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1.  The Making of a Compound Inflorescence in Tomato and Related Nightshades 
PLoS Biology  2008;6(11):e288.
Variation in the branching of plant inflorescences determines flower number and, consequently, reproductive success and crop yield. Nightshade (Solanaceae) species are models for a widespread, yet poorly understood, program of eudicot growth, where short side branches are initiated upon floral termination. This “sympodial” program produces the few-flowered tomato inflorescence, but the classical mutants compound inflorescence (s) and anantha (an) are highly branched, and s bears hundreds of flowers. Here we show that S and AN, which encode a homeobox transcription factor and an F-box protein, respectively, control inflorescence architecture by promoting successive stages in the progression of an inflorescence meristem to floral specification. S and AN are sequentially expressed during this gradual phase transition, and the loss of either gene delays flower formation, resulting in additional branching. Independently arisen alleles of s account for inflorescence variation among domesticated tomatoes, and an stimulates branching in pepper plants that normally have solitary flowers. Our results suggest that variation of Solanaceae inflorescences is modulated through temporal changes in the acquisition of floral fate, providing a flexible evolutionary mechanism to elaborate sympodial inflorescence shoots.
Author Summary
Among the most distinguishing features of plants are the flower-bearing shoots, called inflorescences. Despite a solid understanding of flower development, the molecular mechanisms that control inflorescence architecture remain obscure. We have explored this question in tomato, where mutations in two genes, ANANTHA (AN) and COMPOUND INFLORESCENCE (S), transform the well-known tomato “vine” into a highly branched structure with hundreds of flowers. We find that AN encodes an F-box protein ortholog of a gene called UNUSUAL FLORAL ORGANS that controls the identity of floral organs (petals, sepals, and so on), whereas S encodes a transcription factor related to a gene called WUSCHEL HOMEOBOX 9 that is involved in patterning the embryo within the plant seed. (F-box proteins are known for marking other proteins for degradation, but they can also function in hormone regulation and transcriptional activation) Interestingly, these genes have little or no effect on branching in inflorescences that grow continuously (so-called “indeterminate” shoots), as in Arabidopsis. However, we find that transient sequential expression of S followed by AN promotes branch termination and flower formation in plants where meristem growth ends with inflorescence and flower production (“determinate” shoots). We show that mutant alleles of s dramatically increase branch and flower number and have probably been selected for by breeders during modern cultivation. Moreover, the single-flower inflorescence of pepper (a species related to tomato, within the same Solanaceae family) can be converted to a compound inflorescence upon mutating its AN ortholog. Our results suggest a new developmental mechanism whereby inflorescence elaboration can be controlled through temporal regulation of floral fate.
Plant flower production is largely determined by the number of inflorescences, the branches produced on flower stems. Two genes identified in tomato reveal a new phase transition that may explain the mechanism of evolution of compound inflorescences in the Solanaceae family.
PMCID: PMC2586368  PMID: 19018664
2.  Genetic control of inflorescence architecture in legumes 
The architecture of the inflorescence, the shoot system that bears the flowers, is a main component of the huge diversity of forms found in flowering plants. Inflorescence architecture has also a strong impact on the production of fruits and seeds, and on crop management, two highly relevant agronomical traits. Elucidating the genetic networks that control inflorescence development, and how they vary between different species, is essential to understanding the evolution of plant form and to being able to breed key architectural traits in crop species. Inflorescence architecture depends on the identity and activity of the meristems in the inflorescence apex, which determines when flowers are formed, how many are produced and their relative position in the inflorescence axis. Arabidopsis thaliana, where the genetic control of inflorescence development is best known, has a simple inflorescence, where the primary inflorescence meristem directly produces the flowers, which are thus borne in the main inflorescence axis. In contrast, legumes represent a more complex inflorescence type, the compound inflorescence, where flowers are not directly borne in the main inflorescence axis but, instead, they are formed by secondary or higher order inflorescence meristems. Studies in model legumes such as pea (Pisum sativum) or Medicago truncatula have led to a rather good knowledge of the genetic control of the development of the legume compound inflorescence. In addition, the increasing availability of genetic and genomic tools for legumes is allowing to rapidly extending this knowledge to other grain legume crops. This review aims to describe the current knowledge of the genetic network controlling inflorescence development in legumes. It also discusses how the combination of this knowledge with the use of emerging genomic tools and resources may allow rapid advances in the breeding of grain legume crops.
PMCID: PMC4508509  PMID: 26257753
legumes; pea; inflorescence architecture; meristem identity; AP1; TFL1; VEG1
3.  Characterization of the sequence and expression pattern of LFY homologues from dogwood species (Cornus) with divergent inflorescence architectures 
Annals of Botany  2013;112(8):1629-1641.
Background and Aims LFY
homologues encode transcription factors that regulate the transition from vegetative to reproductive growth in flowering plants and have been shown to control inflorescence patterning in model species. This study investigated the expression patterns of LFY homologues within the diverse inflorescence types (head-like, umbel-like and inflorescences with elongated internodes) in closely related lineages in the dogwood genus (Cornus s.l.). The study sought to determine whether LFY homologues in Cornus species are expressed during floral and inflorescence development and if the pattern of expression is consistent with a function in regulating floral development and inflorescence architectures in the genus.
Total RNAs were extracted using the CTAB method and the first-strand cDNA was synthesized using the SuperScript III first-strand synthesis system kit (Invitrogen). Expression of CorLFY was investigated by RT–PCR and RNA in situ hybridization. Phylogenetic analyses were conducted using the maximum likelihood methods implemented in RAxML-HPC v7.2.8.
Key Results
cDNA clones of LFY homologues (designated CorLFY) were isolated from six Cornus species bearing different types of inflorescence. CorLFY cDNAs were predicted to encode proteins of approximately 375 amino acids. The detection of CorLFY expression patterns using in situ RNA hybridization demonstrated the expression of CorLFY within the inflorescence meristems, inflorescence branch meristems, floral meristems and developing floral organ primordia. PCR analyses for cDNA libraries derived from reverse transcription of total RNAs showed that CorLFY was also expressed during the late-stage development of flowers and inflorescences, as well as in bracts and developing leaves. Consistent differences in the CorLFY expression patterns were not detected among the distinct inflorescence types.
