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Molecular-Basis of the Cauliflower Phenotype in Arabidopsis
Abstract
Genetic studies demonstrate that two Arabidopsis genes, CAULIFLOWER and APETALA1, encode partially redundant activities involved
in the formation of floral meristems, the first step in the development of flowers. Isolation of the CAULIFLOWER gene from
Arabidopsis reveals that it is closely related in sequence to APETALA1. Like APETALA1, CAULIFLOWER is expressed in young flower
primordia and encodes a MADS-domain, indicating that it may function as a transcription factor. Analysis of the cultivated
garden variety of cauliflower (Brassica oleracea var. botrytis) reveals that its CAULIFLOWER gene homolog is not functional,
suggesting a molecular basis for one of the oldest recognized flower abnormalities.
... Paralogs in compensatory drift are more likely to display unequal redundancy, as highlighted by several classical examples from Arabidopsis. These include unequal redundancy between the MADS-box transcription factors APETALA1 and CAULI-FLOWER that control the formation of floral meristems (Bowman et al., 1993;Kempin et al., 1995), the leucine-rich repeat receptorlike kinases ERECTA and ERECTA LIKE1/ERECTA LIKE2 that control organ growth and development (Shpak et al., 2004), and the MYB-related transcription factors LONG HYPOCOTYL5 and HY5 HOMOLOG involved in light signaling (Holm et al., 2002;Briggs et al., 2006). The numerous cases of partial and unequal redundancy suggest that these are evolutionary stable states for ancient paralogs (Briggs et al., 2006). ...
... An excellent example of a transcriptional RBC is represented by the Arabidopsis thaliana APETALA1 (AP1) and CAULIFLOWER (CAL) genes, two paralog MADS-box genes whose expression levels diverged in the floral primordia and developing sepals and petals (Bowman et al., 1993). In the ap1 single mutant, flower meristems are partially converted into inflorescence meristems (Bowman et al., 1993;Kempin et al., 1995). This phenotype is significantly enhanced in the ap1;cal double mutant (Bowman et al., 1993;Kempin et al., 1995). ...
... In the ap1 single mutant, flower meristems are partially converted into inflorescence meristems (Bowman et al., 1993;Kempin et al., 1995). This phenotype is significantly enhanced in the ap1;cal double mutant (Bowman et al., 1993;Kempin et al., 1995). AP1 expression is significantly lower in the ap1;cal double mutant, but not in the ap1 single mutant, leading to the hypothesis that AP1 is positively regulated by CAL (Bowman et al., 1993). ...
Gene duplication is a powerful source of biological innovation giving rise to paralogous genes that undergo diverse fates. Redundancy between paralogous genes is an intriguing outcome of duplicate gene evolution, and its maintenance over evolutionary time has long been considered a paradox. Redundancy can also be dubbed ‘a geneticist's nightmare’: It hinders the predictability of genome editing outcomes and limits our ability to link genotypes to phenotypes. Genetic studies in yeast and plants have suggested that the ability of ancient redundant duplicates to compensate for dosage perturbations resulting from a loss of function depends on the reprogramming of gene expression, a phenomenon known as active compensation. Starting from considerations on the stoichiometric constraints that drive the evolutionary stability of redundancy, this review aims to provide insights into the mechanisms of active compensation between duplicates that could be targeted for breaking paralog dependencies – the next frontier in plant functional studies.
... In today's world where a lot of molecular studies are being performed in plants, it has also been well emphasised that broccoli, an edible crop that's widely sold, is the closest cultivated relative of cauliflower. This deduction is made with possiblities that the phenotype of cauliflower is more likely caused by a defective CAL gene, as tested and confirmed in a study performed on Arabidopsis [6,8]. Therefore, the abnormal flowering, or flowers, of cauliflower are likely to have arisen from the floral stem primordia of cauliflower, and as a result of this mutant CAL gene [8], the flowers of cauliflower have lost their identity [5]. ...
... Furthermore, in cauliflower, although the primordia at the apex of each elongating shoot, the meristem, grow and develop into leaves, the later primordia fails to produce flower buds. It is, therefore, the meristem of the stem that continuously replicates itself in a spiral fashion, and the continuation of this up to the 10th order of branching, or more, causes the phenotype of cauliflower to be made of undifferentiated inflorescence meristems that are closely packed and clustered geometrically [5,6,8]. This texture of plants found in the family Brassicaceae is novel, and it's absent in wildtype plants [9, 10]. ...
... tfl1, flc, tfc2, co, fy, art1, emf1, efs, fha, gi, hy2, and vrn1, are all flower-associated gene, which participate in the genetic control of complete traits in the genus, Brassica. CAULI-FLOWER and APETALA1, are responsible for the curd-like inflorescence in Arabidopsis, however, the architecture of the curd produced, is far more complex, and, thus, it is under much complex genetic control mechanisms [8]. Therefore, the genome of Brassica is able to provide further clarity and insight about the size and shape of plants. ...
Many years ago, the first Brassica species were propagated. There are several methods that can be used to grow Brassica plants, such as intergeneric hybridization, microscope cultivation, anther cultivation, CRISPR/Cas4 Technology and the phylogenetic analysis of Brassica genomes. The plants that have evolved from Brassica species are many, and these include Savoy cabbage, broccoli, mustard greens, Japanese mustard, horseradish, as well as kale. Although the main supplier of Brassica vegetables is China, these species have diverged and emerged to several other countries like Cyprus, Europe, Levant, Greece and the British Isles. Ogura cytoplasm introgression is a technique that has highlighted the differences in floral traits in species of Brassica plants. In cauliflower plants, pre-floral meristem division is a factor that’s often investigated, as divisions of this plant part demonstrates plant growth and mobility. This perspective chapter will address all aspects pertaining to the genus Brassica, and it will provide an account of key characteristics and functions ascribed to Brassica plants.
... The distinction between shoot and floral meristems is maintained by two complementary sets of genes. First, floral fate depends upon the action of meristem identity genes such as LEAFY (LFY), APETALA 1 (AP1), and CAULIFLOWER (CAL) (Mandel et al., 1992;Weigel et al., 1992;Bowman et al., 1993;Gustafson-Brown et al., 1994;Kempin et al., 1995;Mandel and Yanofsky, 1995;Weigel and Nilsson;. Secondly, a group of genes, including TERMINAL FLOWER 1 (TFL1), prevent the shoot from becoming a flower by retarding progression through all growth phases (Ratcliffe et al., 1998). ...
... In wild type, TFL1 and the floral meristem identity genes are expressed in separate domains (Fig. 1). Both types of genes are most strongly expressed during inflorescence development, with TFL1 in the centre of the apex and floral meristem identity genes on its periphery (Mandel et al., 1992;Weigel et al., 1992;Kempin et al., 1995;Bradley et al., 1997). A similar separation is also observed between low levels of TFL1 and LFY expression during vegetative growth (Bradley et al., 1997;Blazquez et al., 1997Blazquez et al., , 1998Hempel et al., 1997). ...
... These observations show that AP1 activity is not needed to prevent TFL1 expression in floral meristems. However, the AP1 gene is known to show functional redundancy with a highly homologous gene, CAL (Bowman, 1992;Bowman et al., 1993;Kempin et al., 1995). This raised the possibility that CAL could also contribute to the inhibition of TFL1. ...
The overall morphology of an Arabidopsis plant depends on the behaviour of its meristems. Meristems derived from the shoot apex can develop into either shoots or flowers. The distinction between these alternative fates requires separation between the function of floral meristem identity genes and the function of an antagonistic group of genes, which includes TERMINAL FLOWER 1. We show that the activities of these genes are restricted to separate domains of the shoot apex by different mechanisms. Meristem identity genes, such as LEAFY, APETALA 1 and CAULIFLOWER, prevent TERMINAL FLOWER 1transcription in floral meristems on the apex periphery.
TERMINAL FLOWER 1, in turn, can inhibit the activity of meristem identity genes at the centre of the shoot apex in two ways; first by delaying their upregulation, and second, by preventing the meristem from responding to LEAFY or APETALA 1. We suggest that the wild-type pattern of TERMINAL FLOWER 1 and floral meristem identity gene expression depends on the relative timing of their upregulation.
