A coherent feed-forward loop drives vascular regeneration in damaged aerial organs of plants growing in a normal developmental context
Radhakrishnan, Dhanya ; Shanmukhan, Anju Pallipurath ; Kareem, Abdul ; Aiyaz, Mohammed ; Varapparambathu, Vijina ; Toms, Ashna ; Kerstens, Merijn ; Valsakumar, Devisree ; Landge, Amit N. ; Shaji, Anil ; Mathew, Mathew K. ; Sawchuk, Megan G. ; Scarpella, Enrico ; Krizek, Beth A. ; Efroni, Idan ; Mähönen, Ari Pekka ; Willemsen, Viola ; Scheres, Ben ; Prasad, Kalika - \ 2020
Development 147 (2020)6. - ISSN 0950-1991
Arabidopsis - Auxin - CUC2 - PIN1 - PLT - Vascular regeneration - Wound repair
Aerial organs of plants, being highly prone to local injuries, require tissue restoration to ensure their survival. However, knowledge of the underlying mechanism is sparse. In this study, we mimicked natural injuries in growing leaves and stems to study the reunion between mechanically disconnected tissues. We show that PLETHORA (PLT) and AINTEGUMENTA (ANT) genes, which encode stem cell-promoting factors, are activated and contribute to vascular regeneration in response to these injuries. PLT proteins bind to and activate the CUC2 promoter. PLT proteins and CUC2 regulate the transcription of the local auxin biosynthesis gene YUC4 in a coherent feed-forward loop, and this process is necessary to drive vascular regeneration. In the absence of this PLT-mediated regeneration response, leaf ground tissue cells can neither acquire the early vascular identity marker ATHB8, nor properly polarise auxin transporters to specify new venation paths. The PLT-CUC2 module is required for vascular regeneration, but is dispensable for midvein formation in leaves. We reveal the mechanisms of vascular regeneration in plants and distinguish between the wound-repair ability of the tissue and its formation during normal development.
Gradient Expression of Transcription Factor Imposes a Boundary on Organ Regeneration Potential in Plants
Durgaprasad, Kavya ; Roy, Merin V. ; Venugopal M., Anjali ; Kareem, Abdul ; Raj, Kiran ; Willemsen, Viola ; Mähönen, Ari Pekka ; Scheres, Ben ; Prasad, Kalika - \ 2019
Cell Reports 29 (2019)2. - ISSN 2211-1247 - p. 453 - 463.
Arabidopsis - autoregulation - dosage dependent - lateral root - multicellular organism - organ regeneration - organ size - PLETHORA gradient - root meristem - stem cells
Durgaprasad et al. show that dosage of a gradient-expressed transcription factor orchestrates the regeneration competence in developing root tip. Interestingly, the regeneration potential of root meristem can be separated from its size.
Mobile PEAR transcription factors integrate positional cues to prime cambial growth
Miyashima, Shunsuke ; Roszak, Pawel ; Sevilem, Iris ; Toyokura, Koichi ; Blob, Bernhard ; Heo, Jung-Ok ; Mellor, Nathan ; Help-Rinta-Rahko, Hanna ; Otero, Sofia ; Smet, Wouter ; Boekschoten, Mark ; Hooiveld, Guido ; Hashimoto, Kayo ; Smetana, Ondřej ; Siligato, Riccardo ; Wallner, Eva Sophie ; Mähönen, Ari Pekka ; Kondo, Yuki ; Melnyk, Charles W. ; Greb, Thomas ; Nakajima, Keiji ; Sozzani, Rosangela ; Bishopp, Anthony ; Rybel, Bert de; Helariutta, Ykä - \ 2019
Nature 565 (2019)7740. - ISSN 0028-0836 - p. 490 - 494.
Apical growth in plants initiates upon seed germination, whereas radial growth is primed only during early ontogenesis in procambium cells and activated later by the vascular cambium1. Although it is not known how radial growth is organized and regulated in plants, this system resembles the developmental competence observed in some animal systems, in which pre-existing patterns of developmental potential are established early on2,3. Here we show that in Arabidopsis the initiation of radial growth occurs around early protophloem-sieve-element cell files of the root procambial tissue. In this domain, cytokinin signalling promotes the expression of a pair of mobile transcription factors—PHLOEM EARLY DOF 1 (PEAR1) and PHLOEM EARLY DOF 2 (PEAR2)—and their four homologues (DOF6, TMO6, OBP2 and HCA2), which we collectively name PEAR proteins. The PEAR proteins form a short-range concentration gradient that peaks at protophloem sieve elements, and activates gene expression that promotes radial growth. The expression and function of PEAR proteins are antagonized by the HD-ZIP III proteins, well-known polarity transcription factors4—the expression of which is concentrated in the more-internal domain of radially non-dividing procambial cells by the function of auxin, and mobile miR165 and miR166 microRNAs. The PEAR proteins locally promote transcription of their inhibitory HD-ZIP III genes, and thereby establish a negative-feedback loop that forms a robust boundary that demarks the zone of cell division. Taken together, our data establish that during root procambial development there exists a network in which a module that links PEAR and HD-ZIP III transcription factors integrates spatial information of the hormonal domains and miRNA gradients to provide adjacent zones of dividing and more-quiescent cells, which forms a foundation for further radial growth.
