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.
Root branching toward water involves posttranslational modification of transcription factor ARF7
Orosa-Puente, Beatriz ; Leftley, Nicola ; Wangenheim, Daniel von; Banda, Jason ; Srivastava, Anjil K. ; Hill, Kristine ; Truskina, Jekaterina ; Bhosale, Rahul ; Morris, Emily ; Srivastava, Moumita ; Kümpers, Britta ; Goh, Tatsuaki ; Fukaki, Hidehiro ; Vermeer, Joop E.M. ; Vernoux, Teva ; Dinneny, José R. ; French, Andrew P. ; Bishopp, Anthony ; Sadanandom, Ari ; Bennett, Malcolm J. - \ 2018
Science 362 (2018)6421. - ISSN 0036-8075 - p. 1407 - 1410.
Plants adapt to heterogeneous soil conditions by altering their root architecture. For example, roots branch when in contact with water by using the hydropatterning response. We report that hydropatterning is dependent on auxin response factor ARF7. This transcription factor induces asymmetric expression of its target gene LBD16 in lateral root founder cells. This differential expression pattern is regulated by posttranslational modification of ARF7 with the small ubiquitin-like modifier (SUMO) protein. SUMOylation negatively regulates ARF7 DNA binding activity. ARF7 SUMOylation is required to recruit the Aux/IAA (indole-3-acetic acid) repressor protein IAA3. Blocking ARF7 SUMOylation disrupts IAA3 recruitment and hydropatterning. We conclude that SUMO-dependent regulation of auxin response controls root branching pattern in response to water availability.
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.
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.