... Curd biogenesis is a complex process regulated by multiple developmental signals and environmental factors 10,12,13 , involving vernalization 14 , photoperiod 15 , gibberellin 16 , and autonomous 17 flowering-related pathways. In cauliflower and Arabidopsis, several important curd-biogenesis-related genes have been identified, including MADS-box genes CAULIFLOWER (CAL/AGL10), APETALA1 (AP1/AGL7) 18 , FRUITFULL (FUL/AGL8) 19 , SUPPRESSOR OF OVEREXPRES-SION OF CO 1 (SOC1/AGL20) 20 , AGAMOUSLIKE 24 (AGL24) 21 and XAAN-TAL2 (XAL2/AGL14) 22 , as well as phosphatidylethanolamine-binding protein TERMINAL FLOWER 1 (TFL1) 23 and a plant-specific transcription factor gene, LEAFY (LFY) 24 . The nested-spiral pattern of cauliflower curd has been preliminarily deciphered using a three-dimensional computational model 13 . ...
... varied between the Curdless and Green-curd categories (Fig. 3d), potentially affecting their function through transcriptional regulation. These findings are consistent with those of a previous study in Arabidopsis showing that CAL and AP1 control the 'curd-like' phenotype, which arises from an abnormal inflorescence meristem 18 . More informatively, we found that the promoter region of FUL2, a gene controlling meristem arrest and lifespan in Arabidopsis 19 , further differed between the Green-curd and White-curd categories. ...
Cauliflower (Brassica oleracea L. var. botrytis) is a distinctive vegetable that supplies a nutrient-rich edible inflorescence meristem for the human diet. However, the genomic bases of its selective breeding have not been studied extensively. Herein, we present a high-quality reference genome assembly C-8 (V2) and a comprehensive genomic variation map consisting of 971 diverse accessions of cauliflower and its relatives. Genomic selection analysis and deep-mined divergences were used to explore a stepwise domestication process for cauliflower that initially evolved from broccoli (Curd-emergence and Curd-improvement), revealing that three MADS-box genes, CAULIFLOWER1 (CAL1), CAL2 and FRUITFULL (FUL2), could have essential roles during curd formation. Genome-wide association studies identified nine loci significantly associated with morphological and biological characters and demonstrated that a zinc-finger protein (BOB06G135460) positively regulates stem height in cauliflower. This study offers valuable genomic resources for better understanding the genetic bases of curd biogenesis and florescent development in crops.
... Their fractal-like shape derives from a modification of the flower development process. Strikingly, a cauliflower-like severe change of morphology is produced by mutations of the APETALA1 (AP1) and CAULIFLOWER (CAL) genes in Arabidopsis thaliana [3,4], a brassicaceae from the same family as the cauliflower and broccoli (Figure 1a, b). In a recent work [5], we provided a mechanistic explanation of how these mutations alter flower development, by recursively triggering lateral meristem development, which results in the fractal-like shape of the curds. ...
... AP1 inhibits shoot identity by repressing TFL1 in FM [7,12,13] and stabilises the expression of floral regulators by forming a positive feedback loop with LFY ( Figure 2a) [6][7][8][9][10][14][15][16][17]. In A. thaliana, the double mutant of ap1 cal, produces cauliflower-like structures instead of flowers [3,4,6]. Those structures correspond to meristems initiated as floral (with LFY expression) but that revert to shoot (with TFL1 expression) because the AP1/CAL-LFY positive feedback is missing (Figure 2c). ...
Biological organisms have an immense diversity of forms. Some of them exhibit conspicuous and fascinating fractal structures that present self-similar patterns at all scales. How such structures are produced by biological processes is intriguing. In a recent publication, we used a multi-scale modelling approach to understand how gene activity can produce macroscopic cauliflower curds. Our work provides a plausible explanation for the appearance of fractal-like structures in plants, linking gene activity with development.
... Studies had shown that high expression of SVP resulted in smaller flowers and also inhibited the flowering process in most dicotyledonous plants (Jaudal et al., 2014). In addition to this, AGL12 suppressed the process of flowering transformation in plants, while FUL promoted the formation of inflorescence meristematic tissue in plants at an early stage of flower development (Kempin et al., 1995;Li et al., 2008;Tapia-Lopez et al., 2008). The results of some other studies showed that both SVP and AGL12 inhibited flowering transition, while FUL promoted the formation of inflorescence meristem at the early stage of flower development (Kempin et al., 1995;Li et al., 2008;Tapia-Lopez et al., 2008). ...
... In addition to this, AGL12 suppressed the process of flowering transformation in plants, while FUL promoted the formation of inflorescence meristematic tissue in plants at an early stage of flower development (Kempin et al., 1995;Li et al., 2008;Tapia-Lopez et al., 2008). The results of some other studies showed that both SVP and AGL12 inhibited flowering transition, while FUL promoted the formation of inflorescence meristem at the early stage of flower development (Kempin et al., 1995;Li et al., 2008;Tapia-Lopez et al., 2008). It can be seen from the results of this study that the expression levels of SVP and AGL12 in H. attenuatum were higher than those in H. longistylum, while the expression levels of FUL were lower than those in H. longistylum. ...
To explore the differences between the hypericum in the Changbai Mountains, we carried out a transcriptome analysis of two common hypericums in the area, which was Hypericum attenuatum Choisy and Hypericum longistylum Oliv. We screened the MADS-box genes to analyze divergence time and evolutionary selection expression, and determine their expression levels. The results showed that we detected 9287 differentially expressed genes in the two species, of which shared 6044 genes by the two species. Analysis of the selected MADS genes revealed that the species was in an environment adapted to its natural evolution. The divergence time estimation showed that the segregation of these genes in the two species was related to the changes of external environment and genome replication events. The results of relative expression showed that the later flowering period of Hypericum attenuatum Choisy was related to the higher expression of the SVP (SHORT VEGETATIVE PHASE) and the AGL12 (AGAMOUS LIKE 12), while the lower expression of the FUL (FRUITFULL).
... AP1 and CAL have only a few amino acid differences in the K region of MADS, most of which are conserved, and these differences play a key role in determining their functional differences. AP1 and CAL have a partially redundant function in the development of Arabidopsis flowers (Mandel et al., 1992;Kempin et al., 1995). In addition, Ferrándiz et al. (2000) found that another MADS-box Abbreviations: aa, amino acid(s); bp, base pair(s); Y2H, Yeast two-hybrid; SEP, SEPALLATA; SVP, SHORT VEGETATIVE PHASE; SOC1, SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1; Di19-4, Dehydration-induced 19 homologue 4; KNO3, potassium nitrate; PBZ, paclobutrazol; FT, FLOWERING LOCUS T; AP1, APETALA1; CO, CONSTANS; FUL, FRUITFULL; LFY, LEAFY; AGL24, AGAMOUE-like24; TFL1, TERMINAL FLOWER1; DAPI, 4,6-diamidino-2-phenylindole; cDNA, complementary DNA; qRT-PCR, real-time quantitative PCR; WT, wild type. ...
... AP1, FUL and CAL all encode closely related transcription factors of the MADS domain and exhibit redundancy in the process of floral meristem identity development (Lawton-Rauh et al., 1999;McCarthy et al., 2015). Many copies of the AP1/FUL/CAL gene have been found in plants, such as four AP1 copies in soybean , two AP1 copies in mango , three FUL copies in Platanus acerifolia (Zhang et al., 2018), and one CAL copy each in Arabidopsis and Chinese cabbage (Kempin et al., 1995;Li et al., 2000). In the present study, two CAL genes, namely, MiCAL1 and MiCAL2, were found in mango. ...
CAULIFLOWER (CAL) genes and APETALA1 (AP1) genes are two closely related genes with redundant functions, both of which have unique functions in the process of flower meristem formation in Arabidopsis thaliana. MiCAL homologous genes play a key role in flower transformation and flower morphogenesis in Arabidopsis. Two CAL genes, MiCAL1 and MiCAL2, were cloned from mango (Mangifera indica L.). Its full-length sequence was 717 bp and 714 bp, encoding 239 and 238 amino acids, respectively. Both the MiCAL1 and MiCAL2 proteins contained typical MADS-box and K-box domains and therefore belonged to the CAL-like protein family. MiCAL1 and MiCAL2 were expressed in all tissues at the inflorescence elongation stage and flowering stage, with the highest expression in the leaves at the flowering stage. They have similar expression patterns during flower development, with the highest expression levels in leaves during flower differentiation and the lowest expression levels during fruit development. Overexpression of MiCAL1 and MiCAL2 resulted in the flowering of Arabidopsis significantly earlier. Overexpression of MiCAL1 resulted in terminal flowers with normal flower organs, while overexpression of MiCAL2 induced partial variation in floral organs but had no effect on inflorescences. Yeast two-hybrid (Y2H) experiments showed that MiCAL1 and MiCAL2 can interact with several flower-related proteins as well as stress response proteins, such as SEP1, SVP1, SVP2, SOC1G and Di19-4. These results suggest that these two MiCAL genes may have an important influence on mango flowering.
