A Gene Regulatory Network for Cellular Reprogramming in Plant Regeneration

Abstract Wounding triggers organ regeneration in many plant species, and application of plant hormones, such as auxin and cytokinin, enhances their regenerative capacities in tissue culture. Recent studies have identified several key players mediating wound- and/or plant hormone-induced cellular rep...

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Vydané v:	Plant and cell physiology Ročník 59; číslo 4; s. 765 - 777
Hlavní autori:	Ikeuchi, Momoko, Shibata, Michitaro, Rymen, Bart, Iwase, Akira, B�gman, Anne-Maarit, Watt, Lewis, Coleman, Duncan, Favero, David S, Takahashi, Tatsuya, Ahnert, Sebastian E, Brady, Siobhan M, Sugimoto, Keiko
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	Japan Oxford University Press 01.04.2018
Predmet:	Arabidopsis Proteins - metabolism Cellular Reprogramming - drug effects Cellular Reprogramming - genetics Cytokinins - pharmacology Gene Regulatory Networks - drug effects Genes, Plant Indoleacetic Acids - pharmacology Plant Cells - metabolism Plants - genetics Promoter Regions, Genetic Regeneration - drug effects Regeneration - genetics Transcription Factors - metabolism Callus formation Cellular reprogramming Regeneration Wound stress Auxin Cytokinin
ISSN:	0032-0781, 1471-9053, 1471-9053
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Abstract	Abstract Wounding triggers organ regeneration in many plant species, and application of plant hormones, such as auxin and cytokinin, enhances their regenerative capacities in tissue culture. Recent studies have identified several key players mediating wound- and/or plant hormone-induced cellular reprogramming, but the global architecture of gene regulatory relationships underlying plant cellular reprogramming is still far from clear. In this study, we uncovered a gene regulatory network (GRN) associated with plant cellular reprogramming by using an enhanced yeast one-hybrid (eY1H) screen systematically to identify regulatory relationships between 252 transcription factors (TFs) and 48 promoters. Our network analyses suggest that wound- and/or hormone-invoked signals exhibit extensive cross-talk and regulate many common reprogramming-associated genes via multilayered regulatory cascades. Our data suggest that PLETHORA 3 (PLT3), ENHANCER OF SHOOT REGENERATION 1 (ESR1) and HEAT SHOCK FACTOR B 1 (HSFB1) act as critical nodes that have many overlapping targets and potentially connect upstream stimuli to downstream developmental decisions. Interestingly, a set of wound-inducible APETALA 2/ETHYLENE RESPONSE FACTORs (AP2/ERFs) appear to regulate these key genes, which, in turn, form feed-forward cascades that control downstream targets associated with callus formation and organ regeneration. In addition, we found another regulatory pathway, mediated by LATERAL ORGAN BOUNDARY/ASYMMETRIC LEAVES 2 (LOB/AS2) TFs, which probably plays a distinct but partially overlapping role alongside the AP2/ERFs in the putative gene regulatory cascades. Taken together, our findings provide the first global picture of the GRN governing plant cell reprogramming, which will serve as a valuable resource for future studies.
