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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.
AINTEGUMENTA-LIKE proteins: hubs in a plethora of networks
Horstman, A. ; Willemsen, V. ; Boutilier, K.A. ; Heidstra, R. - \ 2014
Trends in Plant Science 19 (2014)3. - ISSN 1360-1385 - p. 146 - 157.
stem-cell niche - ethylene-responsive element - lateral root initiation - homeodomain finger proteins - actin-depolymerizing factor - homeotic gene apetala2 - shoot apical meristem - dna-binding proteins - transcription factors - arabidopsis root
Members of the AINTEGUMENTA-LIKE (AIL) family of APETALA 2/ETHYLENE RESPONSE FACTOR (AP2/ERF) domain transcription factors are expressed in all dividing tissues in the plant, where they have central roles in developmental processes such as embryogenesis, stem cell niche specification, meristem maintenance, organ positioning, and growth. When overexpressed, AIL proteins induce adventitious growth, including somatic embryogenesis and ectopic organ formation. The Arabidopsis (Arabidopsis thaliana) genome contains eight AIL genes, including AINTEGUMENTA, BABY BOOM, and the PLETHORA genes. Studies on these transcription factors have revealed their intricate relationship with auxin as well as their involvement in an increasing number of gene regulatory networks, in which extensive crosstalk and feedback loops have a major role.
Unraveling Root Developmental Programs Initiated by Beneficial Pseudomonas spp. Bacteria
Zamioudis, C. ; Mastranesti, P. ; Dhonukshe, P. ; Blilou, I. ; Pieterse, C.M.J. - \ 2013
Plant Physiology 162 (2013)1. - ISSN 0032-0889 - p. 304 - 318.
induced systemic resistance - stem-cell niche - arabidopsis-thaliana root - transcription factor myc2 - auxin biosynthesis - rhizosphere microbiome - biocontrol bacteria - promote growth - ethylene - rhizobacteria
Plant roots are colonized by an immense number of microbes, referred to as the root microbiome. Selected strains of beneficial soil-borne bacteria can protect against abiotic stress and prime the plant immune system against a broad range of pathogens. Pseudomonas spp. rhizobacteria represent one of the most abundant genera of the root microbiome. Here, by employing a germfree experimental system, we demonstrate the ability of selected Pseudomonas spp. strains to promote plant growth and drive developmental plasticity in the roots of Arabidopsis (Arabidopsis thaliana) by inhibiting primary root elongation and promoting lateral root and root hair formation. By studying cell type-specific developmental markers and employing genetic and pharmacological approaches, we demonstrate the crucial role of auxin signaling and transport in rhizobacteria-stimulated changes in the root system architecture of Arabidopsis. We further show that Pseudomonas spp.-elicited alterations in root morphology and rhizobacteria-mediated systemic immunity are mediated by distinct signaling pathways. This study sheds new light on the ability of soil-borne beneficial bacteria to interfere with postembryonic root developmental programs.
Tightly controlled WRKY23 expression mediates Arabidopsis embryo development
Grunewald, W. ; Smet, I. De; Rybel, B. De; Robert, H.S. ; Cotte, B. van de; Willemsen, V.A. ; Gheysen, G. ; Weijers, D. ; Friml, J. ; Beeckman, T. - \ 2013
Embo Reports 14 (2013). - ISSN 1469-221X - p. 1136 - 1142.
stem-cell niche - transcription factor - root development - genes - axis - regulators - thaliana - proteins - encodes
The development of a multicellular embryo from a single zygote is a complex and highly organized process that is far from understood. In higher plants, apical–basal patterning mechanisms are crucial to correctly specify root and shoot stem cell niches that will sustain and drive post-embryonic plant growth and development. The auxin-responsive AtWRKY23 transcription factor is expressed from early embryogenesis onwards and the timing and localization of its expression overlaps with the root stem cell niche. Knocking down WRKY23 transcript levels or expression of a dominant-negative WRKY23 version via a translational fusion with the SRDX repressor domain affected both apical–basal axis formation as well as installation of the root stem cell niche. WRKY23 expression is affected by two well-known root stem cell specification mechanisms, that is, SHORTROOT and MONOPTEROS–BODENLOS signalling and can partially rescue the root-forming inability of mp embryos. On the basis of these results, we postulate that a tightly controlled WRKY23 expression is involved in the regulation of both auxin-dependent and auxin-independent signalling pathways towards stem cell specification.
