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1.
Proc Natl Acad Sci U S A ; 121(29): e2320470121, 2024 Jul 16.
Article in English | MEDLINE | ID: mdl-38990951

ABSTRACT

Although the formation of new walls during plant cell division tends to follow maximal tensile stress direction, analyses of individual cells over time reveal a much more variable behavior. The origin of such variability as well as the exact role of interphasic microtubule behavior before cell division have remained mysterious so far. To approach this question, we took advantage of the Arabidopsis stem, where the tensile stress pattern is both highly anisotropic and stable. Although cortical microtubules (CMTs) generally align with maximal tensile stress, we detected a specific time window, ca. 3 h before cell division, where cells form a radial pattern of CMTs. This microtubule array organization preceded preprophase band (PPB) formation, a transient CMT array predicting the position of the future division plane. It was observed under different growth conditions and was not related to cell geometry or polar auxin transport. Interestingly, this cortical radial pattern correlated with the well-documented increase of cytoplasmic microtubule accumulation before cell division. This radial organization was prolonged in cells of the trm678 mutant, where CMTs are unable to form a PPB. Whereas division plane orientation in trm678 is noisier, we found that cell division symmetry was in contrast less variable between daughter cells. We propose that this "radial step" reflects a trade-off in robustness for two essential cell division attributes: symmetry and orientation. This involves a "reset" stage in G2, where an increased cytoplasmic microtubule accumulation transiently disrupts CMT alignment with tissue stress.


Subject(s)
Arabidopsis Proteins , Arabidopsis , Cell Division , Microtubules , Arabidopsis/metabolism , Arabidopsis/cytology , Microtubules/metabolism , Cell Division/physiology , Arabidopsis Proteins/metabolism , Arabidopsis Proteins/genetics , Indoleacetic Acids/metabolism
2.
Biol Lett ; 20(5): 20240099, 2024 May.
Article in English | MEDLINE | ID: mdl-38807547

ABSTRACT

How organisms produce organs with robust shapes and sizes is still an open question. In recent years, the Arabidopsis sepal has been used as a model system to study this question because of its highly reproducible shape and size. One interesting aspect of the sepal is that its epidermis contains cells of very different sizes. Previous reports have qualitatively shown that sepals with more or less giant cells exhibit comparable final size and shape. Here, we investigate this question using quantitative approaches. We find that a mixed population of cell size modestly contribute to the normal width of the sepal but is not essential for its shape robustness. Furthermore, in a mutant with increased cell and organ growth variability, the change in final sepal shape caused by giant cells is exaggerated but the shape robustness is not affected. This formally demonstrates that sepal shape variability is robust to cell size heterogeneity.


Subject(s)
Arabidopsis , Cell Size , Flowers , Arabidopsis/anatomy & histology , Arabidopsis/growth & development , Arabidopsis/cytology , Flowers/anatomy & histology , Flowers/growth & development , Plant Epidermis/cytology , Mutation
3.
Proc Natl Acad Sci U S A ; 120(30): e2302441120, 2023 07 25.
Article in English | MEDLINE | ID: mdl-37459526

ABSTRACT

To relate gene networks and organ shape, one needs to address two wicked problems: i) Gene expression is often variable locally, and shape is reproducible globally; ii) gene expression can have cascading effects on tissue mechanics, with possibly counterintuitive consequences for the final organ shape. Here, we address such wicked problems, taking advantage of simpler plant organ development where shape only emerges from cell division and elongation. We confirm that mutation in VERNALIZATION INDEPENDENCE 3 (VIP3), a subunit of the conserved polymerase-associated factor 1 complex (Paf1C), increases gene expression variability in Arabidopsis. Then, we focused on the Arabidopsis sepal, which exhibits a reproducible shape and stereotypical regional growth patterns. In vip3 sepals, we measured higher growth heterogeneity between adjacent cells. This even culminated in the presence of negatively growing cells in specific growth conditions. Interestingly, such increased local noise interfered with the stereotypical regional pattern of growth. We previously showed that regional differential growth at the wild-type sepal tip triggers a mechanical conflict, to which cells resist by reinforcing their walls, leading to growth arrest. In vip3, the disturbed regional growth pattern delayed organ growth arrest and increased final organ shape variability. Altogether, we propose that gene expression variability is managed by Paf1C to ensure organ robustness by building up mechanical conflicts at the regional scale, instead of the local scale.


