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1.
Proc Natl Acad Sci U S A ; 118(13)2021 03 30.
Article in English | MEDLINE | ID: mdl-33771923

ABSTRACT

Phyllotaxis, the distribution of organs such as leaves and flowers on their support, is a key attribute of plant architecture. The geometric regularity of phyllotaxis has attracted multidisciplinary interest for centuries, resulting in an understanding of the patterns in the model plants Arabidopsis and tomato down to the molecular level. Nevertheless, the iconic example of phyllotaxis, the arrangement of individual florets into spirals in the heads of the daisy family of plants (Asteraceae), has not been fully explained. We integrate experimental data and computational models to explain phyllotaxis in Gerbera hybrida We show that phyllotactic patterning in gerbera is governed by changes in the size of the morphogenetically active zone coordinated with the growth of the head. The dynamics of these changes divides the patterning process into three phases: the development of an approximately circular pattern with a Fibonacci number of primordia near the head rim, its gradual transition to a zigzag pattern, and the development of a spiral pattern that fills the head on the template of this zigzag pattern. Fibonacci spiral numbers arise due to the intercalary insertion and lateral displacement of incipient primordia in the first phase. Our results demonstrate the essential role of the growth and active zone dynamics in the patterning of flower heads.


Subject(s)
Asteraceae/physiology , Inflorescence/growth & development , Organogenesis, Plant , Asteraceae/anatomy & histology , Genes, Reporter , Indoleacetic Acids/metabolism , Inflorescence/anatomy & histology , Plant Proteins/genetics , Plant Proteins/metabolism , Plants, Genetically Modified
2.
Plant Physiol ; 184(3): 1455-1468, 2020 11.
Article in English | MEDLINE | ID: mdl-32900982

ABSTRACT

The large sunflower family, Asteraceae, is characterized by compressed, flower-like inflorescences that may bear phenotypically distinct flower types. The CYCLOIDEA (CYC)/TEOSINTE BRANCHED1-like transcription factors (TFs) belonging to the TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR (TCP) protein family are known to regulate bilateral symmetry in single flowers. In Asteraceae, they function at the inflorescence level, and were recruited to define differential flower type identities. Here, we identified upstream regulators of GhCYC3, a gene that specifies ray flower identity at the flower head margin in the model plant Gerbera hybrida We discovered a previously unidentified expression domain and functional role for the paralogous CINCINNATA-like TCP proteins. They function upstream of GhCYC3 and affect the developmental delay of marginal ray primordia during their early ontogeny. At the level of single flowers, the Asteraceae CYC genes show a unique function in regulating the elongation of showy ventral ligules that play a major role in pollinator attraction. We discovered that during ligule development, the E class MADS-box TF GRCD5 activates GhCYC3 expression. We propose that the C class MADS-box TF GAGA1 contributes to stamen development upstream of GhCYC3 Our data demonstrate how interactions among and between the conserved floral regulators, TCP and MADS-box TFs, contribute to the evolution of the elaborate inflorescence architecture of Asteraceae.


Subject(s)
Asteraceae/growth & development , Asteraceae/genetics , Inflorescence/growth & development , Inflorescence/genetics , MADS Domain Proteins/metabolism , Plant Proteins/metabolism , Transcription Factors/metabolism , Gene Expression Regulation, Plant , MADS Domain Proteins/genetics , Plant Proteins/genetics , Plants, Genetically Modified/metabolism , Transcription Factors/genetics
3.
New Phytol ; 216(3): 939-954, 2017 Nov.
Article in English | MEDLINE | ID: mdl-28742220

ABSTRACT

The pseudanthial inflorescences of the sunflower family, Asteraceae, mimic a solitary flower but are composed of multiple flowers. Our studies in Gerbera hybrida indicate functional diversification for SEPALLATA (SEP)-like MADS box genes that often function redundantly in other core eudicots. We conducted phylogenetic and expression analysis for eight SEP-like GERBERA REGULATOR OF CAPITULUM DEVELOPMENT (GRCD) genes, including previously unstudied gene family members. Transgenic gerbera plants were used to infer gene functions. Adding to the previously identified stamen and carpel functions for GRCD1 and GRCD2, two partially redundant genes, GRCD4 and GRCD5, were found to be indispensable for petal development. Stepwise conversion of floral organs into leaves in the most severe RNA interference lines suggest redundant and additive GRCD activities in organ identity regulation. We show conserved and redundant functions for several GRCD genes in regulation of flower meristem maintenance, while functional diversification for three SEP1/2/4 clade genes in regulation of inflorescence meristem patterning was observed. GRCD genes show both specialized and pleiotropic functions contributing to organ differentiation and flower meristem fate, and uniquely, to patterning of the inflorescence meristem. Altogether, we provide an example of how plant reproductive evolution has used conserved genetic modules for regulating the elaborate inflorescence architecture in Asteraceae.