The results suggest a role for CorLFY genes during floral and inflorescence development in dogwoods. However, the failure to detect expression differences between the inflorescence types in the Cornus species analysed suggests that the evolutionary shift between major inflorescence types in the genus is not controlled by dramatic alterations in the levels of CorLFY gene transcript accumulation. However, due to spatial, temporal and quantitative limitations of the expression data, it cannot be ruled out that subtle differences in the level or location of CorLFY transcripts may underlie the different inflorescence architectures that are observed across these species. Alternatively, differences in CorLFY protein function or the expression or function of other regulators (e.g. TFL1 and UFO homologues) may support the divergent developmental trajectories.
PMCID: PMC3828947  PMID: 24052556
Cornus; dogwood; inflorescence evolution; LFY homologues; CorLFY expression; RT–PCR; in situ hybridization
4.  Regulation of inflorescence architecture by cytokinins 
In flowering plants, the arrangement of flowers on a stem becomes an inflorescence, and a huge variety of inflorescence architecture occurs in nature. Inflorescence architecture also affects crop yield. In simple inflorescences, flowers form on a main stem; by contrast, in compound inflorescences, flowers form on branched stems and the branching pattern defines the architecture of the inflorescence. In this review, we highlight recent findings on the regulation of inflorescence architecture by cytokinin plant hormones. Results in rice (Oryza sativa) and Arabidopsis thaliana show that although these two species have distinct inflorescence architectures, cytokinins have a common effect on inflorescence branching. Based on these studies, we discuss how cytokinins regulate distinct types of inflorescence architecture through their effect on meristem activities.
PMCID: PMC4241816  PMID: 25505480
branching; cytokinin; floral meristem; inflorescence; shoot apical meristem
5.  AGO1 controls arabidopsis inflorescence architecture possibly by regulating TFL1 expression 
Annals of Botany  2014;114(7):1471-1481.
Background and Aims
The TERMINAL FLOWER 1 (TFL1) gene is pivotal in the control of inflorescence architecture in arabidopsis. Thus, tfl1 mutants flower early and have a very short inflorescence phase, while TFL1-overexpressing plants have extended vegetative and inflorescence phases, producing many coflorescences. TFL1 is expressed in the shoot meristems, never in the flowers. In the inflorescence apex, TFL1 keeps the floral genes LEAFY (LFY) and APETALA1 (AP1) restricted to the flower, while LFY and AP1 restrict TFL1 to the inflorescence meristem. In spite of the central role of TFL1 in inflorescence architecture, regulation of its expression is poorly understood. This study aims to expand the understanding of inflorescence development by identifying and studying novel TFL1 regulators.
Mutagenesis of an Arabidopsis thaliana line carrying a TFL1::GUS (β-glucuronidase) reporter construct was used to isolate a mutant with altered TFL1 expression. The mutated gene was identified by positional cloning. Expression of TFL1 and TFL1::GUS was analysed by real-time PCR and histochemical GUS detection. Double-mutant analysis was used to assess the contribution of TFL1 to the inflorescence mutant phenotype.
Key Results
A mutant with both an increased number of coflorescences and high and ectopic TFL1 expression was isolated. Cloning of the mutated gene showed that both phenotypes were caused by a mutation in the ARGONAUTE1 (AGO1) gene, which encodes a key component of the RNA silencing machinery. Analysis of another ago1 allele indicated that the proliferation of coflorescences and ectopic TFL1 expression phenotypes are not allele specific. The increased number of coflorescences is suppressed in ago1 tfl1 double mutants.
The results identify AGO1 as a repressor of TFL1 expression. Moreover, they reveal a novel role for AGO1 in inflorescence development, controlling the production of coflorescences. AGO1 seems to play this role through regulating TFL1 expression.
PMCID: PMC4204786  PMID: 24989784
Flower development; TERMINAL FLOWER 1; TFL1; ARGONAUTE1; AGO1; plant architecture; inflorescence architecture; flowering; Arabidopsis thaliana
6.  Determination of Flower Structure in Elaeis guineensis: Do Palms use the Same Homeotic Genes as Other Species? 
Annals of Botany  2007;100(1):1-12.
In this article a review is made of data recently obtained on the structural diversity and possible functions of MADS box genes in the determination of flower structure in the African oil palm (Elaeis guineensis). MADS box genes play a dominant role in the ABC model established to explain how floral organ identity is determined in model dicotyledon species such as Arabidopsis thaliana and Antirrhinum majus. In the monocotyledons, although there appears to be a broad general conservation of ABC gene functions, the model itself needs to be adapted in some cases, notably for certain species which produce flowers with sepals and petals of similar appearance. For the moment, ABC genes remain unstudied in a number of key monocot clades, so only a partial picture is available for the Liliopsida as a whole. The aim of this article is to summarize data recently obtained for the African oil palm Elaeis guineensis, a member of the family Arecaceae (Arecales), and to discuss their significance with respect to knowledge gained from other Angiosperm groups, particularly within the monocotyledons.
The essential details of reproductive development in oil palm are discussed and an overview is provided of the structural and functional characterization of MADS box genes likely to play a homeotic role in flower development in this species.
The structural and functional data provide evidence for a general conservation of the generic ‘ABC’ model in oil palm, rather than the ‘modified ABC model’ proposed for some other monocot species which produce homochlamydeous flowers (i.e. with morphologically similar organs in both perianth whorls), such as members of the Liliales. Our oil palm data therefore follow a similar pattern to those obtained for other Commelinid species in the orders Commelinales and Poales. The significance of these findings is discussed.
PMCID: PMC2735288  PMID: 17355996
Palm; MADS box; flower; Elaeis; monoecious; homeotic
7.  The interplay between inflorescence development and function as the crucible of architectural diversity 
Annals of Botany  2012;112(8):1477-1493.
Most angiosperms present flowers in inflorescences, which play roles in reproduction, primarily related to pollination, beyond those served by individual flowers alone. An inflorescence's overall reproductive contribution depends primarily on the three-dimensional arrangement of the floral canopy and its dynamics during its flowering period. These features depend in turn on characteristics of the underlying branching structure (scaffold) that supports and supplies water and nutrients to the floral canopy. This scaffold is produced by developmental algorithms that are genetically specified and hormonally mediated. Thus, the extensive inflorescence diversity evident among angiosperms evolves through changes in the developmental programmes that specify scaffold characteristics, which in turn modify canopy features that promote reproductive performance in a particular pollination and mating environment. Nevertheless, developmental and ecological aspects of inflorescences have typically been studied independently, limiting comprehensive understanding of the relations between inflorescence form, reproductive function, and evolution.