Theoretical approaches to understanding root vascular patterning : A consensus between recent models
Mellor, Nathan ; Adibi, Milad ; El-Showk, Sedeer ; Rybel, Bert De; King, John ; Mähönen, Ari Pekka ; Weijers, Dolf ; Bishopp, Anthony ; Etchells, Peter - \ 2017
Journal of Experimental Botany 68 (2017)1. - ISSN 0022-0957 - p. 5 - 16.
Auxin - Cytokinin - Mathematical modeling - Organ patterning - Systems biology - Vascular development
The root vascular tissues provide an excellent system for studying organ patterning, as the specification of these tissues signals a transition from radial symmetry to bisymmetric patterns. The patterning process is controlled by the combined action of hormonal signaling/transport pathways, transcription factors, and miRNA that operate through a series of non-linear pathways to drive pattern formation collectively. With the discovery of multiple components and feedback loops controlling patterning, it has become increasingly difficult to understand how these interactions act in unison to determine pattern formation in multicellular tissues. Three independent mathematical models of root vascular patterning have been formulated in the last few years, providing an excellent example of how theoretical approaches can complement experimental studies to provide new insights into complex systems. In many aspects these models support each other; however, each study also provides its own novel findings and unique viewpoints. Here we reconcile these models by identifying the commonalities and exploring the differences between them by testing how transferable findings are between models. New simulations herein support the hypothesis that an asymmetry in auxin input can direct the formation of vascular pattern. We show that the xylem axis can act as a sole source of cytokinin and specify the correct pattern, but also that broader patterns of cytokinin production are also able to pattern the root. By comparing the three modeling approaches, we gain further insight into vascular patterning and identify several key areas for experimental investigation.
The PLETHORA Gene Regulatory Network Guides Growth and Cell Differentiation in Arabidopsis Roots
Santuari, Luca ; Sanchez-Perez, Gabino F. ; Luijten, Marijn ; Rutjens, Bas ; Terpstra, Inez ; Berke, Lidija ; Gorte, Maartje ; Prasad, Kalika ; Bao, Dongping ; Timmermans-Hereijgers, Johanna L.P.M. ; Maeo, Kenichiro ; Nakamura, Kenzo ; Shimotohno, Akie ; Pencik, Ales ; Novak, Ondrej ; Ljung, Karin ; Heesch, Sebastiaan Van; Bruijn, Ewart De; Cuppen, Edwin ; Willemsen, Viola ; Mähönen, Ari Pekka ; Lukowitz, Wolfgang ; Snel, Berend ; Ridder, Dick De; Scheres, Ben ; Heidstra, Renze - \ 2016
The Plant Cell 28 (2016)12. - ISSN 1040-4651 - p. 2937 - 2951.
Organ formation in animals and plants relies on precise control of cell state transitions to turn stem cell daughters into fully differentiated cells. In plants, cells cannot rearrange due to shared cell walls. Thus, differentiation progression and the accompanying cell expansion must be tightly coordinated across tissues. PLETHORA (PLT) transcription factor gradients are unique in their ability to guide the progression of cell differentiation at different positions in the growing Arabidopsis thaliana root, which contrasts with well-described transcription factor gradients in animals specifying distinct cell fates within an essentially static context. To understand the output of the PLT gradient, we studied the gene set transcriptionally controlled by PLTs. Our work reveals how the PLT gradient can regulate cell state by region-specific induction of cell proliferation genes and repression of differentiation. Moreover, PLT targets include major patterning genes and autoregulatory feedback components, enforcing their role as master regulators of organ development.
Plant vascular development : From early specification to differentiation
Rybel, Bert De; Mähönen, Ari Pekka ; Helariutta, Yrjö ; Weijers, Dolf - \ 2016
Nature Reviews. Molecular Cell Biology 17 (2016)1. - ISSN 1471-0072 - p. 30 - 40.
Vascular tissues in plants are crucial to provide physical support and to transport water, sugars and hormones and other small signalling molecules throughout the plant. Recent genetic and molecular studies have identified interconnections among some of the major signalling networks that regulate plant vascular development. Using Arabidopsis thaliana as a model system, these studies enable the description of vascular development from the earliest tissue specification events during embryogenesis to the differentiation of phloem and xylem tissues. Moreover, we propose a model for how oriented cell divisions give rise to a three-dimensional vascular bundle within the root meristem.
Multisite gateway-compatible cell type-specific gene-inducible system for plants
Siligato, Riccardo ; Wang, Xin ; Yadav, Shri Ram ; Lehesranta, Satu ; Ma, Guojie ; Ursache, Robertas ; Sevilem, Iris ; Zhang, Jing ; Gorte, Maartje ; Prasad, Kalika ; Wrzaczek, Michael ; Heidstra, Renze ; Murphy, Angus ; Scheres, Ben ; Mähönen, Ari Pekka - \ 2016
Plant Physiology 170 (2016)2. - ISSN 0032-0889 - p. 627 - 641.