Subject(s)
Asteraceae/genetics , Inflorescence/genetics , Plant Proteins/genetics , Asteraceae/physiology , Flowers/physiology , Gene Expression Regulation, Plant , MADS Domain Proteins/genetics , Meristem/genetics , Multigene Family , Phylogeny , Plant Leaves/physiology , Plants, Genetically Modified , RNA Interference
4.
Plant Physiol ; 172(1): 284-96, 2016 09.
Article in English | MEDLINE | ID: mdl-27382139

ABSTRACT

The evolutionary success of Asteraceae, the largest family of flowering plants, has been attributed to the unique inflorescence architecture of the family, which superficially resembles an individual flower. Here, we show that Asteraceae inflorescences (flower heads, or capitula) resemble solitary flowers not only morphologically but also at the molecular level. By conducting functional analyses for orthologs of the flower meristem identity genes LEAFY (LFY) and UNUSUAL FLORAL ORGANS (UFO) in Gerbera hybrida, we show that GhUFO is the master regulator of flower meristem identity, while GhLFY has evolved a novel, homeotic function during the evolution of head-like inflorescences. Resembling LFY expression in a single flower meristem, uniform expression of GhLFY in the inflorescence meristem defines the capitulum as a determinate structure that can assume floral fate upon ectopic GhUFO expression. We also show that GhLFY uniquely regulates the ontogeny of outer, expanded ray flowers but not inner, compact disc flowers, indicating that the distinction of different flower types in Asteraceae is connected with their independent evolutionary origins from separate branching systems.


Subject(s)
Asteraceae/genetics , Flowers/genetics , Genes, Plant/genetics , Inflorescence/genetics , Meristem/genetics , Asteraceae/growth & development , Asteraceae/ultrastructure , Evolution, Molecular , Flowers/growth & development , Flowers/ultrastructure , Gene Expression Regulation, Developmental , Gene Expression Regulation, Plant , In Situ Hybridization , Inflorescence/growth & development , Inflorescence/ultrastructure , Meristem/growth & development , Meristem/ultrastructure , Microscopy, Electron, Scanning , Mutation , Plant Proteins/genetics , Plant Proteins/metabolism , Plants, Genetically Modified , Protein Binding , RNA Interference , Reverse Transcriptase Polymerase Chain Reaction , Two-Hybrid System Techniques
5.
Plant J ; 79(5): 783-96, 2014 Sep.
Article in English | MEDLINE | ID: mdl-24923429

ABSTRACT

The complex inflorescences (capitula) of Asteraceae consist of different types of flowers. In Gerbera hybrida (gerbera), the peripheral ray flowers are bilaterally symmetrical and lack functional stamens while the central disc flowers are more radially symmetrical and hermaphroditic. Proteins of the CYC2 subclade of the CYC/TB1-like TCP domain transcription factors have been recruited several times independently for parallel evolution of bilaterally symmetrical flowers in various angiosperm plant lineages, and have also been shown to regulate flower-type identity in Asteraceae. The CYC2 subclade genes in gerbera show largely overlapping gene expression patterns. At the level of single flowers, their expression domain in petals shows a spatial shift from the dorsal pattern known so far in species with bilaterally symmetrical flowers, suggesting that this change in expression may have evolved after the origin of Asteraceae. Functional analysis indicates that GhCYC2, GhCYC3 and GhCYC4 mediate positional information at the proximal-distal axis of the inflorescence, leading to differentiation of ray flowers, but that they also regulate ray flower petal growth by affecting cell proliferation until the final size and shape of the petals is reached. Moreover, our data show functional diversification for the GhCYC5 gene. Ectopic activation of GhCYC5 increases flower density in the inflorescence, suggesting that GhCYC5 may promote the flower initiation rate during expansion of the capitulum. Our data thus indicate that modification of the ancestral network of TCP factors has, through gene duplications, led to the establishment of new expression domains and to functional diversification.