This review fosters an integrated perspective on inflorescences by summarizing aspects of their development and pollination function that enable and guide inflorescence evolution and diversification.
The architecture of flowering inflorescences comprises three related components: topology (branching patterns, flower number), geometry (phyllotaxis, internode and pedicel lengths, three-dimensional flower arrangement) and phenology (flower opening rate and longevity, dichogamy). Genetic and developmental evidence reveals that these components are largely subject to quantitative control. Consequently, inflorescence evolution proceeds along a multidimensional continuum. Nevertheless, some combinations of topology, geometry and phenology are represented more commonly than others, because they serve reproductive function particularly effectively. For wind-pollinated species, these combinations often represent compromise solutions to the conflicting physical influences on pollen removal, transport and deposition. For animal-pollinated species, dominant selective influences include the conflicting benefits of large displays for attracting pollinators and of small displays for limiting among-flower self-pollination. The variety of architectural components that comprise inflorescences enable diverse resolutions of these conflicts.
PMCID: PMC3828939  PMID: 23243190
Inflorescence; angiosperm; form and function; evolution; development; architecture; floral display; pollination; geitonogamy; heterochrony
8.  The unique pseudanthium of Actinodium (Myrtaceae) - morphological reinvestigation and possible regulation by CYCLOIDEA-like genes 
EvoDevo  2013;4:8.
Genes encoding TCP transcription factors, such as CYCLOIDEA-like (CYC-like) genes, are well known actors in the control of plant morphological development, particularly regarding the control of floral symmetry. Despite recent understanding that these genes play a role in establishing the architecture of inflorescences in the sunflower family (Asteraceae), where hundreds of finely organized flowers are arranged to mimic an individual flower, little is known about their function in the development of flower-like inflorescences across diverse phylogenetic groups. Here, we studied the head-like pseudanthium of the Australian swamp daisy Actinodium cunninghamii Schau. (Myrtaceae, the myrtle family), which consists of a cluster of fertile flowers surrounded by showy ray-shaped structures, to fully characterize its inflorescence development and to test whether CYC-like genes may participate in the control of its daisy-like flowering structures.
We used standard morphological and anatomical methods to analyze Actinodium inflorescence development. Furthermore, we isolated Actinodium CYC-like genes using degenerate PCR primers, and studied the expression patterns of these genes using quantitative RT-PCR. We found that the ray-shaped elements of Actinodium are not single flowers but instead branched short-shoots occasionally bearing flowers. We found differential expression of CYC-like genes across the pseudanthium of Actinodium, correlating with the showiness and branching pattern of the ray structures.
The Actinodium inflorescence represents a novel type of pseudanthium with proximal branches mimicking ray flowers. Expression patterns of CYC-like genes are suggestive of participation in the control of pseudanthium development, in a manner analogous to the distantly related Asteraceae. As such, flowering plants appear to have recruited CYC-like genes for heteromorphic inflorescence development at least twice during their evolutionary history.
PMCID: PMC3610234  PMID: 23448118
Asteraceae; CYCLOIDEA; Gene expression; Inflorescence development; Myrtaceae; Pseudanthium; TCP
9.  Tomato Yield Heterosis Is Triggered by a Dosage Sensitivity of the Florigen Pathway That Fine-Tunes Shoot Architecture 
PLoS Genetics  2013;9(12):e1004043.
The superiority of hybrids has long been exploited in agriculture, and although many models explaining “heterosis” have been put forth, direct empirical support is limited. Particularly elusive have been cases of heterozygosity for single gene mutations causing heterosis under a genetic model known as overdominance. In tomato (Solanum lycopersicum), plants carrying mutations in SINGLE FLOWER TRUSS (SFT) encoding the flowering hormone florigen are severely delayed in flowering, become extremely large, and produce few flowers and fruits, but when heterozygous, yields are dramatically increased. Curiously, this overdominance is evident only in the background of “determinate” plants, in which the continuous production of side shoots and inflorescences gradually halts due to a defect in the flowering repressor SELF PRUNING (SP). How sp facilitates sft overdominance is unclear, but is thought to relate to the opposing functions these genes have on flowering time and shoot architecture. We show that sft mutant heterozygosity (sft/+) causes weak semi-dominant delays in flowering of both primary and side shoots. Using transcriptome sequencing of shoot meristems, we demonstrate that this delay begins before seedling meristems become reproductive, followed by delays in subsequent side shoot meristems that, in turn, postpone the arrest of shoot and inflorescence production. Reducing SFT levels in sp plants by artificial microRNAs recapitulates the dose-dependent modification of shoot and inflorescence production of sft/+ heterozygotes, confirming that fine-tuning levels of functional SFT transcripts provides a foundation for higher yields. Finally, we show that although flowering delays by florigen mutant heterozygosity are conserved in Arabidopsis, increased yield is not, likely because cyclical flowering is absent. We suggest sft heterozygosity triggers a yield improvement by optimizing plant architecture via its dosage response in the florigen pathway. Exploiting dosage sensitivity of florigen and its family members therefore provides a path to enhance productivity in other crops, but species-specific tuning will be required.
Author Summary
For over a century, it has been known that inbreeding harms plant and animal fitness, whereas interbreeding between genetically distinct individuals can lead to more robust offspring in a phenomenon known as hybrid vigor, or heterosis. While heterosis has been harnessed to boost agricultural productivity, its causes are not understood. Especially controversial is a model called “overdominance,” which states in its simplest form that a single gene can drive heterosis, although multiple overdominant genes can also contribute. In tomato, a mutation in just one of two copies of a gene encoding the flowering hormone called florigen causes remarkable increases in yield, but it is not known why. We show that yield increases are triggered by a fine-tuning of florigen levels that cause subtle delays in the time it takes all shoots to produce flowers. The resulting plant architecture maximizes yield in varieties that dominate the processing tomato industry. We show that while similar changes in flowering occur when one copy of florigen is mutated in the model crucifer plant Arabidopsis, yield is not increased, suggesting that, while manipulating florigen holds potential to improve crop productivity, the tuning of florigen and related genes will have to be tailored according to species.
PMCID: PMC3873276  PMID: 24385931
10.  Racemose inflorescences of monocots: structural and morphogenetic interaction at the flower/inflorescence level 
Annals of Botany  2012;112(8):1553-1566.
