Symmetry formation is a remarkable feature of biological life forms associated with evolutionary advantages and often with great beauty. Several examples exist in which organisms undergo a transition ...in symmetry during development 1–4. Such transitions are almost exclusively in the direction from radial to bilateral symmetry 5–8. Here, we describe the dynamics of symmetry establishment during development of the Arabidopsis gynoecium. We show that the apical style region undergoes an unusual transition from a bilaterally symmetric stage ingrained in the gynoecium due to its evolutionary origin to a radially symmetric structure. We also identify two transcription factors, INDEHISCENT 9 and SPATULA 10, that are both necessary and sufficient for the radialization process. Our work furthermore shows that these two transcription factors control style symmetry by directly regulating auxin distribution. Establishment of specific auxin-signaling foci and the subsequent development of a radially symmetric auxin ring at the style are required for the transition to radial symmetry, because genetic manipulations of auxin transport can either cause loss of radialization in a wild-type background or rescue mutants with radialization defects. Whereas many examples have described how auxin provides polarity and specific identity to cells in a range of developmental contexts, our data presented here demonstrate that auxin can also be recruited to impose uniform identity to a group of cells that are otherwise differentially programmed.
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•Apex of the Arabidopsis gynoecium undergoes a bilateral-to-radial symmetry transition•Transcription factors IND/SPT are necessary and sufficient for organ radialization•IND and SPT regulate auxin transport to achieve radial symmetry•Spatiotemporal auxin dynamics control growth and symmetry of the gynoecium
Symmetry transitions in nature are common and occur almost exclusively via a change from radial to bilateral symmetry. Here, Moubayidin and Østergaard reveal how control of auxin transport by SPATULA and INDEHISCENT imposes a rare bilateral-to-radial symmetry switch during Arabidopsis gynoecium development.
Abstract
Symmetry establishment is a critical process in the development of multicellular organs and requires careful coordination of polarity axes while cells actively divide within tissues. ...Formation of the apical style in the Arabidopsis gynoecium involves a bilateral-to-radial symmetry transition, a stepwise process underpinned by the dynamic distribution of the plant morphogen auxin. Here we show that SPATULA (SPT) and the HECATE (HEC) bHLH proteins mediate the final step in the style radialisation process and synergistically control the expression of adaxial-identity genes,
HOMEOBOX ARABIDOPSIS THALIANA 3
(
HAT3
) and
ARABIDOPSIS THALIANA HOMEOBOX 4
(
ATHB4
). HAT3/ATHB4 module drives radialisation of the apical style by promoting basal-to-apical auxin flow and via a negative feedback mechanism that finetune auxin distribution through repression of
SPT
expression and cytokinin sensitivity. Thus, this work reveals the molecular basis of axes-coordination and hormonal cross-talk during the sequential steps of symmetry transition in the Arabidopsis style.
Upon seed germination, apical meristems grow as cell division prevails over differentiation and reach their final size when division and differentiation reach a balance. In the Arabidopsis root ...meristem, this balance results from the interaction between cytokinin (promoting differentiation) 1–4 and auxin (promoting division) 2, 5 through a regulatory circuit whereby the ARR1 cytokinin-responsive transcription factor 6 activates the gene SHY2 2, 6, 7, which negatively regulates the PIN genes encoding auxin transport facilitators 2, 5. However, it remains unknown how the final meristem size is set, i.e., how a change in the relative rates of cell division and differentiation is brought about to cause meristem growth to stop. Here, we show that during meristem growth, expression of SHY2 is driven by another cytokinin-response factor, ARR12 1, and that completion of growth is brought about by the upregulation of SHY2 caused by both ARR12 and ARR1: this leads to an increase in cell differentiation rate that balances it with division, thus setting root meristem size. We also show that gibberellins selectively repress expression of ARR1 at early stages of meristem development, and that the DELLA protein REPRESSOR OF GA 1-3 (RGA) 8 mediates this negative control.
► Cell differentiation increases during root meristem growth and balances cell division ► SHY2 level increases during root meristem growth and enhances cell differentiation ► High levels of SHY2, depending on both ARR1 and ARR12, set root meristem size ► Gibberellins antagonize the cytokinin cell differentiation input by repressing ARR1
Plant growth and development are sustained by meristems. Meristem activity is controlled by auxin and cytokinin, two hormones whose interactions in determining a specific developmental output are ...still poorly understood. By means of a comprehensive genetic and molecular analysis in Arabidopsis, we show that a primary cytokinin-response transcription factor, ARR1, activates the gene SHY2/IAA3 (SHY2), a repressor of auxin signaling that negatively regulates the PIN auxin transport facilitator genes: thereby, cytokinin causes auxin redistribution, prompting cell differentiation. Conversely, auxin mediates degradation of the SHY2 protein, sustaining PIN activities and cell division. Thus, the cell differentiation and division balance necessary for controlling root meristem size and root growth is the result of the interaction between cytokinin and auxin through a simple regulatory circuit converging on the SHY2 gene.