AbstractList	Wounding triggers organ regeneration in many plant species, and application of plant hormones, such as auxin and cytokinin, enhances their regenerative capacities in tissue culture. Recent studies have identified several key players mediating wound- and/or plant hormone-induced cellular reprogramming, but the global architecture of gene regulatory relationships underlying plant cellular reprogramming is still far from clear. In this study, we uncovered a gene regulatory network (GRN) associated with plant cellular reprogramming by using an enhanced yeast one-hybrid (eY1H) screen systematically to identify regulatory relationships between 252 transcription factors (TFs) and 48 promoters. Our network analyses suggest that wound- and/or hormone-invoked signals exhibit extensive cross-talk and regulate many common reprogramming-associated genes via multilayered regulatory cascades. Our data suggest that PLETHORA 3 (PLT3), ENHANCER OF SHOOT REGENERATION 1 (ESR1) and HEAT SHOCK FACTOR B 1 (HSFB1) act as critical nodes that have many overlapping targets and potentially connect upstream stimuli to downstream developmental decisions. Interestingly, a set of wound-inducible APETALA 2/ETHYLENE RESPONSE FACTORs (AP2/ERFs) appear to regulate these key genes, which, in turn, form feed-forward cascades that control downstream targets associated with callus formation and organ regeneration. In addition, we found another regulatory pathway, mediated by LATERAL ORGAN BOUNDARY/ASYMMETRIC LEAVES 2 (LOB/AS2) TFs, which probably plays a distinct but partially overlapping role alongside the AP2/ERFs in the putative gene regulatory cascades. Taken together, our findings provide the first global picture of the GRN governing plant cell reprogramming, which will serve as a valuable resource for future studies.Wounding triggers organ regeneration in many plant species, and application of plant hormones, such as auxin and cytokinin, enhances their regenerative capacities in tissue culture. Recent studies have identified several key players mediating wound- and/or plant hormone-induced cellular reprogramming, but the global architecture of gene regulatory relationships underlying plant cellular reprogramming is still far from clear. In this study, we uncovered a gene regulatory network (GRN) associated with plant cellular reprogramming by using an enhanced yeast one-hybrid (eY1H) screen systematically to identify regulatory relationships between 252 transcription factors (TFs) and 48 promoters. Our network analyses suggest that wound- and/or hormone-invoked signals exhibit extensive cross-talk and regulate many common reprogramming-associated genes via multilayered regulatory cascades. Our data suggest that PLETHORA 3 (PLT3), ENHANCER OF SHOOT REGENERATION 1 (ESR1) and HEAT SHOCK FACTOR B 1 (HSFB1) act as critical nodes that have many overlapping targets and potentially connect upstream stimuli to downstream developmental decisions. Interestingly, a set of wound-inducible APETALA 2/ETHYLENE RESPONSE FACTORs (AP2/ERFs) appear to regulate these key genes, which, in turn, form feed-forward cascades that control downstream targets associated with callus formation and organ regeneration. In addition, we found another regulatory pathway, mediated by LATERAL ORGAN BOUNDARY/ASYMMETRIC LEAVES 2 (LOB/AS2) TFs, which probably plays a distinct but partially overlapping role alongside the AP2/ERFs in the putative gene regulatory cascades. Taken together, our findings provide the first global picture of the GRN governing plant cell reprogramming, which will serve as a valuable resource for future studies. Abstract Wounding triggers organ regeneration in many plant species, and application of plant hormones, such as auxin and cytokinin, enhances their regenerative capacities in tissue culture. Recent studies have identified several key players mediating wound- and/or plant hormone-induced cellular reprogramming, but the global architecture of gene regulatory relationships underlying plant cellular reprogramming is still far from clear. In this study, we uncovered a gene regulatory network (GRN) associated with plant cellular reprogramming by using an enhanced yeast one-hybrid (eY1H) screen systematically to identify regulatory relationships between 252 transcription factors (TFs) and 48 promoters. Our network analyses suggest that wound- and/or hormone-invoked signals exhibit extensive cross-talk and regulate many common reprogramming-associated genes via multilayered regulatory cascades. Our data suggest that PLETHORA 3 (PLT3), ENHANCER OF SHOOT REGENERATION 1 (ESR1) and HEAT SHOCK FACTOR B 1 (HSFB1) act as critical nodes that have many overlapping targets and potentially connect upstream stimuli to downstream developmental decisions. Interestingly, a set of wound-inducible APETALA 2/ETHYLENE RESPONSE FACTORs (AP2/ERFs) appear to regulate these key genes, which, in turn, form feed-forward cascades that control downstream targets associated with callus formation and organ regeneration. In addition, we found another regulatory pathway, mediated by LATERAL ORGAN BOUNDARY/ASYMMETRIC LEAVES 2 (LOB/AS2) TFs, which probably plays a distinct but partially overlapping role alongside the AP2/ERFs in the putative gene regulatory cascades. Taken together, our findings provide the first global picture of the GRN governing plant cell reprogramming, which will serve as a valuable resource for future studies. Wounding triggers organ regeneration in many plant species, and application of plant hormones, such as auxin and cytokinin, enhances their regenerative capacities in tissue culture. Recent studies have identified several key players mediating wound- and/or plant hormone-induced cellular reprogramming, but the global architecture of gene regulatory relationships underlying plant cellular reprogramming is still far from clear. In this study, we uncovered a gene regulatory network (GRN) associated with plant cellular reprogramming by using an enhanced yeast one-hybrid (eY1H) screen systematically to identify regulatory relationships between 252 transcription factors (TFs) and 48 promoters. Our network analyses suggest that wound- and/or hormone-invoked signals exhibit extensive cross-talk and regulate many common reprogramming-associated genes via multilayered regulatory cascades. Our data suggest that PLETHORA 3 (PLT3), ENHANCER OF SHOOT REGENERATION 1 (ESR1) and HEAT SHOCK FACTOR B 1 (HSFB1) act as critical nodes that have many overlapping targets and potentially connect upstream stimuli to downstream developmental decisions. Interestingly, a set of wound-inducible APETALA 2/ETHYLENE RESPONSE FACTORs (AP2/ERFs) appear to regulate these key genes, which, in turn, form feed-forward cascades that control downstream targets associated with callus formation and organ regeneration. In addition, we found another regulatory pathway, mediated by LATERAL ORGAN BOUNDARY/ASYMMETRIC LEAVES 2 (LOB/AS2) TFs, which probably plays a distinct but partially overlapping role alongside the AP2/ERFs in the putative gene regulatory cascades. Taken together, our findings provide the first global picture of the GRN governing plant cell reprogramming, which will serve as a valuable resource for future studies.