Subject(s)
Arabidopsis Proteins , Arabidopsis , Arabidopsis/metabolism , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Cell Division , Cell Proliferation , Nucleotidyltransferases/metabolism , Gene Expression
4.
Curr Biol ; 31(3): R143-R159, 2021 02 08.
Article in English | MEDLINE | ID: mdl-33561417

ABSTRACT

Plants produce organs of various shapes and sizes. While much has been learned about genetic regulation of organogenesis, the integration of mechanics in the process is also gaining attention. Here, we consider the role of forces as instructive signals in organ morphogenesis. Turgor pressure is the primary cause of mechanical signals in developing organs. Because plant cells are glued to each other, mechanical signals act, in essence, at multiple scales, through cell wall contiguity and water flux. In turn, cells use such signals to resist mechanical stress, for instance, by reinforcing their cell walls. We show that the three elemental shapes behind plant organs - spheres, cylinders and lamina - can be actively maintained by such a mechanical feedback. Combinations of this 3-letter alphabet can generate more complex shapes. Furthermore, mechanical conflicts emerge at the boundary between domains exhibiting different growth rates or directions. These secondary mechanical signals contribute to three other organ shape features - folds, shape reproducibility and growth arrest. The further integration of mechanical signals with the molecular network offers many fruitful prospects for the scientific community, including the role of proprioception in organ shape robustness or the definition of cell and organ identities as a result of an interplay between biochemical and mechanical signals.


Subject(s)
Plant Development , Plants , Biomechanical Phenomena , Cell Wall , Plant Cells , Reproducibility of Results , Stress, Mechanical
5.
Plant Cell ; 31(12): 3033-3056, 2019 12.
Article in English | MEDLINE | ID: mdl-31591161

ABSTRACT

Members of SEPALLATA (SEP) and APETALA1 (AP1)/SQUAMOSA (SQUA) MADS-box transcription factor subfamilies play key roles in floral organ identity determination and floral meristem determinacy in the rosid species Arabidopsis (Arabidopsis thaliana). Here, we present a functional characterization of the seven SEP/AGL6 and four AP1/SQUA genes in the distant asterid species petunia (Petunia × hybrida). Based on the analysis of single and higher order mutants, we report that the petunia SEP1/SEP2/SEP3 orthologs together with AGL6 encode classical SEP floral organ identity and floral termination functions, with a master role for the petunia SEP3 ortholog FLORAL BINDING PROTEIN2 (FBP2). By contrast, the FBP9 subclade members FBP9 and FBP23, for which no clear ortholog is present in Arabidopsis, play a major role in determining floral meristem identity together with FBP4, while contributing only moderately to floral organ identity. In turn, the four members of the petunia AP1/SQUA subfamily redundantly are required for inflorescence meristem identity and act as B-function repressors in the first floral whorl, together with BEN/ROB genes. Overall, these data together with studies in other species suggest major differences in the functional diversification of the SEP/AGL6 and AP1/SQUA MADS-box subfamilies during angiosperm evolution.plantcell;31/12/3033/FX1F1fx1.


Subject(s)
Arabidopsis/genetics , Flowers/genetics , Gene Expression Regulation, Plant/genetics , MADS Domain Proteins/genetics , Period Circadian Proteins/genetics , Petunia/genetics , Arabidopsis/metabolism , Flowers/ultrastructure , MADS Domain Proteins/metabolism , Magnoliopsida/genetics , Magnoliopsida/metabolism , Meristem/genetics , Meristem/metabolism , Mutation , Period Circadian Proteins/metabolism , Petunia/metabolism , Phenotype , Phylogeny , Plant Proteins/genetics , Plant Proteins/metabolism
6.
Development ; 146(20)2019 10 25.
Article in English | MEDLINE | ID: mdl-31540913