Auxin regulation of embryonic root formation
Yoshida, S. ; Saiga, S. ; Weijers, D. - \ 2013
Plant and Cell Physiology 54 (2013)3. - ISSN 0032-0781 - p. 325 - 332.
homeodomain finger proteins - stem-cell niche - gnom arf-gef - arabidopsis embryo - transcription factor - phd-finger - vascular development - plant development - apical meristem - efflux carrier
The plant hormone auxin was initially identified as the bioactive substance that induces roots in plant tissue culture. In the past decades, mechanisms for auxin action, including its transport and response, have been described in detail. However, a molecular and cellular description of its role in root initiation is far from complete. In this review, we discuss recent advances in our understanding of auxin-dependent embryonic root formation. During this process, a root meristem is initiated in a precise and predictable position, and at a stage when the organism consists of relatively few cells. Recent studies have revealed mechanisms for local control of auxin transport, for cellular differences in auxin response components and cell type-specific chromatin regulation. The recent identification of biologically relevant target genes for auxin regulation during embryonic root initiation now also allows dissection of auxin-activated cellular processes. Finally, we discuss the potential for hormonal cross-regulation in embryonic root formation.
A PHABULOSA/Cytokinin feedback loop controls root growth in Arabidopsis
Dello loio, R. ; Galinha, C. ; Fletcher, A.G. ; Grigg, S.P. ; Molnar, A. ; Willemsen, V. ; Scheres, B. - \ 2012
Current Biology 22 (2012)18. - ISSN 0960-9822 - p. 1699 - 1704.
stem-cell niche - gene family - cytokinin - meristem - auxin - differentiation - expression - polarity - biosynthesis - nitrate
The hormone cytokinin (CK) controls root length in Arabidopsis thaliana by defining where dividing cells, derived from stem cells of the root meristem, start to differentiate. However, the regulatory inputs directing CK to promote differentiation remain poorly understood. Here, we show that the HD-ZIPIII transcription factor PHABULOSA (PHB) directly activates the CK biosynthesis gene ISOPENTENYL TRANSFERASE 7 (IPT7), thus promoting cell differentiation and regulating root length. We further demonstrate that CK feeds back to repress both PHB and microRNA165, a negative regulator of PHB. These interactions comprise an incoherent regulatory loop in which CK represses both its activator and a repressor of its activator. We propose that this regulatory circuit determines the balance of cell division and differentiation during root development and may provide robustness against CK fluctuations.
Control of embryonic meristem initiation in Arabidopsis by PHD-finger protein complexes.
Saiga, S. ; Moller, B.K. ; Watanabe-Taneda, A. ; Abe, M. ; Weijers, D. ; Komeda, Y. - \ 2012
Development 139 (2012). - ISSN 0950-1991 - p. 1391 - 1398.
stem-cell niche - plant homeodomain - transcription factor - histone h3k4me3 - root-meristem - chromatin - thaliana - scarecrow - h3 - trimethylation
Plant growth is directed by the activity of stem cells within meristems. The first meristems are established during early embryogenesis, and this process involves the specification of both stem cells and their organizer cells. One of the earliest events in root meristem initiation is marked by re-specification of the uppermost suspensor cell as hypophysis, the precursor of the organizer. The transcription factor MONOPTEROS (MP) is a key regulator of hypophysis specification, and does so in part by promoting the transport of the plant hormone auxin and by activating the expression of TARGET OF MP (TMO) transcription factors, both of which are required for hypophysis specification. The mechanisms leading to the activation of these genes by MP in a chromatin context are not understood. Here, we show that the PHD-finger proteins OBERON (OBE) and TITANIA (TTA) are essential for MP-dependent embryonic root meristem initiation. TTA1 and TTA2 are functionally redundant and function in the same pathway as OBE1 and OBE2. These PHD-finger proteins interact with each other, and genetic analysis shows that OBE-TTA heterotypic protein complexes promote embryonic root meristem initiation. Furthermore, while MP expression is unaffected by mutations in OBE/TTA genes, expression of MP targets TMO5 and TMO7 is locally lost in obe1 obe2 embryos. PHD-finger proteins have been shown to act in initiation of transcription by interacting with nucleosomes. Indeed, we found that OBE1 binds to chromatin at the TMO7 locus, suggesting a role in its MP-dependent activation. Our data indicate that PHD-finger protein complexes are crucial for the activation of MP-dependent gene expression during embryonic root meristem initiation, and provide a starting point for studying the mechanisms of developmental gene activation within a chromatin context in plants.