Understanding and modelling early events of floral meristem patterning and floral development requires consideration of positional information regarding the organs surrounding the floral meristem, such as the flower-subtending bracts (FSBs) and floral prophylls (bracteoles). In common with models of regulation of floral patterning, the simplest models of phyllotaxy consider only unbranched uniaxial systems. Racemose inflorescences and thyrses offer a useful model system for investigating morphogenetic interactions between organs belonging to different axes.
This review considers (1) racemose inflorescences of early-divergent and lilioid monocots and their possible relationship with other inflorescence types, (2) hypotheses on the morphogenetic significance of phyllomes surrounding developing flowers, (3) patterns of FSB reduction and (4) vascular patterns in the primary inflorescence axis and lateral pedicels.
Racemose (partial) inflorescences represent the plesiomorphic condition in monocots. The presence or absence of a terminal flower or flower-like structure is labile among early-divergent monocots. In some Alismatales, a few-flowered racemose inflorescence can be entirely transformed into a terminal ‘flower’. The presence or absence and position of additional phyllomes on the lateral pedicels represent important taxonomic markers and key features in regulation of flower patterning. Racemose inflorescences with a single floral prophyll are closely related to thyrses. Floral patterning is either unidirectional or simultaneous in species that lack a floral prophyll or possess a single adaxial floral prophyll and usually spiral in the outer perianth whorl in species with a transversely oriented floral prophyll. Inhibitory fields of surrounding phyllomes are relevant but insufficient to explain these patterns; other important factors are meristem space economy and/or the inhibitory activity of the primary inflorescence axis. Two patterns of FSB reduction exist in basal monocots: (1) complete FSB suppression (cryptic flower-subtending bract) and (2) formation of a ‘hybrid’ organ by overlap of the developmental programmes of the FSB and the first abaxial organ formed on the floral pedicel. FSB reduction affects patterns of interaction between the conductive systems of the flower and the primary inflorescence axis.
PMCID: PMC3828938  PMID: 23172413
Bracteole; flower; flower-subtending bract; inflorescence; inhibitory field; pattern formation; prophyll; regulation of development; vasculature
11.  Novel members of the AGAMOUS LIKE 6 subfamily of MIKCC-type MADS-box genes in soybean 
BMC Plant Biology  2013;13:105.
The classical (C) MIKC-type MADS-box transcription factors comprise one gene family that plays diverse roles in the flowering process ranging from floral initiation to the development of floral organs. Despite their importance in regulating developmental processes that impact crop yield, they remain largely unexplored in the major legume oilseed crop, soybean.
We identified 57 MIKCc-type transcription factors from soybean and determined the in silico gene expression profiles of the soybean MIKCc-type genes across different tissues. Our study implicates three MIKCc-type transcription factors as novel members of the AGAMOUS LIKE 6 (AGL6) subfamily of the MIKCC-type MADS-box genes, and we named this sister clade PsMADS3. While similar genes were identified in other legume species, poplar and grape, no such gene is represented in Arabidopsis thaliana or rice. RT-PCR analysis on these three soybean PsMADS3 genes during early floral initiation processes revealed their temporal expression similar to that of APETALA1, a gene known to function as a floral meristem identity gene. However, RNA in situ hybridisation showed that their spatial expression patterns are markedly different from those of APETALA1.
Legume flower development system differs from that in the model plant, Arabidopsis. There is an overlap in the initiation of different floral whorls in soybean, and inflorescent meristems can revert to leaf production depending on the environmental conditions. MIKCC-type MADS-box genes have been shown to play key regulatory roles in different stages of flower development. We identified members of the PsMADS3 sub-clade in legumes that show differential spatial expression during floral initiation, indicating their potential novel roles in the floral initiation process. The results from this study will contribute to a better understanding of legume-specific floral developmental processes.
PMCID: PMC3765189  PMID: 23870482
Development; Floral meristem; MADS-box transcription factor; Soybean
12.  Characterization of SQUAMOSA-like genes in Gerbera hybrida, including one involved in reproductive transition 
BMC Plant Biology  2010;10:128.
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.
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.
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.
PMCID: PMC3017819  PMID: 20579337
13.  Ontogeny and structure of the acervulate partial inflorescence in Hyophorbe lagenicaulis (Arecaceae; Arecoideae) 
Annals of Botany  2011;108(8):1517-1527.
Background and Aims
The palm tribe Chamaedoreeae displays flowers arranged in a complex partial inflorescence called an acervulus. This type of partial inflorescence has so far not been reported elsewhere in the largest palm subfamily Arecoideae, which is traditionally characterized by flowers predominantly arranged in triads of one central female and two lateral male flowers. The ontogenetic basis of the acervulus is as yet unknown and its structural diversity throughout the genera of the Chamaedoreeae poorly recorded. This study aims to provide critical information on these aspects.
Developmental series and mature inflorescences were sampled from plants cultivated in international botanical gardens and wild populations. The main techniques employed included scanning electronic microscopy and serial anatomical sectioning of resin-embedded fragments of rachillae.
Key Results
Inflorescence ontogeny in Hyophorbe lagenicaulis demonstrates that the acervulus and the inflorescence rachilla form a condensed and cymose branching system resembling a coenosome. Syndesmy results from a combined process of rapid development and adnation, without or with reduced axis elongation. Acervulus diversity in the ten taxa of the Chamaedoreeae studied is displayed at the level of their positioning within the inflorescence, their arrangement, the number of floral buds and their sexual expression.
The results show that a more general definition of the type of partial inflorescence observed within the large subfamily Arecoideae would correspond to a cyme rather than to a floral triad. In spite of their common cymose architecture, the floral triad and the acervulus present differences with respect to the number and arrangement of floral buds, the superficial pattern of development and sexual expression.
PMCID: PMC3219493  PMID: 21712300
Arecoideae; Chamaedoreeae; Hyophorbe lagenicaulis; acervulus; development; partial inflorescence
14.  A MADS-box gene NtSVP regulates pedicel elongation by directly suppressing a KNAT1-like KNOX gene NtBPL in tobacco (Nicotiana tabacum L.) 
Journal of Experimental Botany  2015;66(20):6233-6244.