... Overexpression of AP1 leads to remarkable early flowering and transformation of inflorescence shoot apical meristem into floral meristem [25]. In single Arabidopsis cal mutants, there are no remarkable changes in floral organs, but the cal mutation enhances the repetitive branching pattern in the floral meristem of ap1 mutants [24,26]. In other core eudicots, the ap1 mutation only changes the sepal structure, but it does not affect petal structure [27,28]. ...
... In Arabidopsis, AP1 is an early-acting gene, and it functions as a class A gene to specify sepal and petal identity [22,63]. AP1 is expressed in floral meristems and developing sepal and petal primordia [22,23,26,64]. However, in other core eudicots, the AP1-like genes can also be expressed in bracts and reproductive organs [31,45,65,66]. ...
Members of AP1/FUL subfamily genes play an essential role in the regulation of floral meristem transition, floral organ identity, and fruit ripping. At present, there have been insufficient studies to explain the function of the AP1/FUL-like subfamily genes in Asteraceae. Here, we cloned two euAP1 clade genes TeAP1-1 and TeAP1-2, and three euFUL clade genes TeFUL1, TeFUL2, and TeFUL3 from marigold (Tagetes erecta L.). Expression profile analysis demonstrated that TeAP1-1 and TeAP1-2 were mainly expressed in receptacles, sepals, petals, and ovules. TeFUL1 and TeFUL3 were expressed in flower buds, stems, and leaves, as well as reproductive tissues, while TeFUL2 was mainly expressed in flower buds and vegetative tissues. Overexpression of TeAP1-2 or TeFUL2 in Arabidopsis resulted in early flowering, implying that these two genes might regulate the floral transition. Yeast two-hybrid analysis indicated that TeAP1/FUL proteins only interacted with TeSEP proteins to form heterodimers and that TeFUL2 could also form a homodimer. In general, TeAP1-1 and TeAP1-2 might play a conserved role in regulating sepal and petal identity, similar to the functions of MADS-box class A genes, while TeFUL genes might display divergent functions. This study provides a theoretical basis for the study of AP1/FUL-like genes in Asteraceae species.
... botrytis) were domesticated from the wild Brassica oleracea (2). The cauliflower inflorescence (the flower bearing shoot) takes a curd shape because each emerging flower primordia never fully reaches the floral stage, and repeatedly generates a novel curd-shaped inflorescence instead (3). In B. oleracea, the genetic modifications causing curd development are still debated (4,5). ...
... In B. oleracea, the genetic modifications causing curd development are still debated (4,5). However, cauliflowers also exist in the model brassicaceae Arabidopsis thaliana and are known to be caused by a double mutation in APETALA1 (AP1) and CAULIFLOWER (CAL) (Fig. 1h-i), two paralogous genes encoding MADS-box transcription factors (TF) promoting floral development (3,6). The Arabidopsis networks of molecular regulators governing the development of shoots and flowers have been largely identified. ...
The arrangement of plant organs, called phyllotaxis, produce remarkable spiral or whorled patterns. Cauliflowers present a unique phyllotaxis with a multitude of spirals over a wide range of scales. How such a self-similar fractal organization emerges from developmental mechanisms has remained elusive. Combining experimental assays with modeling, we found that cauliflowers arise due to the hysteresis of the bistable floral network that generates inflorescences imprinted by a transient floral state. We further show how additional mutations affecting meristem growth dynamics can induce the production of conical phyllotactic structures reminiscent of the conspicuous fractal Romanesco shape. This study reveals how the spectacular morphological modification of the inflorescences in cauliflower and Romanesco shape arises from the hysteresis of the genetic programs controlling inflorescence development.
One Sentence Summary
The molecular making of cauliflowers
... For instance, LFY is a key regulator for the establishment of the FM regulatory network [42]. Two Arabidopsis genes, APETALA1 and CAULIFLOWER, have redundant roles in the formation of FM [43]. The AGL6-like MADS-box gene in wheat is a target of spikelet meristem development regulation and is a key regulator of floral organ identity [44]. ...
MADS-box transcription factors act as the crucial regulators in plant organ differentiation. Crop yields are highly influenced by the flower number and fruit growth. However, flower identification is a very complex biological process, which involves many cascade regulations. The molecular mechanisms underlying the genetic regulation of flower identification in cultivated plants, such as tomato, are intricate and require further exploration. In this study, we investigated the vital function of a SEPALLATA (SEP) MADS-box gene, SlMBP21, in tomato sympodial inflorescence meristem (SIM) development for the conversion from SIMs to floral meristems (FMs). SlMBP21 transcripts were primarily accumulated in young inflorescence meristem, flowers, sepals, and abscission zones. The Ailsa Craig (AC++) tomato plants with suppressed SlMBP21 mRNA levels using RNAi exhibited a large increase in flower number and fruit yields in addition to enlarged sepals and inhibited abscission zone development. Scanning electron microscopy (SEM) revealed that the maturation of inflorescence meristems (IMs) was repressed in SlMBP21-RNAi lines. RNA-seq and qRT-PCR analyses showed that numerous genes related to the flower development, plant hormone signal transduction, cell cycle, and cell proliferation et al. were dramatically changed in SlMBP21-RNAi lines. Yeast two-hybrid assay exhibited that SlMBP21 can respectively interact with SlCMB1, SFT, JOINTLESS, and MC, which play key roles in inflorescence meristems or FM development. In summary, our data demonstrate that SlMBP21 functions as a key regulator in SIM development and the conversion from SIMs to FMs, through interacting with other regulatory proteins to control the expression of related genes.
... CAULIFLOWER gene (CAL) was identified by Bowman et al. (1993) showing the same ap1or CAL phenotype in Arabidopsis exhibiting curd resembling cauliflower. The orthologue of this gene was found in cauliflower by Kempin et al. (1995) and was called BoCAL. The following genes, in different genotypes, showed different alleles and one of them named Bocala was responsible of the premature stop codon in exon 5, arresting the inflorescence primordia proliferation (Schilling et al. 2018). ...
... ;https://doi.org/10.1101https://doi.org/10. /2024 We next captured rare shoot stem cells in arabidopsis (Neumann et al., 2022;Zhang et al., 2017), using apetala1; cauliflower (ap1;cal) double mutants, with over proliferating inflorescence meristems ( Figure 1E) (Kempin et al., 1995). The CLV-WUS network is operational in this mutant background (Yadav et al., 2009). ...
Stem cells in plant shoots are a rare population of cells that produce leaves, fruits and seeds, vital sources for food and bioethanol. Uncovering regulators expressed in these stem cells will inform crop engineering to boost productivity. Single-cell analysis is a powerful tool for identifying regulators expressed in specific groups of cells. However, accessing plant shoot stem cells is challenging. Recent single-cell analyses of plant shoots have not captured these cells, and failed to detect stem cell regulators like CLAVATA3 and WUSCHEL. In this study, we finely dissected stem cell-enriched shoot tissues from both maize and arabidopsis for single-cell RNA-seq profiling. We optimized protocols to efficiently recover thousands of CLAVATA3 and WUSCHEL expressed cells. A cross-species comparison identified conserved stem cell regulators between maize and arabidopsis. We also performed single-cell RNA-seq on maize stem cell overproliferation mutants to find additional candidate regulators. Expression of candidate stem cell genes was validated using spatial transcriptomics, and we functionally confirmed roles in shoot development. These candidates include a family of ribosome-associated RNA-binding proteins, and two families of sugar kinase genes related to hypoxia signaling and cytokinin hormone homeostasis. These large-scale single-cell profiling of stem cells provide a resource for mining stem cell regulators, which show significant association with yield traits. Overall, our discoveries advance the understanding of shoot development and open avenues for manipulating diverse crops to enhance food and energy security.
... Finely controlling the expression levels of J2 and EJ2 by genetic engineering allows to generate tomato varieties with a better combination of beneficial traits [71,72]. This reveals the wide and complex In Arabidopsis, the floral meristem identity function is attributed to members of the AP1/SQUA MADS-box subfamily (AP1, CAL and FUL genes in Arabidopsis) [73,74] rather than to a specific subclass of SEP genes as described above for petunia and tomato. Interestingly, AP1, SEP and AGL6 genes all form a superclade with shared ancestry (Fig. 3). ...