ABSTRACT

Although accumulating evidence suggests that gene regulation is highly stochastic, genetic screens have successfully uncovered master developmental regulators, questioning the relationship between transcriptional noise and intrinsic robustness of development. To identify developmental modules that are more or less resilient to large-scale genetic perturbations, we used the Arabidopsis polymerase II-associated factor 1 complex (Paf1c) mutant vip3, which is impaired in several RNA polymerase II-dependent transcriptional processes. We found that the control of flower termination was not as robust as classically pictured. In angiosperms, the floral female organs, called carpels, display determinate growth: their development requires the arrest of stem cell maintenance. In vip3 mutant flowers, carpels displayed a highly variable morphology, with different degrees of indeterminacy defects up to wild-type size inflorescence emerging from carpels. This phenotype was associated with variable expression of two key regulators of flower termination and stem cell maintenance in flowers, WUSCHEL and AGAMOUS The phenotype was also dependent on growth conditions. Together, these results highlight the surprisingly plastic nature of stem cell maintenance in plants and its dependence on Paf1c.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/metabolism , Flowers/metabolism , Meristem/metabolism , Arabidopsis/cytology , Arabidopsis/genetics , Arabidopsis Proteins/genetics , Flowers/cytology , Flowers/genetics , Gene Expression Regulation, Plant/genetics , Gene Expression Regulation, Plant/physiology , In Situ Hybridization , Microscopy, Confocal
7.
FEBS Open Bio ; 8(10): 1636-1648, 2018 Oct.
Article in English | MEDLINE | ID: mdl-30338215

ABSTRACT

The nucleoplasm and nucleolus are the two main territories of the nucleus. While specific functions are associated with each of these territories (such as mRNA synthesis in the nucleoplasm and ribosomal rRNA synthesis in the nucleolus), some proteins are known to be located in both. Here, we investigated the molecular function of REBELOTE (RBL), an Arabidopsis thaliana protein previously characterized as a regulator of floral meristem termination. We show that RBL displays a dual localization, in the nucleolus and nucleoplasm. Moreover, we used direct and global approaches to demonstrate that RBL interacts with nucleic acid-binding proteins. It binds to the NOC proteins SWA2, AtNOC2 and AtNOC3 in both the nucleolus and nucleoplasm, and also to OBE1 and VFP3/ENAP1. Taking into account the identities of these RBL interactors, we hypothesize that RBL acts both in ribosomal biogenesis and in the regulation of gene expression.

8.
Plant Cell ; 30(9): 2020-2037, 2018 09.
Article in English | MEDLINE | ID: mdl-30087206

ABSTRACT

To attract insects, flowers produce nectar, an energy-rich substance secreted by specialized organs called nectaries. For Arabidopsis thaliana, a rosid species with stamen-associated nectaries, the floral B-, C-, and E-functions were proposed to redundantly regulate nectary development. Here, we investigated the molecular basis of carpel-associated nectary development in the asterid species petunia (Petunia hybrida). We show that its euAGAMOUS (euAG) and PLENA (PLE) C-lineage MADS box proteins are essential for nectary development, while their overexpression is sufficient to induce ectopic nectaries on sepals. Furthermore, we demonstrate that Arabidopsis nectary development also fully depends on euAG/PLE C-lineage genes. In turn, we show that petunia nectary development depends on two homologs of CRABS CLAW (CRC), a gene previously shown to be required for Arabidopsis nectary development, and demonstrate that CRC expression in both species depends on the members of both euAG/PLE C-sublineages. Therefore, petunia and Arabidopsis employ a similar molecular mechanism underlying nectary development, despite otherwise major differences in the evolutionary trajectory of their C-lineage genes, their distant phylogeny, and different nectary positioning. However, unlike in Arabidopsis, petunia nectary development is position independent within the flower. Finally, we show that the TARGET OF EAT-type BLIND ENHANCER and APETALA2-type REPRESSOR OF B-FUNCTION genes act as major regulators of nectary size.


Subject(s)
Arabidopsis/growth & development , Arabidopsis/metabolism , Flowers/growth & development , Flowers/metabolism , Petunia/growth & development , Petunia/metabolism , Arabidopsis/genetics , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Flowers/genetics , Gene Expression Regulation, Plant , Petunia/genetics , Plant Proteins/genetics , Plant Proteins/metabolism , Transcription Factors/genetics , Transcription Factors/metabolism
9.
Plant Cell ; 29(7): 1605-1621, 2017 Jul.
Article in English | MEDLINE | ID: mdl-28646074