A tobacco (Nicotiana tobaccum) SVP family MADS-box gene is identified as a new regulator working in pedicel elongation for optimal inflorescence architecture by directly regulating an Arabidopsis BP homologue NtBPL
Optimal inflorescence architecture is important for plant reproductive success by affecting the ultimate number of flowers that set fruits and for plant competitiveness when interacting with biotic or abiotic conditions. The pedicel is one of the key contributors to inflorescence architecture diversity. To date, knowledge about the molecular mechanisms of pedicel development is derived from Arabidopsis. Not much is known regarding other plants. Here, an SVP family MADS-box gene, NtSVP, in tobacco (Nicotiana tabacum) that is required for pedicel elongation was identified. It is shown that knockdown of NtSVP by RNA interference (RNAi) caused elongated pedicels, while overexpression resulted in compact inflorescences with much shortened pedicels. Moreover, an Arabidopsis BREVIPEDECELLUS/KNAT1 homologue NtBP-Like (NtBPL) was significantly up-regulated in NtSVP-RNAi plants. Disruption of NtBPL decreased pedicel lengths and shortened cortex cells. Consistent with the presence of a CArG-box at the NtBPL promoter, the direct binding of NtSVP to the NtBPL promoter was demonstrated by yeast one-hybrid assay, electrophoretic mobility shift assay, and dual-luciferase assay, in which NtSVP may act as a repressor of NtBPL. Microarray analysis showed that down-regulation of NtBPL resulted in differential expression of genes associated with a number of hormone biogenesis and signalling genes such as those for auxin and gibberellin. These findings together suggest the function of a MADS-box transcription factor in plant pedicel development, probably via negative regulation of a BP-like class I KNOX gene. The present work thus postulates the conservation and divergence of the molecular regulatory pathways underlying the development of plant inflorescence architecture.
PMCID: PMC4588881  PMID: 26175352
BP; gibberellin; MADS-box transcription factor; pedicel; SVP; tobacco.
15.  A Factor Linking Floral Organ Identity and Growth Revealed by Characterization of the Tomato Mutant unfinished flower development (ufd) 
Floral organogenesis requires coordinated interactions between genes specifying floral organ identity and those regulating growth and size of developing floral organs. With the aim to isolate regulatory genes linking both developmental processes (i.e., floral organ identity and growth) in the tomato model species, a novel mutant altered in the formation of floral organs was further characterized. Under normal growth conditions, floral organ primordia of mutant plants were correctly initiated, however, they were unable to complete their development impeding the formation of mature and fertile flowers. Thus, the growth of floral buds was blocked at an early stage of development; therefore, we named this mutant as unfinished flower development (ufd). Genetic analysis performed in a segregating population of 543 plants showed that the abnormal phenotype was controlled by a single recessive mutation. Global gene expression analysis confirmed that several MADS-box genes regulating floral identity as well as other genes participating in cell division and different hormonal pathways were affected in their expression patterns in ufd mutant plants. Moreover, ufd mutant inflorescences showed higher hormone contents, particularly ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) and strigol compared to wild type. Such results indicate that UFD may have a key function as positive regulator of the development of floral primordia once they have been initiated in the four floral whorls. This function should be performed by affecting the expression of floral organ identity and growth genes, together with hormonal signaling pathways.
PMCID: PMC5098122  PMID: 27872633
flower development; organ growth; phytohormones; transcriptome; Solanum lycopersicum L.; UFD gene
16.  Over-expression of the Gerbera hybrida At-SOC1-like1 gene Gh-SOC1 leads to floral organ identity deterioration 
Annals of Botany  2011;107(9):1491-1499.
Background and Aims
The family of MADS box genes is involved in a number of processes besides controlling floral development. In addition to supplying homeotic functions defined by the ABC model, they influence flowering time and transformation of vegetative meristem into inflorescence meristem, and have functions in roots and leaves. Three Gerbera hybrida At-SOC1-like genes (Gh-SOC1–Gh-SOC3) were identified among gerbera expressed sequence tags.
Evolutionary relationships between SOC1-like genes from gerbera and other plants were studied by phylogenetic analysis. The function of the gerbera gene Gh-SOC1 in gerbera floral development was studied using expression analysis, protein–protein interaction assays and reverse genetics. Transgenic gerbera lines over-expressing or downregulated for Gh-SOC1 were obtained using Agrobacterium transformation and investigated for their floral phenotype.
Key Results
Phylogenetic analysis revealed that the closest paralogues of At-SOC1 are Gh-SOC2 and Gh-SOC3. Gh-SOC1 is a more distantly related paralogue, grouping together with a number of other At-SOC1 paralogues from arabidopsis and other plant species. Gh-SOC1 is inflorescence abundant and no expression was seen in vegetative parts of the plant. Ectopic expression of Gh-SOC1 did not promote flowering, but disturbed the development of floral organs. The epidermal cells of ray flower petals appeared shorter and their shape was altered. The colour of ray flower petals differed from that of the wild-type petals by being darker red on the adaxial side and greenish on the abaxial surface. Several protein–protein interactions with other gerbera MADS domain proteins were identified.
The At-SOC1 paralogue in gerbera shows a floral abundant expression pattern. A late petal expression might indicate a role in the final stages of flower development. Over-expression of Gh-SOC1 led to partial loss of floral identity, but did not affect flowering time. Lines where Gh-SOC1 was downregulated did not show a phenotype. Several gerbera MADS domain proteins interacted with Gh-SOC1.
PMCID: PMC3108810  PMID: 21572092
Gerbera hybrida; MADS box gene; Gh-SOC1; flower development; floral organ identity; gene transfer
17.  PEP1 of Arabis alpina Is Encoded by Two Overlapping Genes That Contribute to Natural Genetic Variation in Perennial Flowering 
PLoS Genetics  2012;8(12):e1003130.
