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Local cues and asymmetric cell divisions underpin body plan transitions in the moss Physcomitrella patens

Harrison, C. Jill and Roeder, Adrienne H. K. and Meyerowitz, Elliot M. and Langdale, Jane A. (2009) Local cues and asymmetric cell divisions underpin body plan transitions in the moss Physcomitrella patens. Current Biology, 19 (6). pp. 461-471. ISSN 0960-9822. doi:10.1016/j.cub.2009.02.050. https://resolver.caltech.edu/CaltechAUTHORS:20090629-093440163

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Abstract

Background: Land plants evolved from aquatic algae more than 450 million years ago. Algal sisters of land plants grow through the activity of apical initial cells that cleave either in one plane to generate filaments or in two planes to generate mats. Acquisition of the capacity for cell cleavage in three planes facilitated the formation of upright bushy body plans and enabled the invasion of land. Evolutionary transitions between filamentous, planar, and bushy growth are mimicked within moss life cycles. Results: We have developed lineage analysis techniques to assess how transitions between growth forms occur in the moss Physcomitrella patens. We show that initial cells giving rise either to new filaments or bushy shoots are frequently juxtaposed on a single parent filament, suggesting a role for short-range cues in specifying differences in cell fate. Shoot initials cleave four times to establish a tetrahedral shape and subsequently cleave in three planes, generating bushy growth. Asymmetric and self-replacing divisions from the tetrahedral initial generate leaf initials that divide asymmetrically to self-replace and to produce daughter cells with restricted fate. The cessation of division in the leaf is distributed unevenly and contributes to final leaf shape. Conclusions: In contrast to flowering plants, changes in body plan in P. patens are regulated by cues acting at the level of single cells and are mediated through asymmetric divisions. Genetic mechanisms regulating shoot and leaf development in P. patens are therefore likely to differ substantially from mechanisms operating in plants with more recent evolutionary origins.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1016/j.cub.2009.02.050DOIArticle
http://www.sciencedirect.com/science/article/pii/S0960982209008033PublisherArticle
ORCID:
AuthorORCID
Meyerowitz, Elliot M.0000-0003-4798-5153
Additional Information:© 2009 Elsevier Ltd. Received 8 October 2008; revised 17 February 2009; accepted 19 February 2009. Published online: March 19, 2009. Available online 19 March 2009. We thank Mohi Rezvani for use of X-ray sets, Mark Fricker and Marcus Heisler for help with microscopy, Ian Moore and Liam Dolan for useful discussions about sectors, Julie Bull and Arnavaz Garda for technical support, and Jeff Duckett for advice on moss. This work was supported by a short-term fellowship from The International Human Frontier Science Program Organization and a Queen’s College Browne Research Fellowship to C.J.H., a Helen Hay Whitney Fellowship to A.H.K.R., grants to J.A.L. from the UK Biotechnology and Biological Sciences Research Council (grant number BB/C513069/1) and the Gatsby Charitable Foundation (G1920), and a grant to E.M.M. from the U.S. National Science Foundation (grant number IOB-0544915).
Funders:
Funding AgencyGrant Number
Biotechnology and Biological Sciences Research Council (BBSRC)BB/C513069/1
Gatsby Charitable FoundationG1920
NSFIOB-0544915
Human Frontier Science ProgramUNSPECIFIED
Queen’s CollegeUNSPECIFIED
Helen Hay Whitney FoundationUNSPECIFIED
Subject Keywords:DEVBIO; EVO_ECOL
Issue or Number:6
DOI:10.1016/j.cub.2009.02.050
Record Number:CaltechAUTHORS:20090629-093440163
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20090629-093440163
Official Citation:C. Jill Harrison, Adrienne H.K. Roeder, Elliot M. Meyerowitz, Jane A. Langdale, Local Cues and Asymmetric Cell Divisions Underpin Body Plan Transitions in the Moss Physcomitrella patens, Current Biology, Volume 19, Issue 6, 24 March 2009, Pages 461-471, ISSN 0960-9822, http://dx.doi.org/10.1016/j.cub.2009.02.050. (http://www.sciencedirect.com/science/article/pii/S0960982209008033)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:14451
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:13 Aug 2009 04:36
Last Modified:08 Nov 2021 23:11

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