ABSTRACT

The ABC model is widely used as a genetic framework for understanding floral development and evolution. In this model, the A-function is required for the development of sepals and petals and to antagonize the C-function in the outer floral whorls. In the rosid species Arabidopsis thaliana, the AP2-type AP2 transcription factor represents a major A-function protein, but how the A-function is encoded in other species is not well understood. Here, we show that in the asterid species petunia (Petunia hybrida), AP2B/BLIND ENHANCER (BEN) confines the C-function to the inner petunia floral whorls, in parallel with the microRNA BLINDBEN belongs to the TOE-type AP2 gene family, members of which control flowering time in Arabidopsis. In turn, we demonstrate that the petunia AP2-type REPRESSOR OF B-FUNCTION (ROB) genes repress the B-function (but not the C-function) in the first floral whorl, together with BEN We propose a combinatorial model for patterning the B- and C-functions, leading to the homeotic conversion of sepals into petals, carpels, or stamens, depending on the genetic context. Combined with earlier results, our findings suggest that the molecular mechanisms controlling the spatial restriction of the floral organ identity genes are more diverse than the well-conserved B and C floral organ identity functions.


Subject(s)
Arabidopsis/physiology , Flowers/physiology , Gene Expression Regulation, Plant , Petunia/physiology , Plant Proteins/genetics , Arabidopsis/genetics , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Genome, Plant , Homeodomain Proteins/genetics , Mutation , Nuclear Proteins/genetics , Petunia/genetics , Phenotype , Phylogeny , Plant Proteins/metabolism , Species Specificity , Transcription Factors/genetics , Transcription Factors/metabolism
10.
Ann Bot ; 117(5): 905-23, 2016 04.
Article in English | MEDLINE | ID: mdl-27098089

ABSTRACT

BACKGROUND AND AIMS: SUPERMAN is a cadastral gene controlling the sexual boundary in the flower. The gene's functions and role in flower development and evolution have remained elusive. The analysis of a contrasting SUP allelic series (for which the names superman, superwoman and supersex have been coined) makes it possible to distinguish early vs. late regulatory processes at the flower meristem centre to which SUP is an important contributor. Their understanding is essential in further addressing evolutionary questions linking bisexuality and flower meristem homeostasis. METHODS: Inter-allelic comparisons were carried out and SUP interactions with other boundary factors and flower meristem patterning and homeostasis regulators (such as CLV, WUS, PAN, CUC, KNU, AG, AP3/PI, CRC and SPT) have been evaluated at genetic, molecular, morphological and histological levels. KEY RESULTS: Early SUP functions include mechanisms of male-female (sexual) boundary specification, flower mersitem termination and control of stamen number. A SUP-dependent flower meristem termination pathway is identified and analysed. Late SUP functions play a role in organ morphogenesis by controlling intra-whorl organ separation and carpel medial region formation. By integrating early and late SUP functions, and by analyzing in one single experiment a series of SUP genetic interactions, the concept of meristematic 'transference' (cascade) - a regulatory bridging process redundantly and sequentially co-ordinating the triggering and completion of flower meristem termination, and carpel margin meristem and placenta patterning - is proposed. CONCLUSIONS: Taken together, the results strongly support the view that SUP(-type) function(s) have been instrumental in resolving male/female gradients into sharp male and female identities (whorls, organs) and in enforcing flower homeostasis during evolution. This has probably been achieved by incorporating the meristem patterning system of the floral axis into the female/carpel programme.


Subject(s)
Arabidopsis Proteins/genetics , Arabidopsis/genetics , Flowers/growth & development , Meristem/growth & development , Transcription Factors/genetics , Alleles , Arabidopsis/growth & development , Arabidopsis Proteins/metabolism , Carrier Proteins/genetics , Crosses, Genetic , DNA-Binding Proteins/genetics , Flowers/genetics , Gene Expression Regulation, Plant , MADS Domain Proteins/genetics , Meristem/genetics , Mutation , Plants, Genetically Modified , Transcription Factors/metabolism
11.
Development ; 143(7): 1108-19, 2016 Apr 01.
Article in English | MEDLINE | ID: mdl-26903506