Higher plants exhibit a variety of different life histories. Annual plants live for less than a year and after flowering produce seeds and senesce. By contrast perennials live for many years, dividing their life cycle into episodes of vegetative growth and flowering. Environmental cues control key check points in both life histories. Genes controlling responses to these cues exhibit natural genetic variation that has been studied most in short-lived annuals. We characterize natural genetic variation conferring differences in the perennial life cycle of Arabis alpina. Previously the accession Pajares was shown to flower after prolonged exposure to cold (vernalization) and only for a limited period before returning to vegetative growth. We describe five accessions of A. alpina that do not require vernalization to flower and flower continuously. Genetic complementation showed that these accessions carry mutant alleles at PERPETUAL FLOWERING 1 (PEP1), which encodes a MADS box transcription factor orthologous to FLOWERING LOCUS C in the annual Arabidopsis thaliana. Each accession carries a different mutation at PEP1, suggesting that such variation has arisen independently many times. Characterization of these alleles demonstrated that in most accessions, including Pajares, the PEP1 locus contains a tandem arrangement of a full length and a partial PEP1 copy, which give rise to two full-length transcripts that are differentially expressed. This complexity contrasts with the single gene present in A. thaliana and might contribute to the more complex expression pattern of PEP1 that is associated with the perennial life-cycle. Our work demonstrates that natural accessions of A. alpina exhibit distinct life histories conferred by differences in PEP1 activity, and that continuous flowering forms have arisen multiple times by inactivation of the floral repressor PEP1. Similar phenotypic variation is found in other herbaceous perennial species, and our results provide a paradigm for how characteristic perennial phenotypes might arise.
Author Summary
Perennial plants live for many years and cycle between flowering and vegetative growth. These stages of the life cycle are often initiated by environmental conditions and occur seasonally. However, many herbaceous perennial species such as strawberry, rose, or Arabis alpina contain varieties that flower continuously irrespective of the seasons. Here we characterize this genetic variation in A. alpina and show that five continuously flowering accessions carry independent mutations in the PERPETUAL FLOWERING 1 (PEP1) gene. These mutations impair the activity of the PEP1 floral repressor causing the plants to flower without requirement for winter cold and to flower continuously. This result has interesting parallels with strawberry and rose, where inactivation of a different floral repressor controlling response to day length gives rise to naturally occurring perpetual flowering forms. We also show that PEP1 in A. alpina has a complex duplicated structure that gives rise to two overlapping transcripts. This arrangement differs from the simple structure of PEP1 orthologues in related annual species, such as FLC of Arabidopsis thaliana, suggesting that duplication of PEP1 might contribute to the complex transcriptional patterns associated with PEP1 function in perennials. Our work provides insight into genetic variation contributing to the perennial life history of plants.
PMCID: PMC3527215  PMID: 23284298
18.  Inflorescence development in tomato: gene functions within a zigzag model 
Tomato is a major crop plant and several mutants have been selected for breeding but also for isolating important genes that regulate flowering and sympodial growth. Besides, current research in developmental biology aims at revealing mechanisms that account for diversity in inflorescence architectures. We therefore found timely to review the current knowledge of the genetic control of flowering in tomato and to integrate the emerging network into modeling attempts. We developed a kinetic model of the tomato inflorescence development where each meristem was represented by its “vegetativeness” (V), reflecting its maturation state toward flower initiation. The model followed simple rules: maturation proceeded continuously at the same rate in every meristem (dV); floral transition and floral commitment occurred at threshold levels of V; lateral meristems were initiated with a gain of V (ΔV) relative to the V level of the meristem from which they derived. This last rule created a link between successive meristems and gave to the model its zigzag shape. We next exploited the model to explore the diversity of morphotypes that could be generated by varying dV and ΔV and matched them with existing mutant phenotypes. This approach, focused on the development of the primary inflorescence, allowed us to elaborate on the genetic regulation of the kinetic model of inflorescence development. We propose that the lateral inflorescence meristem fate in tomato is more similar to an immature flower meristem than to the inflorescence meristem of Arabidopsis. In the last part of our paper, we extend our thought to spatial regulators that should be integrated in a next step for unraveling the relationships between the different meristems that participate to sympodial growth.
PMCID: PMC3978268  PMID: 24744766
Solanum lycopersicum; flowering; morphogenesis; sympodial growth; biological model; AGL24
19.  Characterization of vegetative inflorescence (mc-vin) mutant provides new insight into the role of MACROCALYX in regulating inflorescence development of tomato 
Scientific Reports  2016;6:18796.
Inflorescence development is a key factor of plant productivity, as it determines flower number. Therefore, understanding the mechanisms that regulate inflorescence architecture is critical for reproductive success and crop yield. In this study, a new mutant, vegetative inflorescence (mc-vin), was isolated from the screening of a tomato (Solanum lycopersicum L.) T-DNA mutant collection. The mc-vin mutant developed inflorescences that reverted to vegetative growth after forming two to three flowers, indicating that the mutated gene is essential for the maintenance of inflorescence meristem identity. The T-DNA was inserted into the promoter region of the MACROCALYX (MC) gene; this result together with complementation test and expression analyses proved that mc-vin is a new knock-out allele of MC. Double combinations between mc-vin and jointless (j) and single flower truss (sft) inflorescence mutants showed that MC has pleiotropic effects on the reproductive phase, and that it interacts with SFT and J to control floral transition and inflorescence fate in tomato. In addition, MC expression was mis-regulated in j and sft mutants whereas J and SFT were significantly up-regulated in the mc-vin mutant. Together, these results provide new evidences about MC function as part of the genetic network regulating the development of tomato inflorescence meristem.
PMCID: PMC4698712  PMID: 26727224
20.  Papilionoid inflorescences revisited (Leguminosae-Papilionoideae) 
Annals of Botany  2012;112(8):1567-1576.
Background and Aims
The inflorescence structure determines the spatiotemporal arrangement of the flowers during anthesis and is therefore vital for reproductive success. The Leguminosae are among the largest angiosperm plant families and they include some important crop plants. In papilionoid legumes, the raceme is the most common type of inflorescence. However, a range of other inflorescence types have evolved via various developmental processes. A (re-)investigation of inflorescences in Swainsona formosa, Cicer arietinum, Abrus precatorius, Hardenbergia violacea and Kennedia nigricans leads to new insights into reduction mechanisms and to a new hypothesis on the evolution of the papilionoid pseudoraceme.
Inflorescence morphology and ontogeny were studied using scanning electron microscopy (SEM).
Key Results
The inflorescence in S. formosa is an umbel with a rare type of pendulum symmetry which may be triggered by the subtending leaf. Inflorescences in C. arietinum are reduced to a single flower. An early formed adaxial bulge is the sterile apex of the inflorescence (i.e. the inflorescence is open and not terminated by a flower). In partial inflorescences of A. precatorius, the axis is reduced and its meristem is relocated towards the main inflorescence. Flower initiation follows a peculiar pendulum pattern. Partial inflorescences in H. violacea and in K. nigricans show reduction tendencies. In both taxa, initiated but early reduced bracteoles are present.
