas.1711919115

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T1 - Kelch f-box protein positively influences arabidopsis seed germination by targeting phytochrome-interacting factor1

AU - Majee, Manoj

AU - Kumar, Santosh

AU - Kathare, Praveen Kumar

AU - Wu, Shuiqin

AU - Gingerich, Derek

AU - Nayak, Nihar R.

AU - Salaita, Louai

AU - Dinkins, Randy

AU - Martin, Kathleen

AU - Goodin, Michael

AU - Dirk, Lynnette M.A.

AU - Lloyd, Taylor D.

AU - Zhu, Ling

AU - Chappell, Joseph

AU - Hunt, Arthur G.

AU - Vierstra, Richard

AU - Huq, Enamul

AU - Bruce Downie, A.

PY - 2018/4/24

Y1 - 2018/4/24

N2 - Seeds employ sensory systems that assess various environmental cues over time to maximize the successful transition from embryo to seedling. Here we show that the Arabidopsis F-BOX protein COLD TEMPERATURE-GERMINATING (CTG)-10, identified by activation tagging, is a positive regulator of this process. When overex-pressed (OE), CTG10 hastens aspects of seed germination. CTG10 is expressed predominantly in the hypocotyl, and the protein is localized to the nucleus. CTG10 interacts with PHYTOCHROME-INTERACTING FACTOR 1 (PIF1) and helps regulate its abundance in planta. CTG10-OE accelerates the loss of PIF1 in light, increasing germination efficiency, while PIF1-OE lines fail to complete germination in darkness, which is reversed by concurrent CTG10-OE. Double-mutant (pif1 ctg10) lines demonstrated that PIF1 is epi-static to CTG10. Both CTG10 and PIF1 amounts decline during seed germination in the light but reaccumulate in the dark. PIF1 in turn down-regulates CTG10 transcription, suggesting a feedback loop of CTG10/PIF1 control. The genetic, physiological, and biochemical evidence, when taken together, leads us to propose that PIF1 and CTG10 coexist, and even accumulate, in the nucleus in darkness, but that, following illumination, CTG10 assists in reducing PIF1 amounts, thus promoting the completion of seed germination and subsequent seedling development.

AB - Seeds employ sensory systems that assess various environmental cues over time to maximize the successful transition from embryo to seedling. Here we show that the Arabidopsis F-BOX protein COLD TEMPERATURE-GERMINATING (CTG)-10, identified by activation tagging, is a positive regulator of this process. When overex-pressed (OE), CTG10 hastens aspects of seed germination. CTG10 is expressed predominantly in the hypocotyl, and the protein is localized to the nucleus. CTG10 interacts with PHYTOCHROME-INTERACTING FACTOR 1 (PIF1) and helps regulate its abundance in planta. CTG10-OE accelerates the loss of PIF1 in light, increasing germination efficiency, while PIF1-OE lines fail to complete germination in darkness, which is reversed by concurrent CTG10-OE. Double-mutant (pif1 ctg10) lines demonstrated that PIF1 is epi-static to CTG10. Both CTG10 and PIF1 amounts decline during seed germination in the light but reaccumulate in the dark. PIF1 in turn down-regulates CTG10 transcription, suggesting a feedback loop of CTG10/PIF1 control. The genetic, physiological, and biochemical evidence, when taken together, leads us to propose that PIF1 and CTG10 coexist, and even accumulate, in the nucleus in darkness, but that, following illumination, CTG10 assists in reducing PIF1 amounts, thus promoting the completion of seed germination and subsequent seedling development.

KW - Germination

KW - Light

KW - Seed

KW - Ubiquitination

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JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 17

ER -

Kelch f-box protein positively influences arabidopsis seed germination by targeting phytochrome-interacting factor1

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