ABSTRACT

Higher plants continuously and iteratively produce new above-ground organs in the form of leaves, stems and flowers. These organs arise from shoot apical meristems whose homeostasis depends on coordination between self-renewal of stem cells and their differentiation into organ founder cells. This coordination is stringently controlled by the central transcription factor WUSCHEL (WUS), which is both necessary and sufficient for stem cell specification in Arabidopsis thaliana ULTRAPETALA1 (ULT1) was previously identified as a plant-specific, negative regulator of WUS expression. However, molecular mechanisms underlying this regulation remain unknown. ULT1 protein contains a SAND putative DNA-binding domain and a B-box, previously proposed as a protein interaction domain in eukaryotes. Here, we characterise a novel partner of ULT1, named ULT1 INTERACTING FACTOR 1 (UIF1), which contains a Myb domain and an EAR motif. UIF1 and ULT1 function in the same pathway for regulation of organ number in the flower. Moreover, UIF1 displays DNA-binding activity and specifically binds to WUS regulatory elements. We thus provide genetic and molecular evidence that UIF1 and ULT1 work together in floral meristem homeostasis, probably by direct repression of WUS expression.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/growth & development , Homeodomain Proteins/metabolism , Meristem/growth & development , Morphogenesis/physiology , Transcription Factors/metabolism , Amino Acid Sequence , Arabidopsis Proteins/genetics , Electrophoretic Mobility Shift Assay , Flowers/growth & development , Gene Expression Regulation, Plant , Molecular Sequence Data , Plant Leaves/growth & development , Plant Stems/growth & development , Protein Interaction Domains and Motifs , Protein Structure, Tertiary , Sequence Alignment , Stem Cells/cytology , Transcription Factors/genetics , Transcription, Genetic/genetics
12.
J Exp Bot ; 66(21): 6905-16, 2015 Nov.
Article in English | MEDLINE | ID: mdl-26269626

ABSTRACT

Plant meristems harbour stem cells, which allow for the continuous production of new organs. Here, an analysis of the role of SQUINT (SQN) in stem cell dynamics in Arabidopsis is reported. A close examination of sqn mutants reveals defects that are very similar to that of weak clavata (clv) mutants, both in the flower meristem (increased number of floral organs, occasional delay in stem cell termination) and in the shoot apical meristem (meristem and central zone enlargement, occasional fasciation). sqn has a very mild effect in a clv mutant background, suggesting that SQN and the CLV genes act in the same genetic pathway. Accordingly, a loss-of-function allele of SQN strongly rescues the meristem abortion phenotype of plants that overexpress CLV3. Altogether, these data suggest that SQN is necessary for proper CLV signalling. SQN was shown to be required for normal accumulation of various miRNAs, including miR172. One of the targets of miR172, APETALA2 (AP2), antagonizes CLV signalling. The ap2-2 mutation strongly suppresses the meristem phenotypes of sqn, indicating that the effect of SQN on stem cell dynamics is largely, but not fully, mediated by the miR172/AP2 tandem. This study refines understanding of the intricate genetic networks that control both stem cell homeostasis and floral stem cell termination, two processes that are critical for the proper development and fertility of the plant.


Subject(s)
Arabidopsis Proteins/genetics , Arabidopsis/physiology , Cyclophilins/genetics , Gene Expression Regulation, Plant , Homeodomain Proteins/genetics , Nuclear Proteins/genetics , Arabidopsis/genetics , Arabidopsis/growth & development , Arabidopsis Proteins/metabolism , Cyclophilins/metabolism , Flowers/growth & development , Gene Expression Regulation, Developmental , Homeodomain Proteins/metabolism , Homeostasis , Meristem/growth & development , MicroRNAs/genetics , MicroRNAs/metabolism , Nuclear Proteins/metabolism , Signal Transduction , Stem Cells/physiology
13.
Ann Bot ; 114(7): 1545-53, 2014 Nov.
Article in English | MEDLINE | ID: mdl-24973416

ABSTRACT

BACKGROUND: WOX (Wuschel-like homeobOX) genes form a family of plant-specific HOMEODOMAIN transcription factors, the members of which play important developmental roles in a diverse range of processes. WOX genes were first identified as determining cell fate during embryo development, as well as playing important roles in maintaining stem cell niches in the plant. In recent years, new roles have been identified in plant architecture and organ development, particularly at the flower level. SCOPE: In this review, the role of WOX genes in flower development and flower architecture is highlighted, as evidenced from data obtained in the last few years. The roles played by WOX genes in different species and different flower organs are compared, and differential functional recruitment of WOX genes during flower evolution is considered. CONCLUSIONS: This review compares available data concerning the role of WOX genes in flower and organ architecture among different species of angiosperms, including representatives of monocots and eudicots (rosids and asterids). These comparative data highlight the usefulness of the WOX gene family for evo-devo studies of floral development.