Pendulum symmetry in S. formosa is probably associated with distichous phyllotaxis. In C. arietinum, strong reduction tendencies are revealed. Based on studies of A. precatorius, the papilionoid pseudoraceme is reinterpreted as a compound raceme with condensed lateral axes. From an Abrus-like inflorescence, other types can be derived via reduction of flower number and synchronization of flower development. A plea is made for uniform usage of inflorescence terminology.
PMCID: PMC3828940  PMID: 23235698
Abrus precatorius; Cicer arietinum; Hardenbergia violacea; Kennedia nigricans; inflorescence; Leguminosae; Papilionoideae; pseudoraceme; Swainsona formosa
21.  SEP-class genes in Prunus mume and their likely role in floral organ development 
BMC Plant Biology  2017;17:10.
Flower phylogenetics and genetically controlled development have been revolutionised during the last two decades. However, some of these evolutionary aspects are still debatable. MADS-box genes are known to play essential role in specifying the floral organogenesis and differentiation in numerous model plants like Petunia hybrida, Arabidopsis thaliana and Antirrhinum majus. SEPALLATA (SEP) genes, belonging to the MADS-box gene family, are members of the ABCDE and quartet models of floral organ development and play a vital role in flower development. However, few studies of the genes in Prunus mume have yet been conducted.
In this study, we cloned four PmSEPs and investigated their phylogenetic relationship with other species. Expression pattern analyses and yeast two-hybrid assays of these four genes indicated their involvement in the floral organogenesis with PmSEP4 specifically related to specification of the prolificated flowers in P. mume. It was observed that the flower meristem was specified by PmSEP1 and PmSEP4, the sepal by PmSEP1 and PmSEP4, petals by PmSEP2 and PmSEP3, stamens by PmSEP2 and PmSEP3 and pistils by PmSEP2 and PmSEP3.
With the above in mind, flower development in P. mume might be due to an expression of SEP genes. Our findings can provide a foundation for further investigations of the transcriptional factors governing flower development, their molecular mechanisms and genetic basis.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-016-0954-6) contains supplementary material, which is available to authorized users.
PMCID: PMC5234111  PMID: 28086797
SEP genes; Prunus mume; Floral organ development; Expression analysis; Yeast two-hybrid assay
22.  Cell-type specific analysis of translating RNAs in developing flowers reveals new levels of control 
Combining translating ribosome affinity purification with RNA-seq for cell-specific profiling of translating RNAs in developing flowers.Cell type comparisons of cell type-specific hormone responses, promoter motifs, coexpressed cognate binding factor candidates, and splicing isoforms.Widespread post-transcriptional regulation at both the intron splicing and translational stages.A new class of noncoding RNAs associated with polysomes.
What constitutes a differentiated cell type? How much do cell types differ in their transcription of genes? The development and functions of tissues rely on constant interactions among distinct and nonequivalent cell types. Answering these questions will require quantitative information on transcriptomes, proteomes, protein–protein interactions, protein–nucleic acid interactions, and metabolomes at cellular resolution. The systems approaches emerging in biology promise to explain properties of biological systems based on genome-wide measurements of expression, interaction, regulation, and metabolism. To facilitate a systems approach, it is essential first to capture such components in a global manner, ideally at cellular resolution.
Recently, microarray analysis of transcriptomes has been extended to a cellular level of resolution by using laser microdissection or fluorescence-activated sorting (for review, see Nelson et al, 2008). These methods have been limited by stresses associated with cellular separation and isolation procedures, and biases associated with mandatory RNA amplification steps. A newly developed method, translating ribosome affinity purification (TRAP; Zanetti et al, 2005; Heiman et al, 2008; Mustroph et al, 2009), circumvents these problems by epitopetagging a ribosomal protein in specific cellular domains to selectively purify polysomes. We combined TRAP with deep sequencing, which we term TRAP-seq, to provide cell-level spatiotemporal maps for Arabidopsis early floral development at single-base resolution.
Flower development in Arabidopsis has been studied extensively and is one of the best understood aspects of plant development (for review, see Krizek and Fletcher, 2005). Genetic analysis of homeotic mutants established the ABC model, in which three classes of regulatory genes, A, B and C, work in a combinatorial manner to confer organ identities of four whorls (Coen and Meyerowitz, 1991). Each class of regulatory gene is expressed in a specific and evolutionarily conserved domain, and the action of the class A, B and C genes is necessary for specification of organ identity (Figure 1A).
Using TRAP-seq, we purified cell-specific translating mRNA populations, which we and others call the translatome, from the A, B and C domains of early developing flowers, in which floral patterning and the specification of floral organs is established. To achieve temporal specificity, we used a floral induction system to facilitate collection of early stage flowers (Wellmer et al, 2006). The combination of TRAP-seq with domain-specific promoters and this floral induction system enabled fine spatiotemporal isolation of translating mRNA in specific cellular domains, and at specific developmental stages.
Multiple lines of evidence confirmed the specificity of this approach, including detecting the expression in expected domains but not in other domains for well-studied flower marker genes and known physiological functions (Figures 1B–D and 2A–C). Furthermore, we provide numerous examples from flower development in which a spatiotemporal map of rigorously comparable cell-specific translatomes makes possible new views of the properties of cell domains not evident in data obtained from whole organs or tissues, including patterns of transcription and cis-regulation, new physiological differences among cell domains and between flower stages, putative hormone-active centers, and splicing events specific for flower domains (Figure 2A–D). Such findings may provide new targets for reverse genetics studies and may aid in the formulation and validation of interaction and pathway networks.
Beside cellular heterogeneity, the transcriptome is regulated at several steps through the life of mRNA molecules, which are not directly available through traditional transcriptome profiling of total mRNA abundance. By comparing the translatome and transcriptome, we integratively profiled two key posttranscriptional control points, intron splicing and translation state. From our translatome-wide profiling, we (i) confirmed that both posttranscriptional regulation control points were used by a large portion of the transcriptome; (ii) identified a number of cis-acting features within the coding or noncoding sequences that correlate with splicing or translation state; and (iii) revealed correlation between each regulation mechanism and gene function. Our transcriptome-wide surveys have highlighted target genes transcripts of which are probably under extensive posttranscriptional regulation during flower development.
