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Mechanical Induction of Lateral Root Initiation in Arabidopsis Thaliana

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Mechanical Induction of Lateral Root Initiation in Arabidopsis Thaliana The Pennsylvania State University The Graduate School The Huck Institutes of the Life Sciences MECHANICAL INDUCTION OF LATERAL ROOT INITIATION A Dissertation in Integrative Biosciences by Gregory L. Richter ©2009 Gregory L. Richter Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy May 2009 ii The dissertation of Gregory L. Richter was reviewed and approved* by the following: Richard Cyr Professor of Biology Dissertation Advisor and Chair of Committee Simon Gilroy Professor of Botany David Braun Assistant Professor of Biology Randen Patterson Assistant Professor of Biology Timothy McNellis Associate Professor of Plant Pathology Peter Hudson Willaman Professor of Biology Director, Huck Institutes of the Life Sciences *Signatures are on file in the Graduate School iii ABSTRACT Unlike mammals whose development is limited to a short temporal window, plants produce organs de novo throughout their lifetime in order to adapt their architecture to the prevailing environmental conditions. Development of the root system represents a morphogenetic program where the positioning of new lateral organs occurs through the periodic recruitment of pericycle cells to become founder cells of a new lateral root (LR) primordium. While the hormone auxin appears intimately involved in specifying LR formation, it remains unclear why some pericycle cells are specified to initiate a LR while others are not. In the following thesis, I show that mechanical forces can act as one of the triggers for founder cell formation and so entrain the pattern of LR production to the environment. I observed that transient physical bending of the root was capable of eliciting LR formation to the convex side of the curve. Such mechanical stimulation triggered a Ca2+ transient within the pericycle, which was associated with the recruitment of ordinary pericycle cells to a LR founder cell fate. The initial establishment of the mechanically induced LR primordium was independent of an auxin supply from the shoot and was not disrupted by mutants in a suite of auxin transporters and receptor/response elements. Mechanical forces have long been proposed to act as plant morphogenetic factors, however the cellular elements that translate mechanical force to a developmental signaling cascade have remained obscure. My observations indicate that in the case of mechanical induction of LR formation, the program of organogenesis may be triggered by mechanically elicited Ca2+ changes that can even suppress the requirement for many auxin-related elements normally involved in founder cell recruitment. Thus, the mechano-sensitive Ca2+ signaling system responsible for eliciting LR founder cell fate provides a potentially widespread mechanism whereby external and endogenous mechanical forces could be translated into morphogenetic programs during plant growth and development. iv TABLE OF CONTENTS List of Figures ..........................................................................................................viii List of Movies ..........................................................................................................xi List of Abreviations..................................................................................................xii Acknowlegments......................................................................................................xiii Chapter 1 Introduction to the dissertation ................................................................1 Lateral roots arise from founder pericycle cells...........................................1 Lateral root formation is regulated via auxin-dependent processes ..............3 Interactions between auxin, cytokinins and brassinosteroids in lateral root formation......................................................................................5 Nitric oxide may play a role in auxin-dependent lateral root initiation.........6 Cell cycle control........................................................................................7 Towards a predictable model system for analyzing lateral root initiation.....9 References.........................................................................................................11 Chapter 2 Characterization of lateral root initiation in response to root curvature.....17 Introduction.......................................................................................................17 Auxin dominates lateral root production .....................................................17 Curvature of the primary root promotes lateral root initiation......................20 Materials and methods.......................................................................................21 Plant material and growth conditions ..........................................................21 v Histochemical GUS staining.......................................................................22 Laser ablation.............................................................................................22 Root bending ..............................................................................................23 Results and discussion ........................................................................................23 Root curvature is the result of mechanical force and tropic growth .............23 Root curvature forces lateral root initiation to occur earlier in development ........................................................................................24 Nominal gravitropic root curvature is sufficient for lateral root initiation....24 Gravitropic signaling is not required for curve-associated lateral root formation.............................................................................................25 Auxin dynamics precede curve-associated lateral root initiation events.......25 Mechanical force elicits lateral root initiation .............................................26 Conclusions ........................................................................................................26 References..........................................................................................................43 Chapter 3 Auxin signaling and curve-associated lateral root initiation .....................47 Introduction.......................................................................................................47 Components of the auxin signal..................................................................47 Auxin signaling is resposible for the endogenous regulation of lateral root initiation.......................................................................................49 Materials and methods.......................................................................................51 Plant material and growth conditions ..........................................................51 Shoot removal and auxin treatment.............................................................52 Root bending ..............................................................................................52 vi Results and discussion .......................................................................................53 An acropetal supply of auxin is required for bend-induced lateral root emergence but not for primordium formation.......................................53 Bend-induced lateral root formation occurs in auxin-related mutants ..........53 Bend-induced lateral root formation breaks the spacing rules for lateral root placement.....................................................................................55 References.........................................................................................................67 Chapter 4 Curve associated lateral root initiation is likely a calcium-mediated mechanoresponse...............................................................................................74 Introduction.......................................................................................................74 The generation of calcium signals in plants.................................................74 Calcium as a regulator of cell-cycle progression..........................................77 Materials and methods.......................................................................................79 Plant material and growth conditions ..........................................................79 Application of lathanum chloride................................................................79 Calcium imaging ........................................................................................79 Root bending ..............................................................................................80 Results and discussion .......................................................................................80 Transient bending is sufficient to trigger lateral root production..................80 Bending elicits calcium increases in the pericycle of stretched cells............81 References.........................................................................................................91 Chapter 5 Conclusion ...............................................................................................96 vii Identifying the plant mechanosensory channel from pericycle cells ............98 Identifying downstream targets of the calcium change in founder pericycle cells......................................................................................100 Broader significance of my
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