Subject(s)
Flowers/genetics , Homeodomain Proteins/metabolism , Magnoliopsida/genetics , Arabidopsis/anatomy & histology , Arabidopsis/genetics , Arabidopsis/growth & development , Arabidopsis/metabolism , Flowers/anatomy & histology , Flowers/growth & development , Flowers/metabolism , Homeodomain Proteins/genetics , Magnoliopsida/anatomy & histology , Magnoliopsida/growth & development , Magnoliopsida/metabolism , Phylogeny , Plant Leaves/anatomy & histology , Plant Leaves/genetics , Plant Leaves/growth & development , Plant Leaves/metabolism , Plant Proteins/genetics , Plant Proteins/metabolism , Transcription Factors/genetics , Transcription Factors/metabolism
14.
Development ; 140(23): 4807-17, 2013 Dec.
Article in English | MEDLINE | ID: mdl-24173806

ABSTRACT

Organ morphogenesis largely relies on cell division and elongation, which need to be both coordinated between cells and orchestrated with cytoskeleton dynamics. However, components that bridge the biological signals and the effectors that define cell shape remain poorly described. We have addressed this issue through the functional characterisation of QUIRKY (QKY), previously isolated as being involved in the STRUBBELIG (SUB) genetic pathway that controls cell-cell communication and organ morphogenesis in Arabidopsis. QKY encodes a protein containing multiple C2 domains and transmembrane regions, and SUB encodes an atypical LRR-receptor-like kinase. We show that twisting of the gynoecium observed in qky results from the abnormal division pattern and anisotropic growth of clustered cells arranged sporadically along the gynoecium. Moreover, the cortical microtubule (CMT) network of these cells is disorganised. A cross to botero, a katanin mutant in which the normal orientation of CMTs and anisotropic cell expansion are impaired, strongly reduces silique deviation, reinforcing the hypothesis of a role for QKY in CMT-mediated cell growth anisotropy. We also show that QKY is localised at the plasma membrane and functions in a multiprotein complex that includes SUB and PAL OF QUIRKY (POQ), a previously uncharacterised PB1-domain-containing protein that localises both at the plasma membrane and in intracellular compartments. Our data indicate that QKY and its interactors play central roles linking together cell-cell communication and cellular growth.


Subject(s)
Arabidopsis Proteins/metabolism , Arabidopsis/embryology , Carrier Proteins/metabolism , Membrane Proteins/metabolism , Receptor Protein-Tyrosine Kinases/metabolism , Amino Acid Sequence , Anisotropy , Arabidopsis/genetics , Arabidopsis/metabolism , Arabidopsis Proteins/genetics , Carrier Proteins/genetics , Cell Communication , Cell Membrane/metabolism , Gene Expression Regulation, Plant , Membrane Proteins/genetics , Microtubules , Molecular Sequence Data , Morphogenesis , Receptor Protein-Tyrosine Kinases/genetics , Sequence Alignment , Signal Transduction/genetics
15.
Ann Bot ; 107(9): 1453-63, 2011 Jun.
Article in English | MEDLINE | ID: mdl-21504912

ABSTRACT

BACKGROUND AND AIMS: Bisexual flowers of Carica papaya range from highly regular flowers to morphs with various fusions of stamens to the ovary. Arabidopsis thaliana sup1 mutants have carpels replaced by chimeric carpel-stamen structures. Comparative analysis of stamen to carpel conversions in the two different plant systems was used to understand the stage and origin of carpeloidy when derived from stamen tissues, and consequently to understand how carpeloidy contributes to innovations in flower evolution. METHODS: Floral development of bisexual flowers of Carica was studied by scanning electron microscopy and was compared with teratological sup mutants of A. thaliana. KEY RESULTS: In Carica development of bisexual flowers was similar to wild (unisexual) forms up to locule initiation. Feminization ranges from fusion of stamen tissue to the gynoecium to complete carpeloidy of antepetalous stamens. In A. thaliana, partial stamen feminization occurs exclusively at the flower apex, with normal stamens forming at the periphery. Such transformations take place relatively late in development, indicating strong developmental plasticity of most stamen tissues. These results are compared with evo-devo theories on flower bisexuality, as derived from unisexual ancestors. The Arabidopsis data highlight possible early evolutionary events in the acquisition of bisexuality by a patchy transformation of stamen parts into female parts linked to a flower axis-position effect. The Carica results highlight tissue-fusion mechanisms in angiosperms leading to carpeloidy once bisexual flowers have evolved. CONCLUSIONS: We show two different developmental routes leading to stamen to carpel conversions by late re-specification. The process may be a fundamental aspect of flower development that is hidden in most instances by developmental homeostasis.


