F‐Actin Polarization and Microtubule Integrity Direct Regeneration Patterns and Polarity of Cell Outgrowth in Wound‐Induced Reprogramming
Plants have developed a high regenerative capacity to repair damaged tissues and regenerate new organs in response to injury. When wounded, cells detect mechanical forces through their cytoskeletons and transmit molecular signals to the nucleus, triggering cell reprogramming. As mechanosensing and c...
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Published in | Plant, cell and environment |
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Language | English |
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22.06.2025
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Abstract | Plants have developed a high regenerative capacity to repair damaged tissues and regenerate new organs in response to injury. When wounded, cells detect mechanical forces through their cytoskeletons and transmit molecular signals to the nucleus, triggering cell reprogramming. As mechanosensing and cell reprogramming have been studied separately, the connection between these processes and the role of cytoskeletal networks in regeneration is still unclear. This study used Physcomitrium patens to investigate the spatiotemporal dynamics of actin filaments and microtubules during wound‐induced cell reprogramming. Upon laser‐induced wounding, we observed a rapid and localized accumulation of F‐actin at the plasma membrane of the neighboring cells next to the wounding site, whereas microtubules showed no immediate discernible changes. Disruption of F‐actin severely impaired overall regeneration, leading to significant reductions in the reprogramming rate. Perturbations of microtubules primarily impacted regenerative cell divisions. Depolymerization of cytoskeletal networks altered regeneration patterns, reflected in the higher ratio of cell outgrowth to division and the outgrowth polarity. These findings underscore the functional role of the cytoskeleton in regulating cell reprogramming. This study reveals that early cytoskeletal polarization after wounding guides the polarity of cell outgrowth, providing new insights into how plants regenerate from mechanical damage.
This study establishes a precise wounding system in Physcomitrium patens leaves, enabling cellular‐level analysis of regeneration. We show that rapid F‐actin polarization and sustained microtubule integrity are both essential for guiding cell polarity and proper regeneration patterns. |
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AbstractList | Plants have developed a high regenerative capacity to repair damaged tissues and regenerate new organs in response to injury. When wounded, cells detect mechanical forces through their cytoskeletons and transmit molecular signals to the nucleus, triggering cell reprogramming. As mechanosensing and cell reprogramming have been studied separately, the connection between these processes and the role of cytoskeletal networks in regeneration is still unclear. This study used Physcomitrium patens to investigate the spatiotemporal dynamics of actin filaments and microtubules during wound‐induced cell reprogramming. Upon laser‐induced wounding, we observed a rapid and localized accumulation of F‐actin at the plasma membrane of the neighboring cells next to the wounding site, whereas microtubules showed no immediate discernible changes. Disruption of F‐actin severely impaired overall regeneration, leading to significant reductions in the reprogramming rate. Perturbations of microtubules primarily impacted regenerative cell divisions. Depolymerization of cytoskeletal networks altered regeneration patterns, reflected in the higher ratio of cell outgrowth to division and the outgrowth polarity. These findings underscore the functional role of the cytoskeleton in regulating cell reprogramming. This study reveals that early cytoskeletal polarization after wounding guides the polarity of cell outgrowth, providing new insights into how plants regenerate from mechanical damage.
This study establishes a precise wounding system in Physcomitrium patens leaves, enabling cellular‐level analysis of regeneration. We show that rapid F‐actin polarization and sustained microtubule integrity are both essential for guiding cell polarity and proper regeneration patterns. Plants have developed a high regenerative capacity to repair damaged tissues and regenerate new organs in response to injury. When wounded, cells detect mechanical forces through their cytoskeletons and transmit molecular signals to the nucleus, triggering cell reprogramming. As mechanosensing and cell reprogramming have been studied separately, the connection between these processes and the role of cytoskeletal networks in regeneration is still unclear. This study used Physcomitrium patens to investigate the spatiotemporal dynamics of actin filaments and microtubules during wound-induced cell reprogramming. Upon laser-induced wounding, we observed a rapid and localized accumulation of F-actin at the plasma membrane of the neighboring cells next to the wounding site, whereas microtubules showed no immediate discernible changes. Disruption of F-actin severely impaired overall regeneration, leading to significant reductions in the reprogramming rate. Perturbations of microtubules primarily impacted regenerative cell divisions. Depolymerization of cytoskeletal networks altered