Flower development is the process leading from a reproductive meristem to a mature flower with fully developed floral organs. This multi-step process is complex and involves thousands of genes in intertwined regulatory pathways; navigating through the FLOR-ID website will give an impression of this complexity and of the astonishing amount of work that has been carried on the topic (Bouché et al., Nucleic Acids Res 44:D1167-D1171, 2016). Our understanding of flower development mostly comes from the model species Arabidopsis thaliana, but numerous other studies outside of Brassicaceae have helped apprehend the conservation of these mechanisms in a large evolutionary context (Moyroud and Glover, Curr Biol 27:R941-R951, 2017; Smyth, New Phytol 220:70-86, 2018; Soltis et al., Ann Bot 100:155-163, 2007). Integrating additional species and families to the research on this topic can only advance our understanding of flower development and its evolution.In this chapter, we review the contribution that the Solanaceae family has made to the comprehension of flower development. While many of the general features of flower development (i.e., the key molecular players involved in flower meristem identity, inflorescence architecture or floral organ development) are similar to Arabidopsis, our main objective in this chapter is to highlight the points of divergence and emphasize specificities of the Solanaceae. We will not discuss the large topics of flowering time regulation, inflorescence architecture and fruit development, and we will restrict ourselves to the mechanisms included in a time window after the floral transition and before the fertilization. Moreover, this review will not be exhaustive of the large amount of work carried on the topic, and the choices that we made to describe in large details some stories from the literature are based on the soundness of the functional work performed, and surely as well on our own preferences and expertise.First, we will give a brief overview of the Solanaceae family and some of its specificities. Then, our focus will be on the molecular mechanisms controlling floral organ identity, for which extended functional work in petunia led to substantial revisions to the famous ABC model. Finally, after reviewing some studies on floral organ initiation and growth, we will discuss floral organ maturation, using the examples of the inflated calyx of the Chinese lantern Physalis and petunia petal pigmentation.
... QTL mapping and GWA studies also revealed the genetic architecture of broccoli head and cauliflower curd under heat and various temperatures (Matschegewski et al. 2015;Hasan et al. 2016;Branham et al. 2017;Lin et al. 2018). With forward and reverse genetic analyses, candidate genes for curding phenotypes had been suggested to be CAULIFLOWER (CAL) and APETALA1 (AP1), but these are not the only contributors to the phenotype (Kennard et al. 1994;Kempin et al. 1995;Lan and Paterson 2000;Purugganan et al. 2000;Smith and King 2000;Labate et al. 2006;Gao et al. 2007;Duclos and Björkman 2008;Sheng et al. 2019). QTL mapping of flowering time has been widely practiced in the species with candidate genes inferred from Arabidopsis thaliana (Bohuon et al. 1998;Rae et al. 1999;Lan and Paterson 2000;Axelsson et al. 2001;Lin et al. 2005Lin et al. , 2018Okazaki et al. 2007;Razi et al. 2008;Li et al. 2015;Irwin et al. 2016;Branham et al. 2017). ...
To improve resolution to small genomic regions and sensitivity to small-effect loci in the identification of genetic factors conferring the enlarged inflorescence and other traits of cauliflower while also expediting further genetic dissection, 104 near-isogenic introgression lines (NIILs) covering 78.56% of the cauliflower genome, were selected from an advanced backcross population using cauliflower [B. oleracea var. botrytis L., mutant for Orange gene (ORG)] as the donor parent and a rapid cycling line (TO1434) as recurrent parent. Subsets of the advanced backcross population and NIILs were planted in the field for eight seasons, finding 141 marker-trait associations for 15 leaf-, stem- and flower-traits. Exemplifying the usefulness of these lines, we delineated the previously-known flower color gene to a 4.5 MB interval on C3; a gene for small plant size to a 3.4 MB region on C8; and a gene for large plant size and flowering time to a 6.1 MB region on C9. This approach unmasked closely linked QTL alleles with opposing effects (on chr. 8), and revealed both alleles with expected phenotypic effects and effects opposite the parental phenotypes. Selected B. oleracea NIILs with short generation time add new value to widely used research and teaching materials.
... Flower meristem identity mutants: ap1, cal, lfy, and ufo AP1 is also involved earlier in defining the identity of the flower meristem itself. It does this partly in combination with a closely related MADS paralog CAULIFLOWER (CAL) (Bowman et al. 1993;Kempin et al. 1995) (Table 2). Double mutants of ap1 and cal Fig. 1. ...
In the later part of the 1980s, the time was ripe for identifying genes controlling flower development. In that pregenomic era, the easiest way to do this was to induce random mutations in seeds by chemical mutagens (or irradiation) and to screen thousands of plants for those with phenotypes specifically defective in floral morphogenesis. Here, we discuss the results of premolecular screens for flower development mutants in Arabidopsis thaliana, carried out at Caltech and Monash University, emphasizing the usefulness of saturation mutagenesis, multiple alleles to identify full loss-of-function, conclusions based on multiple mutant analyses, and from screens for enhancer and suppressor modifiers of original mutant phenotypes. One outcome was a series of mutants that led to the ABC floral organ identity model (AP1, AP2, AP3, PI, and AG). In addition, genes controlling flower meristem identity (AP1, CAL, and LFY), floral meristem size (CLV1 and CLV3), development of individual floral organ types (CRC, SPT, and PTL), and inflorescence meristem properties (TFL1, PIN1, and PID) were defined. These occurrences formed targets for cloning that eventually helped lead to an understanding of transcriptional control of the identity of floral organs and flower meristems, signaling within meristems, and the role of auxin in initiating floral organogenesis. These findings in Arabidopsis are now being applied to investigate how orthologous and paralogous genes act in other flowering plants, allowing us to wander in the fertile fields of evo-devo.
... The curd of cauliflower is composed of a spirally iterative pattern of primary inflorescence meristems with floral primordia arrested in their development [26,27]. The first insight in genetic control of the curd-like structure was achieved through characterization of the Arabidopsis ap1 and cal double mutant with a cauliflower curd phenotype [28]. Subsequently, several studies indicated that the genetic nature of the cauliflower curd appears more complex [29][30][31]. ...
Background: Brassica oleracea includes several morphologically diverse, economically important vegetable crops, such as the cauliflower and cabbage. However, genetic variants, especially large structural variants (SVs), that underlie the extreme morphological diversity of B. oleracea remain largely unexplored.
... Ectopic expression of LFY or AP1 converts the inflorescence shoot apical meristem to a flower; 35S:AP1 and 35S: LFY flower show a terminal flower phenotype just like that of tfl1 mutants (Weigel and Nilsson, 1995). Although AP1 and LFY are the major floral meristem identity genes, other genes along with CAULIFLOWER (Kempin et al., 1995), FRUITFULL (Ferrandiz et al., 2000) and AP2 (Jofuku et al., 1994) play secondary roles in specifying floral meristem identity. Both LFY and AP1 encode sequencespecific DNA binding transcription factors. ...
Flowers are arranged into articulated whorls of sepals, petals, stamens and carpels, each of which has a special reproductive function in each of these floral organ groups. Sepals enclose and cover the bud of the flower, while petals may be wide and showy to attract pollinators. Stamens produce male gametes containing pollen grains, while the carpels contain the ovules that will bear the seeds when fertilized. While the scale, form, number and development of each of these types of organs may be quite different, there is the same general arrangement of four types of floral organs organized in clustered whorls across all species of flowering plants. The identities of these exclusive organs are specified by the action of floral organ identity genes in discrete regions of developing flower. The main principle of flower development is the ABC model. Recent work has led identification of SEP genes which work redundantly to determine petals, stamens, and carpels as well as floral determination. The update of the ABC model resulted in the discovery of the value of the SEP genes. The failure of floral organs to grow with the correct identity in A, B, C and E class mutants suggests that the ABCE genes are necessary to specify the identity of floral organ.
... There are three APETALA genes denoted as AP1, AP2 and AP3 which were characterized in model plant A. thaliana and are essential in floral organogenesis as well as differentiation of floral tissues along with having countless functions in A-class of the APETALA gene family [7]. A common characteristic of regulation for the floral meristematic trait in the model plant Arabidopsis which contains AP1 gene and its homologs CAULIFLOWER (CAL) and FRUITFUL (FUL) [8,9]. In the perspective on floral regulatory genes, ABC model establishes to be very much moderated in different plant species, for example, tulip, petunia, wheat and rice [10][11][12][13]. ...