Subject(s)
Arabidopsis Proteins/genetics , Arabidopsis/growth & development , Biological Evolution , Carica/growth & development , Flowers/growth & development , Transcription Factors/genetics , Arabidopsis/genetics , Arabidopsis/ultrastructure , Carica/genetics , Carica/ultrastructure , Flowers/genetics , Flowers/ultrastructure , Meristem/growth & development , Microscopy, Electron, Scanning , Mutation
17.
Plant Cell ; 20(4): 901-19, 2008 Apr.
Article in English | MEDLINE | ID: mdl-18441215

ABSTRACT

In Arabidopsis thaliana, flowers are determinate, showing a fixed number of whorls. Here, we report on three independent genes, a novel gene REBELOTE (RBL; protein of unknown function), SQUINT (SQN; a cyclophilin), and ULTRAPETALA1 (ULT1; a putative transcription factor) that redundantly influence floral meristem (FM) termination. Their mutations, combined with each other or with crabs claw, the genetic background in which they were isolated, trigger a strong FM indeterminacy with reiterations of extra floral whorls in the center of the flower. The range of phenotypes suggests that, in Arabidopsis, FM termination is initiated from stages 3 to 4 onwards and needs to be maintained through stage 6 and beyond, and that RBL, SQN, and ULT1 are required for this continuous regulation. We show that mutant phenotypes result from a decrease of AGAMOUS (AG) expression in an inner 4th whorl subdomain. However, the defect of AG activity alone does not explain all reported phenotypes, and our genetic data suggest that RBL, SQN, and, to a lesser extent, ULT1 also influence SUPERMAN activity. Finally, from all the molecular and genetic data presented, we argue that these genes contribute to the more stable and uniform development of flowers, termed floral developmental homeostasis.


Subject(s)
Arabidopsis Proteins/physiology , Arabidopsis/genetics , Arabidopsis/physiology , Meristem/physiology , Amino Acid Sequence , Arabidopsis Proteins/chemistry , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Cloning, Molecular , Genes, Plant , In Situ Hybridization , Microscopy, Electron, Scanning , Molecular Sequence Data , Mutagenesis , Polymerase Chain Reaction , Sequence Homology, Amino Acid , Subcellular Fractions/metabolism
18.
Plant J ; 38(1): 182-92, 2004 Apr.
Article in English | MEDLINE | ID: mdl-15053771

ABSTRACT

We report a comparative analysis of cell proliferation patterns during Arabidopsis flower development. Cell division was evaluated by a direct method, i.e. the 5-bromo-2'-deoxyuridine (BrdU) incorporation/immunodetection procedure. BrdU patterns in wild-type plants were correlated with the expression profiles of both several cell cycle genes involved in the control of the G(1)/S transition and cell cycle-related repressor genes, MSI4 and MSI5, encoding WD-repeat proteins. To evaluate how proliferation patterns arise with respect to boundaries and vice versa, the expression of a boundary gene, CUP SHAPED COTYLEDON (CUC)2, was determined. Combining these approaches, we demonstrate that boundaries between inflorescence and floral meristems and between floral whorls are narrow bands of non-dividing cells. In addition, we show that negative and positive regulators of cell proliferation are simultaneously and continuously expressed in dividing meristematic domains, being excluded from boundary cells. Finally, BrdU incorporation and CUC2 in situ hybridisation patterns were analysed in two mutant backgrounds, agamous (ag)-1 and superman (sup)-1, in order to assess changes in boundary establishment and different levels of indeterminacy under conditions of altered proliferation at the floral meristem centre.


Subject(s)
Arabidopsis/growth & development , Arabidopsis/cytology , Arabidopsis/genetics , Arabidopsis/metabolism , Arabidopsis Proteins/genetics , Bromodeoxyuridine/metabolism , Cell Cycle , Cell Division , Flowers/cytology , Flowers/growth & development , Flowers/metabolism , Gene Expression Regulation, Developmental , Gene Expression Regulation, Plant , Genes, Plant , Meristem/cytology , Meristem/growth & development , Meristem/metabolism , Mutation
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