Subject(s)
Asteraceae/genetics , Evolution, Molecular , Gene Duplication , Gene Expression Regulation, Plant , Plant Proteins/genetics , Arabidopsis/anatomy & histology , Arabidopsis/genetics , Arabidopsis/growth & development , Asteraceae/anatomy & histology , Asteraceae/growth & development , DNA, Plant/chemistry , DNA, Plant/genetics , Flowers/anatomy & histology , Flowers/genetics , Flowers/growth & development , Gene Expression Profiling , Inflorescence/anatomy & histology , Inflorescence/genetics , Inflorescence/growth & development , Multigene Family , Phylogeny , Plants, Genetically Modified , Real-Time Polymerase Chain Reaction , Transcription Factors/genetics , Transgenes , Up-Regulation
6.
BMC Plant Biol ; 10: 128, 2010 Jun 25.
Article in English | MEDLINE | ID: mdl-20579337

ABSTRACT

BACKGROUND: The flowering process in plants proceeds through the induction of an inflorescence meristem triggered by several pathways. Many of the genes associated with both the flowering process and floral architecture encode transcription factors of the MADS domain family. Gerbera, a member of the sunflower family, Asteraceae, bears compressed inflorescence heads (capitula) with three different flower types characterized by differences in both sexuality and floral symmetry. To understand how such a complex inflorescence structure is achieved at the molecular level, we have characterized the array of Gerbera MADS box genes. The high number of SQUAMOSA-like genes in Gerbera compared to other model species raised the question as to whether they may relate to Gerbera's complex inflorescence structure and whether or not a homeotic A function is present. RESULTS: In this paper we describe six Gerbera genes related to the SQUAMOSA/APETALA1/FRUITFULL genes of snapdragon and Arabidopsis. Based on phylogenetic analysis of the entire gene lineage, our data indicates that GSQUA1 and GSQUA3 are members of the SQUA/AP1 clade, while GSQUA2, GSQUA4, GSQUA5 and GSQUA6 are co-orthologs of the Arabidopsis FUL gene. GSQUA1/GSQUA3 and GSQUA4/GSQUA5/GSQUA6, respectively, represent several gene duplication events unknown in the model systems that may be specific to either Gerbera or Asteraceae. GSQUA genes showed specific expression profiles. GSQUA1, GSQUA2, and GSQUA5 were inflorescence abundant, while GSQUA3, GSQUA4, and GSQUA6 expression was also detected in vegetative organs. Overexpression of GSQUA2 in Gerbera led to accelerated flowering, dwarfism and vegetative abnormalities, all new and specific phenomena observed in transgenic Gerbera plants with modified MADS box gene expression. CONCLUSIONS: Based on expression patterns, none of the Gerbera SQUA-like genes are likely to control flower organ identity in the sense of the floral A function. However, our data shows that the FUL-like gene GSQUA2 plays a vital role in meristem transition. The roles of other GSQUA-genes in Gerbera floral development are intriguing, but require still further study.


Subject(s)
Asteraceae , Gene Expression Regulation, Plant , MADS Domain Proteins/genetics , MADS Domain Proteins/metabolism , Meristem/metabolism , Amino Acid Sequence , Asteraceae/genetics , Asteraceae/growth & development , Asteraceae/metabolism , Flowers/growth & development , MADS Domain Proteins/chemistry , Meristem/growth & development , Molecular Sequence Data , Phenotype , Phylogeny , Plants, Genetically Modified/genetics , Plants, Genetically Modified/metabolism , Reproduction/genetics , Sequence Alignment
7.
J Exp Bot ; 61(1): 75-85, 2010.
Article in English | MEDLINE | ID: mdl-19767305

ABSTRACT

According to the classical ABC model, B-function genes are involved in determining petal and stamen development. Most core eudicot species have B class genes belonging to three different lineages: the PI, euAP3, and TM6 lineages, although both Arabidopsis and Antirrhinum appear to have lost their TM6-like gene. Functional studies were performed for three gerbera (Gerbera hybrida) B class MADS-box genes--PI/GLO-like GGLO1, euAP3 class GDEF2, and TM6-like GDEF1--and data are shown for a second euAP3-like gene, GDEF3. In phylogenetic analysis, GDEF3 is a closely related paralogue of GDEF2, and apparently stems from a duplication common to all Asteraceae. Expression analysis and transgenic phenotypes confirm that GGLO1 and GDEF2 mediate the classical B-function since they determine petal and stamen identities. However, based on assays in yeast, three B class heterodimer combinations are possible in gerbera. In addition to the interaction of GGLO1 and GDEF2 proteins, GGLO1 also pairs with GDEF1 and GDEF3. This analysis of GDEF1 represents the first functional characterization of a TM6-like gene in a core eudicot species outside Solanaceae. Similarly to its relatives in petunia and tomato, the expression pattern and transgenic phenotypes indicate that GDEF1 is not involved in determination of petal identity, but has a redundant role in regulating stamen development.