... Furthermore, within the AP1 subfamily of the MADS-box gene family, there are two AP1 paralogous genes, CAL (CAULIFLOWER) and FUL (FRUITFULL), and all three together form the SQUA-like (SQUAMOSA) gene [11,28]. CAL can positively regulate AP1 expression, but all its functions are redundant with those of AP1 [16,26,29]. In contrast, FUL has evolved with a function in valve identity specification [28]. ...
With its large inflorescences and colorful flowers, Hydrangea macrophylla has been one of the most popular ornamental plants in recent years. However, the formation mechanism of its major ornamental part, the decorative floret sepals, is still not clear. In this study, we compared the transcriptome data of H. macrophylla ‘Endless Summer’ from the nutritional stage (BS1) to the blooming stage (BS5) and annotated them into the Kyoto Encyclopedia of Genes and Genomes (KEGG) and Gene Ontology (GO) databases. The 347 identified differentially expressed genes (DEGs) associated with flower development were subjected to a trend analysis and a protein–protein interaction analysis. The combined analysis of the two yielded 60 DEGs, including four MADS-box transcription factors (HmSVP-1, HmSOC1, HmAP1-2, and HmAGL24-3) and genes with strong connectivity (HmLFY and HmUFO). In addition, 17 transcription factors related to the ABCDE model were screened, and key candidate genes related to the development of decorative floret sepals in H. macrophylla were identified by phylogenetic and expression pattern analysis, including HmAP1-1, HmAP1-2, HmAP1-3, HmAP2-3, HmAP2-4, and HmAP2-5. On this basis, a gene regulatory network model of decorative sepal development was also postulated. Our results provide a theoretical basis for the study of the formation mechanism of decorative floret sepals and suggest a new direction for the molecular breeding of H. macrophylla.
... Many genes associated with meristem identity conversion have been identified via studies using Arabidopsis as a model, including LEAFY (LFY), APETALA1 (AP1), and CAULIFLOWER (CAL). These genes enable the lateral meristem to acquire a floral identity and differentiate into flower organs (Mandel et al., 1992;Weigel et al., 1992;Kempin et al., 1995). In recent years, quite a few genes involved in the meristem identity conversion have also been identified in rice (Figure 3). ...
Rice inflorescence is one of the major organs in determining grain yield. The genetic and molecular regulation on rice inflorescence architecture has been well investigated over the past years. In the present review, we described genes regulating rice inflorescence architecture based on their roles in meristem activity maintenance, meristem identity conversion and branch elongation. We also introduced the emerging regulatory pathways of phytohormones involved in rice inflorescence development. These studies show the intricacies and challenges of manipulating inflorescence architecture for rice yield improvement.
... We do not know whether both pistils were at the same developmental stage and whether any of them had an additional involucre. Mutants of Arabidopsis with branched inflorescence-like flowers are well-characterized (Bowman et al., 1993;Kempin et al., 1995) but generally not regarded as evidence for inferring more complex homologies of conventional wild-type flowers of Brassicaceae. ...
Molecular phylogenetic analyses have revealed a superclade of mesangiosperms with five extant lineages: monocots, eudicots, magnoliids, Ceratophyllum and Chloranthaceae. Both Ceratophyllum and Chloranthaceae are ancient lineages with a long fossil record; their precise placement within mesangiosperms is uncertain. Morphological studies have suggested that they form a clade together with some Cretaceous fossils, including Canrightia, Montsechia and Pseudoasterophyllites. Apart from Canrightia, members of this clade share unilocular gynoecia commonly interpreted as monomerous with ascidiate carpels. Alternatively, the gynoecium of Ceratophyllum has also been interpreted as syncarpous with a single fertile carpel (pseudomonomerous). We investigate patterns of morphological, anatomical and developmental variation in gynoecia of three Ceratophyllum species to explore the controversial interpretation of its gynoecium as either monomerous or pseudomonomerous. We use an angiosperm-wide morphological data set and contrasting tree topologies to estimate the ancestral gynoecium type in both Ceratophyllum and mesangiosperms. Gynoecia of all three Ceratophyllum species possess a small (sometimes vestigial) glandular appendage on the abaxial side and an occasionally bifurcating apex. The ovary is usually unilocular with two procambium strands, but sometimes bilocular and/or with three strands in C. demersum. None of the possible phylogenetic placements strongly suggest apocarpy in the stem lineage of Ceratophyllum. Rescoring Ceratophyllum as having two united carpels affects broader-scale reconstructions of the ancestral gynoecium in mesangiosperms. Our interpretation of the glandular appendage as a tepal or staminode homologue makes the Ceratophyllum ovary inferior, thus resembling (semi)inferior ovaries of most Chloranthaceae and potentially related fossils Canrightia and Zlatkocarpus. The entire structure of the flower of Ceratophyllum suggests strong reduction following a long and complex evolutionary history. The widely accepted notion that apocarpy is ancestral in mesangiosperms (and angiosperms) lacks robust support, regardless of which modes of carpel fusion are considered. Our study highlights the crucial importance of incorporating fossils into large-scale analyses to understand character evolution.
... In agriculture, these genetic targets have been used to favour inflorescence modifications, especially inflorescence branching, to increase flower and grain production during crop domestication and improvement. A striking example are the flower heads of broccoli and cauliflower that carry a nonsense mutation in the MADSbox gene BoCAL, which arose during domestication (Kempin et al., 1995;Purugganan et al., 2000). Additionally, increased inflorescence branching substantially contributes to an increase in yield for cereal crops, including barley (Ramsay et al., 2011), maize (Eveland et al., 2014), rice (Huang et al., 2009), andwheat (Boden et al., 2015). ...
... Antagonistic interaction between the IM identity genes, TERMINAL FLOWER 1 (TFL1) and AGAMOUS-LIKE 24 (AGL24), and the FM identity genes, LEAFY (LFY), APETALA 1 (AP1), and CAULIFLOWER (CAL), maintains the identity of both types of SAMs (Bradley et al., 1997;Liljegren et al., 1999;Ratcliffe et al., 1999). AP1 and CAL encode MADS domain TFs that have partially redundant activities involved in the formation of FMs by repression of TFL1 (Ratcliffe et al., 1999;Kempin et al., 1995). In turn, TFL1 bars AP1 and LFY expression in IMs (Liljegren et al., 1999;Ratcliffe et al., 1999). ...
Polycomb group (PcG) protein-mediated histone methylation (H3K27me3) controls the correct spatiotemporal expression of numerous developmental regulators in Arabidopsis. Epigenetic silencing of the stem cell factor WUS in floral meristems (FMs) depends on H3K27me3 deposition by PcG proteins. However, the role of H3K27me3 in silencing of other meristematic regulator and pluripotency genes during FM determinacy has not yet been studied. To this end, we report the genome-wide dynamics of H3K27me3 levels during FM arrest and the consequences of strongly depleted PcG activity on early flower morphogenesis including enlarged and indeterminate FMs. Strong depletion of H3K27me3 levels results in misexpression of the FM identity gene AGL24, which partially leads to floral reversion causing ap1-like flowers and indeterminate FMs expressing ectopically WUS and STM. Loss of STM can rescue supernumerary floral organs and FM indeterminacy in H3K27me3-deficient flowers indicating that the hyperactivity of the FMs is at least partially a result of ectopic STM expression. Nonetheless, WUS remained essential for the FM activity. Our results demonstrate that PcG proteins promote FM determinacy at multi-levels of the floral gene regulatory network, silencing initially floral regulators like AGL24 that promotes FM indeterminacy, and subsequently, meristematic pluripotency genes such as WUS and STM during FM arrest.
... In cauliflower, curd consists of a dense mass of arrested inflorescence meristem, only ~10% of which develop into floral primordia and normal flowers. The cauliflower curd phenotype in mutants of Arabidopsis thaliana is due to a class of flower developmental regulatory genes viz., APETALA 1 (AP1, Mandel et al. 1992) and CAULIFLOWER (CAL; Kempin et al. 1995) that specify the floral meristem identity (as opposed to the inflorescence meristem) developing reproductive primordia. Arabidopsis mutants (AP1 and CAL) are arrested in inflorescence development at the meristem stage and develop into a dense mass similar to cauliflower curd. ...