A powerful method to study gene function is expression or overexpression in an inducible, cell type-specific system followed by observation of consequent phenotypic changes and visualization of linked reporters in the target tissue. Multiple inducible gene overexpression systems have been developed for plants, but very few of these combine plant selection markers, control of expression domains, access to multiple promoters and protein fusion reporters, chemical induction, and high-throughput cloning capabilities. Here, we introduce a MultiSite Gateway-compatible inducible system for Arabidopsis (Arabidopsis thaliana) plants that provides the capability to generate such constructs in a single cloning step. The system is based on the tightly controlled, estrogen-inducible XVE system. We demonstrate that the transformants generated with this system exhibit the expected cell type-specific expression, similar to what is observed with constitutively expressed native promoters. With this new system, cloning of inducible constructs is no longer limited to a few special cases but can be used as a standard approach when gene function is studied. In addition, we present a set of entry clones consisting of histochemical and fluorescent reporter variants designed for gene and promoter expression studies.
Correction: Plasma membrane-bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS(N/S) motifs to direct apical PIN recycling : Correction
Dhonukshe, Pankaj ; Huang, Fang ; Galvan-Ampudia, Carlos S. ; Ma¨ho¨nen, Ari Pekka ; Kleinevehn, Jürgen ; Xu, Jian ; Quint, Ab ; Prasad, Kalika ; Friml, Jirí ; Scheres, Ben ; Offringa, Remko - \ 2015
Development 142 (2015)13. - ISSN 0950-1991 - p. 2386 - 2387.
PLETHORA gradient formation mechanism separates auxin responses
Mahonen, A.P. ; Tusscher, K. ten; Diaz Trivino, S. ; Heidstra, R. ; Scheres, B. - \ 2014
Nature 515 (2014). - ISSN 0028-0836 - p. 125 - 129.
monocyte chemoattractant protein-1 - inflammatory breast-cancer - arabidopsis root apex - stem-cell niche - transcription factors - genomics browser - carcinoma cells - tumor - angiogenesis - expression
During plant growth, dividing cells in meristems must coordinate transitions from division to expansion and differentiation, thus generating three distinct developmental zones: the meristem, elongation zone and differentiation zone1. Simultaneously, plants display tropisms, rapid adjustments of their direction of growth to adapt to environmental conditions. It is unclear how stable zonation is maintained during transient adjustments in growth direction. In Arabidopsis roots, many aspects of zonation are controlled by the phytohormone auxin and auxin-induced PLETHORA (PLT) transcription factors, both of which display a graded distribution with a maximum near the root tip2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12. In addition, auxin is also pivotal for tropic responses13, 14. Here, using an iterative experimental and computational approach, we show how an interplay between auxin and PLTs controls zonation and gravitropism. We find that the PLT gradient is not a direct, proportionate readout of the auxin gradient. Rather, prolonged high auxin levels generate a narrow PLT transcription domain from which a gradient of PLT protein is subsequently generated through slow growth dilution and cell-to-cell movement. The resulting PLT levels define the location of developmental zones. In addition to slowly promoting PLT transcription, auxin also rapidly influences division, expansion and differentiation rates. We demonstrate how this specific regulatory design in which auxin cooperates with PLTs through different mechanisms and on different timescales enables both the fast tropic environmental responses and stable zonation dynamics necessary for coordinated cell differentiation.
A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots.
Bishopp, A. ; Help, H. ; El-Showk, S. ; Weijers, D. ; Scheres, B.J.G. ; Friml, J. ; Benkova, E. ; Pekka Mahonen, A. ; Helariutta, Y. - \ 2011
Current Biology 21 (2011)11. - ISSN 0960-9822 - p. 917 - 926.
cup-shaped-cotyledon - stem-cell niche - class iiihd-zip - arabidopsis root - meristem activity - hormonal-control - gene family - embryo - efflux - embryogenesis
Background Whereas the majority of animals develop toward a predetermined body plan, plants show iterative growth and continually produce new organs and structures from actively dividing meristems. This raises an intriguing question: How are these newly developed organs patterned? In Arabidopsis embryos, radial symmetry is broken by the bisymmetric specification of the cotyledons in the apical domain. Subsequently, this bisymmetry is propagated to the root promeristem. Results Here we present a mutually inhibitory feedback loop between auxin and cytokinin that sets distinct boundaries of hormonal output. Cytokinins promote the bisymmetric distribution of the PIN-FORMED (PIN) auxin efflux proteins, which channel auxin toward a central domain. High auxin promotes transcription of the cytokinin signaling inhibitor AHP6, which closes the interaction loop. This bisymmetric auxin response domain specifies the differentiation of protoxylem in a bisymmetric pattern. In embryonic roots, cytokinin is required to translate a bisymmetric auxin response in the cotyledons to a bisymmetric vascular pattern in the root promeristem. Conclusions Our results present an interactive feedback loop between hormonal signaling and transport by which small biases in hormonal input are propagated into distinct signaling domains to specify the vascular pattern in the root meristem. It is an intriguing possibility that such a mechanism could transform radial patterns and allow continuous vascular connections between other newly emerging organs.