Finally, we reported the finding of a large number of polysome-associated ncRNAs. About one-third of all annotated ncRNA in the Arabidopsis genome were observed co-purified with polysomes. Coding capacity analysis confirmed that most of them are real ncRNA without conserved ORFs. The group of polysome-associated ncRNA reported in this study is a potential new addition to the expanding riboregulator catalog; they could have roles in translational regulation during early flower development.
Determining both the expression levels of mRNA and the regulation of its translation is important in understanding specialized cell functions. In this study, we describe both the expression profiles of cells within spatiotemporal domains of the Arabidopsis thaliana flower and the post-transcriptional regulation of these mRNAs, at nucleotide resolution. We express a tagged ribosomal protein under the promoters of three master regulators of flower development. By precipitating tagged polysomes, we isolated cell type-specific mRNAs that are probably translating, and quantified those mRNAs through deep sequencing. Cell type comparisons identified known cell-specific transcripts and uncovered many new ones, from which we inferred cell type-specific hormone responses, promoter motifs and coexpressed cognate binding factor candidates, and splicing isoforms. By comparing translating mRNAs with steady-state overall transcripts, we found evidence for widespread post-transcriptional regulation at both the intron splicing and translational stages. Sequence analyses identified structural features associated with each step. Finally, we identified a new class of noncoding RNAs associated with polysomes. Findings from our profiling lead to new hypotheses in the understanding of flower development.
PMCID: PMC2990639  PMID: 20924354
Arabidopsis; flower; intron; transcriptome; translation
23.  Reproductive investment within inflorescences of Stylidium armeria varies with the strength of early resource commitment 
Annals of Botany  2010;105(5):697-705.
Background and Aims
Resource allocation to flowers, fruits and seeds can vary greatly within an inflorescence. For example, distal fruits are often smaller and produce fewer and smaller fruits and seeds than more basal fruits. To assess the causes and functional significance of intra-inflorescence variation, pollen and resources were manipulated to test whether such patterns could be altered within racemes of Stylidum armeria, a perennial Australian herb.
Pollen and resource levels were manipulated over two flowering seasons. How the number of ovules, fertilized ovules and seeds, the probability of fruit set, and the biomass of floral and fruiting structures varied with their position on the raceme were analysed.
Key Results
Most plants showed a decline in ovule and seed number toward the distal positions on the raceme, but plants differed in their pattern of intra-inflorescence allocation: racemes with greater investment in basal fruits displayed a stronger trade-off with distal investment than did racemes that made smaller initial investments. This trade-off was (a) much stronger for ovule number than for seed number, (b) ameliorated but not erased by resource addition, and (c) exacerbated by resource reduction. There was large and seemingly erratic variation across fruit positions in ovule fertilization and seed set following both natural and supplemental pollination.
In S. armeria, allocation to reproductive traits within the inflorescence is influenced by dynamic trade-offs in resource allocation between early and late fruits, and may also be subject to inherent architectural effects. Large, unpredictable variation among fruits in fertilization success and seed set may influence the evolution of inflorescence size, ovule number and floral dimorphism.
PMCID: PMC2859907  PMID: 20375201
Architectural effects; floral biomass; intra-inflorescence; pollen limitation; resource pre-emption; Stylidium armeria
24.  The making of a bushy grass with a branched flowering stem 
Plant Signaling & Behavior  2008;3(11):981-983.
In Arabidopsis thaliana, a eudicot species, the transcription factor LFY is expressed throughout the floral meristem and promotes their formation. The expression pattern of the rice LFY homolog-RFL shows distinct differences from that of its Arabidopsis counterpart. In the March issue of PNAS (2008) we have shown the temporally-regulated high-level expression of RFL in the apical meristem is necessary for its transition to an inflorescence meristem and thus to initiate flowering. RFL controls the time taken for flowering, by activating integrators of flowering signals such as OsSOC1 and RFT1. Further, the dynamic pattern of RFL expression in the branching inflorescence meristem (panicle) and in vegetative axillary meristems (tiller buds) is required for panicle branching and tiller outgrowth. Thus RFL functions determine the architecture of the rice plant. Here we propose a plausible model for a regulatory feedback loop between RFL and OsSOC1/RFT1 in controlling the vegetative to flowering phase transition. We discuss the possibility that non-cell autonomous RFL functions may also regulate signaling the net outcome of which determines the rice plant body plan.
PMCID: PMC2633749  PMID: 19704426
RFL; rice flowering time; plant architecture; signaling; regulatory feedback loop
25.  The role of BoFLC2 in cauliflower (Brassica oleracea var. botrytis L.) reproductive development 
Journal of Experimental Botany  2014;66(1):125-135.
Genetic, association, and expression studies indicate that a mutation in BoFLC2 explains much of the variability in cauliflower curd formation, curd growth rate, and flowering time.
In agricultural species that are sexually propagated or whose marketable organ is a reproductive structure, management of the flowering process is critical. Inflorescence development in cauliflower is particularly complex, presenting unique challenges for those seeking to predict and manage flowering time. In this study, an integrated physiological and molecular approach was used to clarify the environmental control of cauliflower reproductive development at the molecular level. A functional allele of BoFLC2 was identified for the first time in an annual brassica, along with an allele disrupted by a frameshift mutation (boflc2). In a segregating F2 population derived from a cross between late-flowering (BoFLC2) and early-flowering (boflc2) lines, this gene behaved in a dosage-dependent manner and accounted for up to 65% of flowering time variation. Transcription of BoFLC genes was reduced by vernalization, with the floral integrator BoFT responding inversely. Overall expression of BoFT was significantly higher in early-flowering boflc2 lines, supporting the idea that BoFLC2 plays a key role in maintaining the vegetative state. A homologue of Arabidopsis VIN3 was isolated for the first time in a brassica crop species and was up-regulated by two days of vernalization, in contrast to findings in Arabidopsis where prolonged exposure to cold was required to elicit up-regulation. The correlations observed between gene expression and flowering time in controlled-environment experiments were validated with gene expression analyses of cauliflowers grown outdoors under ‘natural’ vernalizing conditions, indicating potential for transcript levels of flowering genes to form the basis of predictive assays for curd initiation and flowering time.
PMCID: PMC4265156  PMID: 25355864
BoFLC; BoFT; BoVIN3; Brassica oleracea; cauliflower; expression; flowering time; vernalization.

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