Among the cole vegetables, cauliflower is a widely grown crop worldwide for its nutrients and flavor. It is a thermosensitive crop for its curd formation and development. Different cultivar groups in cauliflower are known such as Italian or Original, Cornish, Northerns, Roscoff, Angers, Erfurt, Snowball and Indian, based on phylogeny and plant traits. The Indian cauliflower group evolved from European cauliflower and later classified as early, mid-early, mid-late and late, depending upon temperature requirements related to curd initiation and development. A large number of varieties and hybrids have been developed in tropical cauliflower, for different maturity groups and established using a cytoplasmic male sterility (CMS) system for hybrid breeding. Recently, biotechnological tools such as DNA markers, genomics and tissue culture for doubled haploid development, pre-breeding for introgressing genes/QTLs from alien brassicas were deployed in cauliflower breeding. Resistant sources identified in cole vegetables for black rot and downy mildew by genetic investigations revealed single dominant gene governance of resistance for both diseases. Cauliflower is one of the best candidate crops for β-carotene biofortification, hence a natural mutant native Or gene was introgressed into Indian cauliflower. Besides, transgenesis is underway to develop diamondback moth resistant varieties by stacking cry 1b and 1c bt genes in cauliflower. This chapter highlights recent developments in cauliflower breeding particularly in tropical types.
... A previous study found that the phenotype of ap1-1/cal-1 mutant of Arabidopsis has similarity with broccoli and cauliflower, leading to speculation that APETALA 1 (AP1) and CAULIFLOWER (CAL, the paralog of AP1) might be responsible for inflorescence architecture in B. oleracea (Smith and King 2000). Surprisingly, the molecular and population genetic studies suggested that the function of CAL in B. oleracea (BoCAL) is compromised both in broccoli and cauliflower (Kempin et al. 1995;Lowman and Purugganan 1999;Purugganan et al. 2000;Smith and King 2000). Although AP1like genes are also associated with the phenotype of inflorescence architecture in B. oleracea, while the situation for AP1-like genes is less clear due to several copies of AP1-like genes in B. oleracea (Lowman andPurugganan 1999, Labate et al. 2006;Duclos and Björkman 2008;Schilling et al. 2018). ...
The genus Brassica contains the most economically valuable cultivated dicotyledonous plants in the world. They provide edible oil, protein, and vegetables for human consumption, as well as fodder for livestock. Extensive researches have been performed with the aim of unraveling the complex genomes of the Brassica species. Of the six Brassica species within the “triangle of U,” the genomes of all six Brassica species have been sequenced and assembled. The analyses of these genomes have revealed the genetic variation, genomic structure, biogeographical origin, and population evolution of the Brassica species, and when combined with large-population resequencing, these data were used to propose the history and genetic effects of domestication and adaptive mechanism of the Brassica species. Advances in resequencing technology have enabled the application of high-efficiency breeding strategies in these crop species, involving the identification of genetic variation and genetic loci underlying a trait, genome-wide association studies, and genomic selection. Moreover, population genomics approaches, including population transcriptomics, population epigenomics, and genomic selection studies, have contributed to enhancing our understanding of acclimation, adaptation and disease and insect resistance for populations in the Brassica species. Population genomics therefore provides new insights and facilitates the deciphering of the secrets of the evolution, domestication, and adaptation of Brassica species.
... It is noteworthy, that some of these mutants show abnormal gynoecia, such as ett which shows defects along the apical-basal axis, and hbb shows defects in transmitting tract development late in gynoecium development [54,56]. However, for nga2 and cal single mutants, no phenotypes in the gynoecium were reported previously [58,62]. Our findings together with published data indicate that at least some of these transcription factors activate expression of CRC in the gynoecium and nectaries, even though one cannot rule out that the downregulation may, to some extent, be due to gynoecium tissues being absent due to mutations present in these plants. ...
Angiosperm flowers are the most complex organs that plants generate, and in their center, the gynoecium forms, assuring sexual reproduction. Gynoecium development requires tight regulation of developmental regulators across time and tissues. How simple on and off regulation of gene expression is achieved in plants was described previously, but molecular mechanisms generating complex expression patterns remain unclear. We use the gynoecium developmental regulator CRABS CLAW (CRC) to study factors contributing to its sophisticated expression pattern. We combine in silico promoter analyses, global TF-DNA interaction screens, and mutant analyses. We find that miRNA action, DNA methylation, and chromatin remodeling do not contribute substantially to CRC regulation. However, 119 TFs, including SEP3, ETT, CAL, FUL, NGA2, and JAG bind to the CRC promoter in yeast. These TFs finetune transcript abundance as homodimers by transcriptional activation. Interestingly, temporal–spatial aspects of expression regulation may be under the control of redundantly acting genes and require higher order complex formation at TF binding sites. Our work shows that endogenous regulation of complex expression pattern requires orchestrated transcription factor action on several conserved promotor sites covering almost 4 kb in length. Our results highlight the utility of comprehensive regulators screens directly linking transcriptional regulators with their targets.
... The CAL is closely related to APETALA1 (AP1), and regulates the floral meristems formation [61]. Like CAL, LEAFY (LFY) is a floral meristem identity gene, participating in the transition from the vegetative to the reproductive [62]. ...
The flower buds continue to develop during the whole winter in tree fruit species, which is affected by environmental factors and hormones. However, little is known about the molecular mechanism of flower development during dormancy phase of sweet cherry in response to light, temperature and ABA. Therefore, we identified two cold induced gene (CIG) PavCIG1 and PavCIG2 from sweet cherry, which were closely to PpCBF and PyDREB from Prunus persica and Prunus yedoensis by using phylogenetic analysis, suggesting conserved functions with these evolutionarily closer DREB subfamily genes. Subcellular localization analysis indicated that, PavCIG1 and PavCIG2 were both localized in the nucleus. The seasonal expression levels of PavCIG1 and PavCIG2 were higher at the stage of endodormancy in winter, and induced by low temperature. Ectopic expression of PavCIG1 and PavCIG2 resulted in a delayed flowering in Arabidopsis. Furthermore, PavCIG2 increased light-responsive gene PavHY5 transcriptional activity by binding to its promoter, meanwhile, PavHY5-mediated positive feedback regulated PavCIG2. Moreover, ABA-responsive protein PavABI5-like could also increase transcriptional activity of PavCIG and PavCIG2. In addition, PavCIG and PavCIG2 target gene PavCAL-like was involved in floral initiation, demonstrated by ectopic expression in Arabidopsis. These findings provide evidences to better understand the molecular mechanism of CIG-mediated flower development and dormancy in fruit species, including sweet cherry.
... In Arabidopsis, indeterminacy in the IM is maintained by the antagonistic relationship between TERMINAL FLOWER 1 (TFL1) and floral identity genes, LEAFY (LFY), APETALA1 (AP1), and CAULIFLOWER (CAL; Piñeiro and Coupland, 1998;Liljegren et al., 1999;Serrano-Mislata et al., 2017). AP1 and CAL belong to the euAP1 subclade of the AP1/FUL (FRUITFUL)-like MADS box gene family and are key players in controlling flowering time and AM determinacy (Kempin et al., 1995;Alvarez-Buylla et al., 2006). TFL1, which encodes a phosphatidylethanolamine-binding protein, is expressed in the central region of the IM and prevents it from acquiring FM identity by suppressing floral identity genes (Weigel et al., 1992;Bradley et al., 1997;Benlloch et al., 2007). ...
Inflorescence architecture in cereal crops directly impacts yield potential through regulation of seed number and harvesting ability. Extensive architectural diversity found in inflorescences of grass species is due to spatial and temporal activity and determinacy of meristems, which control the number and arrangement of branches and flowers, and underlie plasticity. Timing of the floral transition is also intimately associated with inflorescence development and architecture, yet little is known about the intersecting pathways and how they are rewired during development. Here, we show that a single mutation in a gene encoding an AP1/FUL-like MADS-box transcription factor significantly delays flowering time and disrupts multiple levels of meristem determinacy in panicles of the C4 model panicoid grass, Setaria viridis. Previous reports of AP1/FUL-like genes in cereals have revealed extensive functional redundancy, and in panicoid grasses, no associated inflorescence phenotypes have been described. In S. viridis, perturbation of SvFul2, both through chemical mutagenesis and CRISPR/Cas9-based gene editing, converted a normally determinate inflorescence habit to an indeterminate one, and also repressed determinacy in axillary branch and floral meristems. Our analysis of gene networks connected to disruption of SvFul2 identified regulatory hubs at the intersect of floral transition and inflorescence determinacy, providing insights into the optimization of cereal crop architecture.