Symmetry matters Moubayidin, Laila; Østergaard, Lars
The New phytologist,
September 2015, Letnik:
207, Številka:
4
Journal Article
Recenzirano
The development of multicellular organisms depends on correct establishment of symmetry both at the whole-body scale and within individual tissues and organs. Setting up planes of symmetry must rely ...on communication between cells that are located at a distance from each other within the organism, presumably via mobile morphogenic signals. Although symmetry in nature has fascinated scientists for centuries, it is only now that molecular data to unravel mechanisms of symmetry establishment are beginning to emerge. As an example we describe the genetic and hormonal interactions leading to an unusual bilateral-to-radial symmetry transition of an organ in order to promote reproduction.
Flowers are plant structures characteristic of the phylum Angiosperms composed of organs thought to have emerged from homologous structures to leaves in order to specialize in a distinctive function: ...reproduction. Symmetric shapes, colours, and scents all play important functional roles in flower biology. The evolution of flower symmetry and the morphology of individual flower parts (sepals, petals, stamens, and carpels) has significantly contributed to the diversity of reproductive strategies across flowering plant species. This diversity facilitates attractiveness for pollination, protection of gametes, efficient fertilization, and seed production. Symmetry, the establishment of body axes, and fate determination are tightly linked. The complex genetic networks underlying the establishment of organ, tissue, and cellular identity, as well as the growth regulators acting across the body axes, are steadily being elucidated in the field. In this review, we summarise the wealth of research already at our fingertips to begin weaving together how separate processes involved in specifying organ identity within the flower may interact, providing a functional perspective on how identity determination and axial regulation may be coordinated to inform symmetrical floral organ structures.
Cullin-RING E3 ligases （CRLs） regulate different aspects of plant development and are activated by modification of their cullin subunit with the ubiquitin-like protein NEDD8 （NEural precursor cell ...expressed Developmentally Down-regulated 8） （neddylation） and deactivated by NEDD8 removal （deneddylation）. The CONSTITUTIVELY PHOTOMORPHOGENIC9 （COP9） signalosome （CSN） acts as a molecular switch of CRLs activity by reverting their neddylation status, but its contribution to embryonic and early seedling development remains poorly characterized. Here, we analyzed the phenotypic defects of csn mutants and monitored the cullin deneddylation/neddylation ratio during embryonic and early seedling development. We show that while csn mutants can complete embryogenesis （albeit at a slower pace than wildtype） and are able to germinate （albeit at a reduced rate）, they progressively lose meristem activity upon germination until they become unable to sustain growth. We also show that the majority of cullin proteins are progressively neddylated during the late stages of seed maturation and become deneddylated upon seed germination. This developmentally regulated shift in the cullin neddylation status is absent in csn mutants. We conclude that the CSN and its cullin deneddylation activity are required to sustain postembryonic meristem function in Arabidopsis.
Cytokinin–auxin crosstalk Moubayidin, Laila; Di Mambro, Riccardo; Sabatini, Sabrina
Trends in plant science,
10/2009, Letnik:
14, Številka:
10
Journal Article
Recenzirano
Post-embryonic plant growth and development are sustained by meristems, a source of undifferentiated cells that give rise to the adult plant structures. Two hormones, cytokinin and auxin, are known ...to act antagonistically in controlling meristem activities. Here, we review recent significant progress in elucidating the molecular mechanisms through which these hormones interact to control specific aspects of plant development. For example, in the root meristem of
Arabidopsis thaliana, cytokinin promotes cell differentiation by repressing both auxin signalling and transport, whereas auxin sustains root meristem activity by promoting cell division. The coordinated action of these two hormones is essential for maintaining root meristem size and for ensuring root growth.
The molecular basis of cytokinin function Perilli, Serena; Moubayidin, Laila; Sabatini, Sabrina
Current opinion in plant biology,
02/2010, Letnik:
13, Številka:
1
Journal Article
Recenzirano
Cytokinins are a class of phytohormones that regulate a wide variety of physiological and developmental processes such as shoot and root growth. Cytokinin signaling relies on a phosphorelay mechanism ...similar to the prokaryotic two-component system. Although the principal components mediating this cascade have been identified, only recently have we begun to understand the molecular basis of cytokinin action. For example cytokinins control cell differentiation rate during root meristem development by suppressing both auxin signaling and transport, whereas at early stages of embryo development auxin counteracts cytokinin signaling to establish the embryonic root stem-cell niche. The antagonistic interaction between cytokinins and auxin seems to also occur in other developmental processes, such as lateral root emergence and leaf initiation.
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