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PLETHORA Genes Control Regeneration by a Two-Step Mechanism

Kareem, Abdul and Durgaprasad, Kavya and Sugimoto, Kaoru and Du, Yujuan and Pulianmackal, Ajai J. and Trivedi, Zankhana B. and Abhayadev, Pazhoor V. and Pinon, Violaine and Meyerowitz, Elliot M. and Scheres, Ben and Prasad, Kalika (2015) PLETHORA Genes Control Regeneration by a Two-Step Mechanism. Current Biology, 25 (8). pp. 1017-1030. ISSN 0960-9822. PMCID PMC4829346. https://resolver.caltech.edu/CaltechAUTHORS:20150407-081937193

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Abstract

Regeneration, a remarkable example of developmental plasticity displayed by both plants and animals, involves successive developmental events driven in response to environmental cues. Despite decades of study on the ability of the plant tissues to regenerate a complete fertile shoot system after inductive cues, the mechanisms by which cells acquire pluripotency and subsequently regenerate complete organs remain unknown. Here, we show that three PLETHORA (PLT) genes, PLT3, PLT5, and PLT7, regulate de novo shoot regeneration in Arabidopsis by controlling two distinct developmental events. Cumulative loss of function of these three genes causes the intermediate cell mass, callus, to be incompetent to form shoot progenitors, whereas induction of PLT5 or PLT7 can render shoot regeneration hormone-independent. We further show that PLT3, PLT5, and PLT7 establish pluripotency by activating root stem cell regulators PLT1 and PLT2, as reconstitution of either PLT1 or PLT2 in the plt3; plt5-2; plt7 mutant re-established the competence to regenerate shoot progenitor cells but did not lead to the completion of shoot regeneration. PLT3, PLT5, and PLT7 additionally regulate and require the shoot-promoting factor CUP-SHAPED COTYLEDON2 (CUC2) to complete the shoot-formation program. Our findings uncouple the acquisition of competence to regenerate shoot progenitor cells from completion of shoot formation, indicating a two-step mechanism of de novo shoot regeneration that operates in all tested plant tissues irrespective of their origin. Our studies reveal intermediate developmental phases of regeneration and provide a deeper understanding into the mechanistic basis of regeneration.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1016/j.cub.2015.02.022DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4829346/PubMed CentralArticle
ORCID:
AuthorORCID
Meyerowitz, Elliot M.0000-0003-4798-5153
Additional Information:© 2015 Elsevier Ltd. Received 2 December 2014, Revised 14 January 2015, Accepted 4 February 2015, Available online 26 March 2015. Published: March 26, 2015. K.P. acknowledges early startup grant from Indian Institute of Science Education and Research, Thiruvananthapuram and the grant from Department of Biotechnology, Government of India. E.M.M. and K.S. acknowledge funding from grant IOS-0846192 from the US National Science Foundation and funding from the Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation (through grant GBMF3406). B.S., Y.D., and V.P. acknowledge European Research Council Advanced Investigator Grant and SPINOZA grant Dutch Science Organization. A.K. is supported by IISER-TVM fellowship. K.D. and Z.B.T. are supported by INSPIRE fellowship. The authors acknowledge Dr. L.S. Shashidhara and Dr. Sunish K. Radhakrishnan for critical reading of the manuscript. We thank Dr. Ari Pekka Mahonen for the generous gift of wild-type seeds of PLT1::PLT1:vYFP and PLT2::PLT2:vYFP and Dr. Mitsuhiro Aida for kindly providing cuc1-5; cuc2-3/+ mutant seeds. We thank Allipra Sreejith, Renjini Rajan, Pooja Panchariya, and Pallavi Palival for the technical support during the course of experiments.
Funders:
Funding AgencyGrant Number
Indian Institute of Science Education and ResearchUNSPECIFIED
Department of Biotechnology (India)UNSPECIFIED
NSFIOS-0846192
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Gordon and Betty Moore FoundationGBMF3406
European Research Council (ERC)UNSPECIFIED
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)SPINOZA
IISER-TVM fellowshipUNSPECIFIED
INSPIRE fellowshipUNSPECIFIED
Issue or Number:8
PubMed Central ID:PMC4829346
Record Number:CaltechAUTHORS:20150407-081937193
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20150407-081937193
Official Citation:Abdul Kareem, Kavya Durgaprasad, Kaoru Sugimoto, Yujuan Du, Ajai J. Pulianmackal, Zankhana B. Trivedi, Pazhoor V. Abhayadev, Violaine Pinon, Elliot M. Meyerowitz, Ben Scheres, Kalika Prasad, PLETHORA Genes Control Regeneration by a Two-Step Mechanism, Current Biology, Volume 25, Issue 8, 20 April 2015, Pages 1017-1030, ISSN 0960-9822, http://dx.doi.org/10.1016/j.cub.2015.02.022. (http://www.sciencedirect.com/science/article/pii/S096098221500161X)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:56409
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:07 Apr 2015 19:47
Last Modified:06 May 2020 22:47

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