... The curd of cauliflower is composed of a spirally iterative pattern of primary inflorescence meristems with floral primordia arrested in their development [26,27]. The first insight in genetic control of the curd-like structure was achieved through characterization of the Arabidopsis ap1 and cal double mutant with a cauliflower curd phenotype [28]. Subsequently, several studies indicated that the genetic nature of the cauliflower curd appears more complex [29][30][31]. ...
Background
Brassica oleracea includes several morphologically diverse, economically important vegetable crops, such as the cauliflower and cabbage. However, genetic variants, especially large structural variants (SVs), that underlie the extreme morphological diversity of B. oleracea remain largely unexplored.
Results
Here we present high-quality chromosome-scale genome assemblies for two B. oleracea morphotypes, cauliflower and cabbage. Direct comparison of these two assemblies identifies ~ 120 K high-confidence SVs. Population analysis of 271 B. oleracea accessions using these SVs clearly separates different morphotypes, suggesting the association of SVs with B. oleracea intraspecific divergence. Genes affected by SVs selected between cauliflower and cabbage are enriched with functions related to response to stress and stimulus and meristem and flower development. Furthermore, genes affected by selected SVs and involved in the switch from vegetative to generative growth that defines curd initiation, inflorescence meristem proliferation for curd formation, maintenance and enlargement, are identified, providing insights into the regulatory network of curd development.
Conclusions
This study reveals the important roles of SVs in diversification of different morphotypes of B. oleracea, and the newly assembled genomes and the SVs provide rich resources for future research and breeding.
... A later study took a broader view of genetic redundancy, with the degree of redundancy ranging from "complete redundancy" among genes with housekeeping functions to "partial overlap of function" among genes with primarily regulatory functions (Pickett and Meeks-Wagner 1995). In studies from a number of model organisms, multiple examples of what is considered genetic redundancy have been given, including: genes derived from convergent evolution encoding enzymes that perform the same function (Pickett and Meeks-Wagner 1995); biochemical pathways that are redundant due to interconnected metabolic networks (Weintraub 1993); and genes from the same family (paralogs) that maintain some of the same functionality (Kempin et al. 1995). Discussions of genetic redundancy in recent literature mostly encompass this last definition, where a duplication event results in multiple copies of a gene that retain overlapping functions (e.g., Chen et al. 2010, Bolle et al. 2013, Rutter et al. 2017. ...
Genetic redundancy refers to a situation where an individual with a loss-of-function mutation in one gene (single mutant) does not show an apparent phenotype until one or more paralogs are also knocked out (double/higher-order mutant). Previous studies have identified some characteristics common among redundant gene pairs, but a predictive model of genetic redundancy incorporating a wide variety of features derived from accumulating omics and mutant phenotype data is yet to be established. In addition, the relative importance of these features for genetic redundancy remains largely unclear. Here, we establish machine learning models for predicting whether a gene pair is likely redundant or not in the model plant Arabidopsis thaliana based on six feature categories: functional annotations, evolutionary conservation including duplication patterns and mechanisms, epigenetic marks, protein properties including post-translational modifications, gene expression, and gene network properties. The definition of redundancy, data transformations, feature subsets, and machine learning algorithms used significantly affected model performance based on hold-out, testing phenotype data. Among the most important features in predicting gene pairs as redundant were having a paralog(s) from recent duplication events, annotation as a transcription factor, downregulation during stress conditions, and having similar expression patterns under stress conditions. We also explored the potential reasons underlying mispredictions and limitations of our studies. This genetic redundancy model sheds light on characteristics that may contribute to long-term maintenance of paralogs, and will ultimately allow for more targeted generation of functionally informative double mutants, advancing functional genomic studies.
... Besides AP1 and FUL, other MADS-box genes are also part of the network that promotes the floral meristem identity, including CAULI-FLOWER (CAL) (an AP1 paralog with partially redundant functions to those of AP1, only present in Brassicaceae), AGAMOUS-LIKE24 (AGL24), SHORT VEGETATIVE PHASE (SVP) and SUPPRESSOR OF CONSTANS1 (SOC1) as previous mentioned (Aukerman et al., 1999;Gregis et al., 2008;Kempin et al., 1995;Langmore et al., 2009;Lawton-Rauh et al., 1999;Lowman, 1999;Melzer et al., 2008;Zhao et al., 2017). ...
Plants evolved different strategies to better adapt to the environmental conditions in which they live: the control of their body architecture and the timing of phase change are two important processes that can improve their fitness. As they age, plants undergo two major phase changes (juvenile to adult and adult to reproductive) that are a response to environmental and endogenous signals. These phase transitions are accompanied by alterations in plant morphology and also by changes in physiology and the behavior of gene regulatory networks. Six main pathways involving environmental and endogenous cues that crosstalk with each other have been described as responsible for the control of plant phase transitions: the photoperiod pathway, the autonomous pathway, the vernalization pathway, the temperature pathway, the GA pathway, and the age pathway. However, studies have revealed that sugar is also involved in phase change and the control of branching behavior. In this review, we discuss recent advances in plant biology concerning the genetic and molecular mechanisms that allow plants to regulate phase transitions in response to the environment. We also propose connections between phase transition and plant architecture control.
... Two closely related MADS-box TFs, APETALA 1 (AP1) andCAULIFLOWER are found to be enriched in the epidermal cell layer in the cell type microarray study. Past studies have shown that these TFs are expressed in emerging flower primordia(Alejandra Mandel et al., 1992;Kempin et al., 1995; Ye et al., ). Confocal imaging ofpAP1::H2B-YFP revealed its expression restricted to flower meristem. ...
Transcriptional control of gene expression is an exquisitely regulated process in both animals and plants. Transcription factors (TFs) and the regulatory networks that drive the expression of TF genes in epidermal and subepidermal cell layers in Arabidopsis are unexplored. Here, we identified 65 TF genes enriched in the epidermal and subepidermal cell layers of the shoot apical meristem (SAM). To determine the cell type specificity in different stages of Arabidopsis development, we made YFP based transcriptional fusion constructs by taking a 3‐kb upstream noncoding region above the translation start site. Here, we report that for ~52% (22/42) TF genes, we detected transcription activity. TF genes derived from epidermis show uniform expression in early embryo development; however, in the late globular stage, their transcription activity is suppressed in the inner cell layers. Expression patterns linked to subepidermal cell layer identity were apparent in the postembryonic development. Potential upstream regulators that could modulate the activity of epidermal and subepidermal cell layer‐enriched TF genes were identified using enhanced yeast‐one‐hybrid (eY1H) assay and validated. This study describes the activation of TF genes in epidermal and subepidermal cell layers in embryonic and postembryonic development of Arabidopsis shoot apex.
... The genetic basis underlying the phenotypic diversity present in Cole crops has been addressed for only some morphotypes. For example, the cauliflower phenotype of Arabidopsis is comparable to inflorescence development in the cauliflower B. oleracea morphotype, and it has been shown that the gene CAULIFLOWER is responsible for the phenotype observed in both species (Kempin et al., 1995;Carr and Irish, 1997;Purugganan et al., 2000;Smith and King, 2000). However, quantitative trait locus (QTL) mapping for the curd of cauliflower indicates that 86 QTLs are controlling eight curdrelated traits, demonstrating this phenotype is under complex genetic control (Lan and Paterson, 2000). ...
Morphotypes of Brassica oleracea are the result of a dynamic interaction between genes that regulate the transition between vegetative and reproductive stages and those that regulate leaf morphology and plant architecture. In kales, ornate leaves, extended vegetative phase, and nutritional quality are some of the characters potentially selected by humans during domestication. We used a combination of developmental studies and transcriptomics to understand the vegetative domestication syndrome of kale. To identify candidate genes that are responsible for the evolution of domestic kale, we searched for transcriptome-wide differences among three vegetative B. oleracea morphotypes. RNA-seq experiments were used to understand the global pattern of expressed genes during a mixture of stages at one time in kale, cabbage, and the rapid cycling kale line TO1000. We identified gene expression patterns that differ among morphotypes and estimate the contribution of morphotype-specific gene expression that sets kale apart (3958 differentially expressed genes). Differentially expressed genes that regulate the vegetative to reproductive transition were abundant in all morphotypes. Genes involved in leaf morphology, plant architecture, defense, and nutrition were differentially expressed in kale. This allowed us to identify a set of candidate genes we suggest may be important in the kale domestication syndrome. Understanding candidate genes responsible for kale domestication is of importance to ultimately improve Cole crop production.
