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The role of HEXOKINASE1 in Arabidopsis leaf growth

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Here, we used a hxk1 mutant in the Col-0 background. We demonstrated that HXK1 regulates cell proliferation and expansion early during leaf development, and that HXK1 is involved in sucrose-induced leaf growth stimulation independent of GPT2. Furthermore, we identified KINγ as a novel HXK1-interacting protein.

Abstract

In the last decade, extensive efforts have been made to unravel the underlying mechanisms of plant growth control through sugar availability. Signaling by the conserved glucose sensor HEXOKINASE1 (HXK1) has been shown to exert both growth-promoting and growth-inhibitory effects depending on the sugar levels, the environmental conditions and the plant species. Here, we used a hxk1 mutant in the Col-0 background to investigate the role of HXK1 during leaf growth in more detail and show that it is affected in both cell proliferation and cell expansion early during leaf development. Furthermore, the hxk1 mutant is less sensitive to sucrose-induced cell proliferation with no significant increase in final leaf growth after transfer to sucrose. Early during leaf development, transfer to sucrose stimulates expression of GLUCOSE-6-PHOSPHATE/PHOSPHATE TRANSPORTER2 (GPT2) and represses chloroplast differentiation. However, in the hxk1 mutant GPT2 expression was still upregulated by transfer to sucrose although chloroplast differentiation was not affected, suggesting that GPT2 is not involved in HXK1-dependent regulation of leaf growth. Finally, using tandem affinity purification of protein complexes from cell cultures, we identified KINγ, a protein containing four cystathionine β-synthase domains, as an interacting protein of HXK1.

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Acknowledgements

We thank all colleagues of the Systems Biology of Yield research group for many fruitful discussions. Special thanks to Riet De Rycke and Michiel De Bruyne for performing the TEM experiments, Véronique Storme for her help with the statistical analysis, Wim Dejonghe for confocal imaging assistance and Annick Bleys for her help in preparing the manuscript. This work was supported by Ghent University (‘Bijzonder Onderzoeksfonds Methusalem Project’ no. BOF08/01M00408) and the Research Foundation-Flanders (FWO project G046512N “Controle van de bladgroei door suiker-en energiesignalering”).

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Authors and Affiliations

  1. Center for Plant Systems Biology, VIB-Ghent University, Technologiepark 927, 9052, Gent, Belgium

    Judith Van Dingenen, Mattias Vermeersch, Liesbeth De Milde, Nancy De Winne, Jelle Van Leene, Nathalie Gonzalez, Stijn Dhondt, Geert De Jaeger & Dirk Inzé

  2. Department of Plant Biotechnology and Bioinformatics, Ghent University, Gent, Belgium

    Judith Van Dingenen, Mattias Vermeersch, Liesbeth De Milde, Nancy De Winne, Jelle Van Leene, Nathalie Gonzalez, Stijn Dhondt, Geert De Jaeger & Dirk Inzé

  3. Laboratory of Molecular Plant Biology, KU Leuven Department of Biology, Kasteelpark Arenberg 31, 3001, Leuven, Belgium

    Sander Hulsmans & Filip Rolland

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  1. Judith Van Dingenen
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  2. Mattias Vermeersch
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  3. Liesbeth De Milde
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  4. Sander Hulsmans
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  7. Nathalie Gonzalez
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  9. Geert De Jaeger
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  10. Filip Rolland
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  11. Dirk Inzé
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Contributions

JVD performed experiments, analyzed data and is the main author; MV and LDM assisted experiments; SH performed the BiFC experiments; JVL, NDW and GDJ performed the TAP experiments; FR, NG, SD and JVL were involved in discussions throughout the project; NG, SD, FR and DI contributed to the writing of the manuscript. GDJ and DI supervised the project.

Corresponding author

Correspondence to Dirk Inzé.

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Van Dingenen, J., Vermeersch, M., De Milde, L. et al. The role of HEXOKINASE1 in Arabidopsis leaf growth. Plant Mol Biol 99, 79–93 (2019). https://doi.org/10.1007/s11103-018-0803-0

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