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Touch-triggered bZIP translocation regulates elongation and secondary wall biosynthesis

View ORCID ProfileJoshua H. Coomey, Kirk J.-M. MacKinnon, View ORCID ProfilePubudu P. Handakumbura, Ian W. McCahill, Gina M. Trabucco, Jessica Mazzola, View ORCID ProfileNicole A. Leblanc, Rithany Kheam, Miriam Hernandez-Romero, View ORCID ProfileKerrie Barry, Lifeng Liu, Ji E. Lee, View ORCID ProfileJohn P. Vogel, Ronan C. O’Malley, View ORCID ProfileJames J. Chambers, View ORCID ProfileSamuel P. Hazen
doi: https://doi.org/10.1101/2021.02.03.429573
Joshua H. Coomey
1Biology Department, University of Massachusetts, Amherst, MA 01003, USA
2Plant Biology Graduate Program, University of Massachusetts, Amherst, MA 01003, USA
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  • ORCID record for Joshua H. Coomey
Kirk J.-M. MacKinnon
1Biology Department, University of Massachusetts, Amherst, MA 01003, USA
3Molecular and Cellular Biology Graduate Program, University of Massachusetts, Amherst, MA 01003, USA
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Pubudu P. Handakumbura
1Biology Department, University of Massachusetts, Amherst, MA 01003, USA
2Plant Biology Graduate Program, University of Massachusetts, Amherst, MA 01003, USA
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Ian W. McCahill
1Biology Department, University of Massachusetts, Amherst, MA 01003, USA
2Plant Biology Graduate Program, University of Massachusetts, Amherst, MA 01003, USA
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Gina M. Trabucco
1Biology Department, University of Massachusetts, Amherst, MA 01003, USA
3Molecular and Cellular Biology Graduate Program, University of Massachusetts, Amherst, MA 01003, USA
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Jessica Mazzola
1Biology Department, University of Massachusetts, Amherst, MA 01003, USA
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Nicole A. Leblanc
1Biology Department, University of Massachusetts, Amherst, MA 01003, USA
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  • ORCID record for Nicole A. Leblanc
Rithany Kheam
1Biology Department, University of Massachusetts, Amherst, MA 01003, USA
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Miriam Hernandez-Romero
1Biology Department, University of Massachusetts, Amherst, MA 01003, USA
2Plant Biology Graduate Program, University of Massachusetts, Amherst, MA 01003, USA
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Kerrie Barry
4DOE Joint Genome Institute, Berkeley, CA 94720, USA
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  • ORCID record for Kerrie Barry
Lifeng Liu
4DOE Joint Genome Institute, Berkeley, CA 94720, USA
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Ji E. Lee
4DOE Joint Genome Institute, Berkeley, CA 94720, USA
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John P. Vogel
4DOE Joint Genome Institute, Berkeley, CA 94720, USA
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Ronan C. O’Malley
4DOE Joint Genome Institute, Berkeley, CA 94720, USA
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James J. Chambers
5Institute for Applied Life Science, University of Massachusetts, Amherst, MA 01003, USA
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  • ORCID record for James J. Chambers
Samuel P. Hazen
1Biology Department, University of Massachusetts, Amherst, MA 01003, USA
2Plant Biology Graduate Program, University of Massachusetts, Amherst, MA 01003, USA
3Molecular and Cellular Biology Graduate Program, University of Massachusetts, Amherst, MA 01003, USA
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  • For correspondence: hazen@bio.umass.edu
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ABSTRACT

Plant growth is mediated by the integration of internal and external cues, perceived by cells and transduced into a developmental program that gives rise to cell division, elongation, and wall thickening. Extra-, inter-, and intra-physical cellular forces contribute to this regulation. Across the plant kingdom thigmomorphogenesis is widely observed to alter plant morphology by reducing stem height and increasing stem diameter. The transcriptome is highly responsive to touch, including components of calcium signalling pathways and cell wall modification. One aspect of this cascade involves gibberellins and bZIP family transcription factors. Here, we present data connecting thigmomorphogenesis with secondary cell wall synthesis by gibberellin (GA) inactivation and bZIP translocation into the nucleus. Brachypodium distachyon SECONDARY WALL INTERACTING bZIP (SWIZ) protein translocated into the nucleus in response to mechanical stimulation. This translocation was mitigated by supplement with exogenous bioactive GA, and induced by chemical inhibition of GA synthesis. Misregulation of SWIZ expression resulted in plants hypersensitive to mechanical stimulation, with reduced height and increased secondary wall thickness. Classical touch responsive genes were upregulated in B. distachyon following touch, and we observe significant induction of the glycoside hydrolase 17 family, which may be indicative of a grass specific facet of thigmomorphogenesis. SWIZ binding to an E-box variant in exons and introns was associated with immediate activation followed by repression of gene expression. Thus, SWIZ is a transcriptional regulatory component of thigmomorphogenesis, which includes the thickening of secondary cell walls.

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Posted February 03, 2021.
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Touch-triggered bZIP translocation regulates elongation and secondary wall biosynthesis
Joshua H. Coomey, Kirk J.-M. MacKinnon, Pubudu P. Handakumbura, Ian W. McCahill, Gina M. Trabucco, Jessica Mazzola, Nicole A. Leblanc, Rithany Kheam, Miriam Hernandez-Romero, Kerrie Barry, Lifeng Liu, Ji E. Lee, John P. Vogel, Ronan C. O’Malley, James J. Chambers, Samuel P. Hazen
bioRxiv 2021.02.03.429573; doi: https://doi.org/10.1101/2021.02.03.429573
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Touch-triggered bZIP translocation regulates elongation and secondary wall biosynthesis
Joshua H. Coomey, Kirk J.-M. MacKinnon, Pubudu P. Handakumbura, Ian W. McCahill, Gina M. Trabucco, Jessica Mazzola, Nicole A. Leblanc, Rithany Kheam, Miriam Hernandez-Romero, Kerrie Barry, Lifeng Liu, Ji E. Lee, John P. Vogel, Ronan C. O’Malley, James J. Chambers, Samuel P. Hazen
bioRxiv 2021.02.03.429573; doi: https://doi.org/10.1101/2021.02.03.429573

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