Subject(s)
Asteraceae/metabolism , MADS Domain Proteins/metabolism , Asteraceae/genetics , Down-Regulation/genetics , Flowers/genetics , Flowers/ultrastructure , Gene Expression Profiling , Gene Expression Regulation, Plant , Genes, Plant/genetics , MADS Domain Proteins/genetics , Organ Specificity , Phenotype , Phylogeny , Plant Epidermis/cytology , Plant Epidermis/ultrastructure , Plants, Genetically Modified , Protein Binding
8.
J Exp Bot ; 59(13): 3691-703, 2008.
Article in English | MEDLINE | ID: mdl-18725377

ABSTRACT

Genetic modification of the flavonoid pathway has been used to produce novel colours and colour patterns in ornamental plants as well as to modify the nutritional and pharmaceutical properties of food crops. It has been suggested that co-ordinate control of multiple steps of the pathway with the help of regulatory genes would lead to a more predictable control of metabolic flux. Regulation of anthocyanin biosynthesis has been studied in a common ornamental plant, Gerbera hybrida (Asteraceae). An R2R3-type MYB factor, GMYB10, shares high sequence similarity and is phylogenetically grouped together with previously characterized regulators of anthocyanin pigmentation. Ectopic expression of GMYB10 leads to strongly enhanced accumulation of anthocyanin pigments as well as to an altered pigmentation pattern in transgenic gerbera plants. Anthocyanin analysis indicates that GMYB10 specifically induces cyanidin biosynthesis in undifferentiated callus and in vegetative tissues. Furthermore, in floral tissues enhanced pelargonidin production is detected. Microarray analysis using the gerbera 9K cDNA array revealed a highly predicted set of putative target genes for GMYB10 including new gene family members of both early and late biosynthetic genes of the flavonoid pathway. However, completely new candidate targets, such as a serine carboxypeptidase-like gene as well, as two new MYB domain factors, GMYB11 and GMYB12, whose exact function in phenylpropanoid biosynthesis is not clear yet, were also identified.


Subject(s)
Anthocyanins/biosynthesis , Asteraceae/genetics , Asteraceae/metabolism , Gene Expression Regulation, Plant , Genes, Regulator , Plant Proteins/genetics , Transcription Factors/metabolism , Flowers/genetics , Flowers/metabolism , Molecular Sequence Data , Phenotype , Plant Proteins/metabolism , Transcription Factors/genetics
9.
Proc Natl Acad Sci U S A ; 105(26): 9117-22, 2008 Jul 01.
Article in English | MEDLINE | ID: mdl-18574149

ABSTRACT

Several key processes in plant development are regulated by TCP transcription factors. CYCLOIDEA-like (CYC-like) TCP domain proteins have been shown to control flower symmetry in distantly related plant lineages. Gerbera hybrida, a member of one of the largest clades of angiosperms, the sunflower family (Asteraceae), is an interesting model for developmental studies because its elaborate inflorescence comprises different types of flowers that have specialized structures and functions. The morphological differentiation of flower types involves gradual changes in flower size and symmetry that follow the radial organization of the densely packed inflorescence. Differences in the degree of petal fusion further define the distinct shapes of the Gerbera flower types. To study the role of TCP transcription factors during specification of this complex inflorescence organization, we characterized the CYC-like homolog GhCYC2 from Gerbera. The expression of GhCYC2 follows a gradient along the radial axis of the inflorescence. GhCYC2 is expressed in the marginal, bilaterally symmetrical ray flowers but not in the centermost disk flowers, which are nearly radially symmetrical and have significantly less fused petals. Overexpression of GhCYC2 causes disk flowers to obtain morphologies similar to ray flowers. Both expression patterns and transgenic phenotypes suggest that GhCYC2 is involved in differentiation among Gerbera flower types, providing the first molecular evidence that CYC-like TCP factors take part in defining the complex inflorescence structure of the Asteraceae, a major determinant of the family's evolutionary success.


Subject(s)
Asteraceae/embryology , Body Patterning , Flowers/embryology , Plant Proteins/chemistry , Plant Proteins/metabolism , Asteraceae/cytology , Asteraceae/genetics , Asteraceae/ultrastructure , DNA-Binding Proteins , Flowers/cytology , Flowers/genetics , Flowers/ultrastructure , Gene Expression Profiling , Gene Expression Regulation, Plant , Molecular Sequence Data , Phenotype , Phylogeny , Plant Proteins/genetics , Plant Proteins/isolation & purification , Plants, Genetically Modified , Protein Structure, Tertiary , Sequence Homology, Amino Acid , Transcription Factors/chemistry , Transcription Factors/genetics , Transcription Factors/isolation & purification , Transcription Factors/metabolism
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