POPCORN Functions in the Auxin Pathway to Regulate Embryonic Body Plan and Meristem Organization in Arabidopsis
Xiang, D.Q. ; Yang, H. ; Venglat, P. ; Cao, Y.G. ; Wen, R. ; Ren, M.Z. ; Stone, S. ; Wang, E. ; Wang, H. ; Xiao, W. ; Weijers, D. ; Berleth, T. ; Laux, T. ; Selvaraj, G. ; Datla, R. - \ 2011
The Plant Cell 23 (2011)12. - ISSN 1040-4651 - p. 4348 - 4367.
stem-cell niche - cup-shaped-cotyledon - shoot meristem - wild-type - gene - embryogenesis - wuschel - fate - monopteros - thaliana
The shoot and root apical meristems (SAM and RAM) formed during embryogenesis are crucial for postembryonic plant development. We report the identification of POPCORN (PCN), a gene required for embryo development and meristem organization in Arabidopsis thaliana. Map-based cloning revealed that PCN encodes a WD-40 protein expressed both during embryo development and postembryonically in the SAM and RAM. The two pcn alleles identified in this study are temperature sensitive, showing defective embryo development when grown at 22 degrees C that is rescued when grown at 29 degrees C. In pcn mutants, meristem-specific expression of WUSCHEL (WUS), CLAVATA3, and WUSCHEL-RELATED HOMEOBOX5 is not maintained; SHOOTMERISTEMLESS, BODENLOS (BDL) and MONOPTEROS (MP) are misexpressed. Several findings link PCN to auxin signaling and meristem function: ectopic expression of DR5(rev):green fluorescent protein (GFP), pBDL:BDL-GFP, and pMP:MP-beta-glucuronidase in the meristem; altered polarity and expression of pPIN1:PIN1-GFP in the apical domain of the developing embryo; and resistance to auxin in the pcn mutants. The bdl mutation rescued embryo lethality of pcn, suggesting that improper auxin response is involved in pcn defects. Furthermore, WUS, PINFORMED1, PINOID, and TOPLESS are dosage sensitive in pcn, suggesting functional interaction. Together, our results suggest that PCN functions in the auxin pathway, integrating auxin signaling in the organization and maintenance of the SAM and RAM.
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.
Regulation of transcription in plants: mechanisms controlling developmental switches.
Kaufmann, K. ; Pajoro, A. ; Angenent, G.C. - \ 2010
Nature Reviews Genetics 11 (2010). - ISSN 1471-0056 - p. 830 - 842.
floral organ identity - shoot apical meristem - flowering-time genes - stem-cell niche - adaxial-abaxial polarity - polycomb-group proteins - short-vegetative-phase - mads-box proteins - arabidopsis-thaliana - reproductive development
Unlike animals, plants produce new organs throughout their life cycle using pools of stem cells that are organized in meristems. Although many key regulators of meristem and organ identities have been identified, it is still not well understood how they function at the molecular level and how they can switch an entire developmental programme in which thousands of genes are involved. Recent advances in the genome-wide identification of target genes controlled by key plant transcriptional regulators and their interactions with epigenetic factors provide new insights into general transcriptional regulatory mechanisms that control switches of developmental programmes and cell fates in complex organisms.