regeneration patterns, reflected in the higher ratio of cell outgrowth to division and the outgrowth polarity. These findings underscore the functional role of the cytoskeleton in regulating cell reprogramming. This study reveals that early cytoskeletal polarization after wounding guides the polarity of cell outgrowth, providing new insights into how plants regenerate from mechanical damage. Plants have developed a high regenerative capacity to repair damaged tissues and regenerate new organs in response to injury. When wounded, cells detect mechanical forces through their cytoskeletons and transmit molecular signals to the nucleus, triggering cell reprogramming. As mechanosensing and cell reprogramming have been studied separately, the connection between these processes and the role of cytoskeletal networks in regeneration is still unclear. This study used Physcomitrium patens to investigate the spatiotemporal dynamics of actin filaments and microtubules during wound-induced cell reprogramming. Upon laser-induced wounding, we observed a rapid and localized accumulation of F-actin at the plasma membrane of the neighboring cells next to the wounding site, whereas microtubules showed no immediate discernible changes. Disruption of F-actin severely impaired overall regeneration, leading to significant reductions in the reprogramming rate. Perturbations of microtubules primarily impacted regenerative cell divisions. Depolymerization of cytoskeletal networks altered regeneration patterns, reflected in the higher ratio of cell outgrowth to division and the outgrowth polarity. These findings underscore the functional role of the cytoskeleton in regulating cell reprogramming. This study reveals that early cytoskeletal polarization after wounding guides the polarity of cell outgrowth, providing new insights into how plants regenerate from mechanical damage.Plants have developed a high regenerative capacity to repair damaged tissues and regenerate new organs in response to injury. When wounded, cells detect mechanical forces through their cytoskeletons and transmit molecular signals to the nucleus, triggering cell reprogramming. As mechanosensing and cell reprogramming have been studied separately, the connection between these processes and the role of cytoskeletal networks in regeneration is still unclear. This study used Physcomitrium patens to investigate the spatiotemporal dynamics of actin filaments and microtubules during wound-induced cell reprogramming. Upon laser-induced wounding, we observed a rapid and localized accumulation of F-actin at the plasma membrane of the neighboring cells next to the wounding site, whereas microtubules showed no immediate discernible changes. Disruption of F-actin severely impaired overall regeneration, leading to significant reductions in the reprogramming rate. Perturbations of microtubules primarily impacted regenerative cell divisions. Depolymerization of cytoskeletal networks altered regeneration patterns, reflected in the higher ratio of cell outgrowth to division and the outgrowth polarity. These findings underscore the functional role of the cytoskeleton in regulating cell reprogramming. This study reveals that early cytoskeletal polarization after wounding guides the polarity of cell outgrowth, providing new insights into how plants regenerate from mechanical damage. |
Author | Huang, Yi‐Ting Tang, Han Willemsen, Viola Yen, Yun‐Ching Vermeer, Joop E. M. |
Author_xml | – sequence: 1 givenname: Yi‐Ting surname: Huang fullname: Huang, Yi‐Ting organization: Graduate Institute of Biochemistry National Chung Hsing University Taichung ROC Taiwan – sequence: 2 givenname: Yun‐Ching surname: Yen fullname: Yen, Yun‐Ching organization: Graduate Institute of Biochemistry National Chung Hsing University Taichung ROC Taiwan – sequence: 3 givenname: Joop E. M. surname: Vermeer fullname: Vermeer, Joop E. M. organization: Laboratory of Molecular and Cell Biology, Institute of Biology University of Neuchâtel Neuchâtel Switzerland – sequence: 4 givenname: Viola surname: Willemsen fullname: Willemsen, Viola organization: Cluster of Plant Developmental Biology, Laboratory of Cell and Developmental Biology Wageningen University & Research Wageningen the Netherlands – sequence: 5 givenname: Han orcidid: 0000-0001-6152-6637 surname: Tang fullname: Tang, Han organization: Graduate Institute of Biochemistry National Chung Hsing University Taichung ROC Taiwan, Advanced Plant and Food Crop Biotechnology Center National Chung Hsing University Taichung Taiwan |
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Cites_doi | 10.1016/j.pbi.2017.08.004 10.1126/science.1165594 10.1105/tpc.108.061705 10.1242/dev.097444 10.1007/s11693-014-9142-x 10.1073/pnas.2003346117 10.1111/jmi.12395 10.1111/nph.19090 10.1242/dev.134668 10.1083/jcb.201802039 10.1093/dnares/7.1.9 10.1111/febs.16571 10.1016/j.tcb.2010.12.004 10.1038/nprot.2014.024 10.1016/j.pbi.2018.12.002 10.1016/j.pbi.2020.05.008 10.1016/j.cell.2008.01.040 10.1007/BF00265581 10.1038/s41477-019-0464-2 10.1105/tpc.111.088005 10.1093/plcell/koab230 10.1111/nph.18683 10.1007/s10265-015-0706-y 10.1105/tpc.19.00828 10.1016/j.devcel.2024.03.009 10.1073/pnas.0901170106 10.1093/pcp/pcaf008 |
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Keywords | mechanosensing polarization wound‐induced cell reprogramming P. patens cytoskeletal networks |
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