Author	Ikeuchi, Momoko Sugimoto, Keiko Rymen, Bart Ahnert, Sebastian E Brady, Siobhan M B�gman, Anne-Maarit Coleman, Duncan Favero, David S Iwase, Akira Takahashi, Tatsuya Watt, Lewis Shibata, Michitaro
Author_xml	– sequence: 1 givenname: Momoko orcidid: 0000-0001-9474-5131 surname: Ikeuchi fullname: Ikeuchi, Momoko email: momoko.ikeuchi@riken.jp organization: RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi, Yokohama, Kanagawa, 230-0045 Japan – sequence: 2 givenname: Michitaro surname: Shibata fullname: Shibata, Michitaro organization: RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi, Yokohama, Kanagawa, 230-0045 Japan – sequence: 3 givenname: Bart surname: Rymen fullname: Rymen, Bart organization: RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi, Yokohama, Kanagawa, 230-0045 Japan – sequence: 4 givenname: Akira surname: Iwase fullname: Iwase, Akira organization: RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi, Yokohama, Kanagawa, 230-0045 Japan – sequence: 5 givenname: Anne-Maarit surname: B�gman fullname: B�gman, Anne-Maarit organization: Department of Plant Biology and Genome Center, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA – sequence: 6 givenname: Lewis surname: Watt fullname: Watt, Lewis organization: RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi, Yokohama, Kanagawa, 230-0045 Japan – sequence: 7 givenname: Duncan surname: Coleman fullname: Coleman, Duncan organization: RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi, Yokohama, Kanagawa, 230-0045 Japan – sequence: 8 givenname: David S surname: Favero fullname: Favero, David S organization: RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi, Yokohama, Kanagawa, 230-0045 Japan – sequence: 9 givenname: Tatsuya surname: Takahashi fullname: Takahashi, Tatsuya organization: RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi, Yokohama, Kanagawa, 230-0045 Japan – sequence: 10 givenname: Sebastian E surname: Ahnert fullname: Ahnert, Sebastian E organization: Sainsbury Laboratory, University of Cambridge, Bateman Street, Cambridge, CB2 1LR UK – sequence: 11 givenname: Siobhan M surname: Brady fullname: Brady, Siobhan M organization: Department of Plant Biology and Genome Center, University of California, Davis, One Shields Avenue, Davis, CA 95616, USA – sequence: 12 givenname: Keiko surname: Sugimoto fullname: Sugimoto, Keiko email: keiko.sugimoto@riken.jp organization: RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi, Yokohama, Kanagawa, 230-0045 Japan
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Keywords	Callus formation Cellular reprogramming Regeneration Wound stress Auxin Cytokinin
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Snippet	Abstract Wounding triggers organ regeneration in many plant species, and application of plant hormones, such as auxin and cytokinin, enhances their... Wounding triggers organ regeneration in many plant species, and application of plant hormones, such as auxin and cytokinin, enhances their regenerative...
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SubjectTerms	Arabidopsis Proteins - metabolism Cellular Reprogramming - drug effects Cellular Reprogramming - genetics Cytokinins - pharmacology Gene Regulatory Networks - drug effects Genes, Plant Indoleacetic Acids - pharmacology Plant Cells - metabolism Plants - genetics Promoter Regions, Genetic Regeneration - drug effects Regeneration - genetics Transcription Factors - metabolism
Title	A Gene Regulatory Network for Cellular Reprogramming in Plant Regeneration
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