... The classic example is the genetic interaction between AP1 and CAL: ap1 mutants display a floral homeotic phenotype whereas cal mutants resemble the WT. However, ap1cal double mutants have an enhanced ap1 phenotype (Kempin et al., 1995). Other examples include the genetic interaction between HY5 and its homolog HYH (Holm et al., 2002), between ARF4 and its homolog ARF7 (Okushima et al., 2005) and between BRI1 and BRL1 (Cano-Delgado et al., 2004). ...
The C2H2-type zinc finger transcription factor STOP1 is crucial for aluminum (Al) resistance in Arabidopsis. The F-box protein Regulation of AtALMT1 Expression 1 (RAE1) was recently reported to regulate the stability of STOP1. There is a unique homolog of RAE1, RAH1 (RAE1 homolog 1), in Arabidopsis, but the biological function of RAH1 is still known. In this study, we characterized the role of RAH1 and/or RAE1 in the regulation of Al resistance and plant growth. We demonstrate that RAH1 can directly interact with STOP1 and promote its ubiquitination and degradation. RAH1 is preferentially expressed in root caps and vascular tissues of various tissues, and its expression is induced by Al and controlled by STOP1. Mutation of RAH1 in rae1 but not wild-type (WT) background increases STOP1 protein level, leading to increased expression of STOP1-regulated genes and enhanced Al resistance. Interestingly, rah1rae1 double mutant shows reduced plant growth compared to WT and single mutants under normal conditions, and introduction of stop1 mutation into the double mutant background can rescue its reduced plant growth phenotype. Our results thus reveal that RAH1 plays an unequally redundant role with RAE1 in the modulation of STOP1 stability and plant growth, and dynamic regulation of the STOP1 level is critical for the balance of Al resistance and normal plant growth.
... The first insight in genetic control of the curd-like structure was achieved through characterization of the Arabidopsis ap1 and cal double mutant with a cauliflower curd phenotype (Kempin et al., 1995). Subsequently, several studies indicated that the genetic nature of the cauliflower curd appears more complex (Smith and King, 2000;Labate et al., 2006;Duclos and Björkman, 2008). ...
Brassica oleracea includes several morphologically diverse, economically important vegetable crops. Here we present high-quality chromosome-scale genome assemblies for two B. oleracea morphotypes, cauliflower and cabbage. Direct comparison of these two assemblies identifies ~120 K high-confidence structural variants (SVs). Population analysis of 271 B. oleracea accessions using these SVs clearly separates different morphotypes, suggesting the association of SVs with B. oleracea intraspecific divergence. Genes affected by SVs selected between cauliflower and cabbage are enriched with functions related to response to stress and stimulus and meristem and flower development. Furthermore, genes affected by selected SVs and involved in the switch from vegetative to generative growth that defines curd initiation, inflorescence meristem proliferation for curd formation, maintenance and enlargement, are identified, providing insights into the regulatory network of curd development. This study reveals the important roles of SVs in diversification of different morphotypes of B. oleracea , and the newly assembled genomes and the SVs provide rich resources for future research and breeding.
The cultivated diploid Brassica oleracea is an important vegetable crop, but the genetic basis of domestication remains largely unclear without high-quality reference genomes of wild B. oleracea. Here, we report the first chromosome-level assembly of the wild Brassica oleracea L. W03 genome, (total genome size, 630.7 Mb; scaffold N50, 64.6 Mb). Using newly assembled W03 genome, we constructed a gene-based B. oleracea pangenome and identified 29,744 core genes, 23,306 dispensable genes, and 1,896 private genes. We resequenced 53 accessions, which represent six potential wild B. oleracea progenitor species. The results of the population genomic analysis showed that wild B. oleracea population had the highest level of diversity and represented the more closely related population of horticultural B. oleracea. Additionally, the WUSCHEL gene was found to play a decisive role in domestication and to be involved in cauliflower and broccoli curd formation. We also illustrate the loss of disease resistance genes during domestication selection. Our results provide deep insights into B. oleracea domestication and will facilitate Brassica crop genetic improvement.
The formulation of the ABC model by a handful of pioneer plant developmental geneticists was a seminal event in the quest to answer a seemingly simple question: how are flowers formed? Fast forward 30 years and this elegant model has generated a vibrant and diverse community, capturing the imagination of developmental and evolutionary biologists, structuralists, biochemists and molecular biologists alike. Together they have managed to solve many floral mysteries, uncovering the regulatory processes that generate the characteristic spatio-temporal expression patterns of floral homeotic genes, elucidating some of the mechanisms allowing ABC genes to specify distinct organ identities, revealing how evolution tinkers with the ABC to generate morphological diversity and even shining a light on the origins of the floral gene regulatory network itself. Here we retrace the history of the ABC model, from its genesis to its current form, highlighting specific milestones along the way before drawing attention to some of the unsolved riddles still hidden in the floral alphabet.
Background
Traditional spring-summer sown oat is a typical long-day crop that cannot head under short-day conditions. The creation of photoperiod-insensitive oats overcomes this limitation. MADS-box genes are a class of transcription factors involved in plant flowering signal transduction regulation. Previous transcriptome studies have shown that MADS-box genes may be related to the oat photoperiod.
Methods
Putative MADS-box genes were identified in the whole genome of oat. Bioinformatics methods were used to analyze their classification, conserved motifs, gene structure, evolution, chromosome localization, collinearity and cis -elements. Ten representative genes were further screened via qRT‒PCR analysis under short days.
Results
In total, sixteen AsMADS genes were identified and grouped into nine subfamilies. The domains, conserved motifs and gene structures of all AsMADS genes were conserved. All members contained light-responsive elements. Using the photoperiod-insensitive oat MENGSIYAN4HAO (MSY4) and spring-summer sown oat HongQi2hao (HQ2) as materials, qRT‒PCR analysis was used to analyze the AsMADS gene at different panicle differentiation stages under short-day conditions. Compared with HQ2, AsMADS3 , AsMADS8 , AsMADS11 , AsMADS13 , and AsMADS16 were upregulated from the initial stage to the branch differentiation stage in MSY4, while AsMADS12 was downregulated. qRT‒PCR analysis was also performed on the whole panicle differentiation stages in MSY4 under short-day conditions, the result showed that the expression levels of AsMADS9 and AsMADS11 gradually decreased. Based on the subfamily to which these genes belong, the above results indicated that AsMADS genes, especially SVP, SQUA and Mα subfamily members, regulated panicle development in MSY4 by responding to short-days. This work provides a foundation for revealing the function of the AsMADS gene family in the oat photoperiod pathway.
TEMPRANILLO1 ( TEM1 ) is a transcription factor belonging to related to ABI3 and VP1 family, which is also known as ethylene response DNA‐binding factor 1 and functions as a repressor of flowering in Arabidopsis . Here, a putative homolog of AtTEM1 was isolated and characterized from chrysanthemum, designated as CmTEM1 . Exogenous application of ethephon leads to an upregulation in the expression of CmTEM1 . Knockdown of CmTEM1 promotes floral initiation, while overexpression of CmTEM1 retards floral transition. Further phenotypic observations suggested that CmTEM1 involves in the ethylene‐mediated inhibition of flowering. Transcriptomic analysis established that expression of the flowering integrator CmAFL1 , a member of the APETALA1/FRUITFULL subfamily, was downregulated significantly in CmTEM1 ‐overexpressing transgenic plants compared with wild‐type plants but was verified to be upregulated in amiR‐ CmTEM1 lines by quantitative RT‐PCR. In addition, CmTEM1 is capable of binding to the promoter of the CmAFL1 gene to inhibit its transcription. Moreover, the genetic evidence supported the notion that CmTEM1 partially inhibits floral transition by targeting CmAFL1 . In conclusion, these findings demonstrate that CmTEM1 acts as a regulator of ethylene‐mediated delayed flowering in chrysanthemum, partly through its interaction with CmAFL1 .
Flower busd formation is an important plant growth process. It has been reported that dwarfing rootstocks can significantly affect the flower bud formation of scions. In this study, we found the dwarfing rootstock 'Yunnan' quince could significantly increase the flowering rate of 'Abbé Fetel' pear scions. The RNA-sequencing data revealed significant changes in the expression of genes related to hormone pathways. Furthermore, hormone analyses indicated that 'Yunnan' quince significantly decreased the GA3 content and increased the cytokinin/auxin ratio in 'Abbé Fetel' pear apical buds. The hormone contents were consistent with the RNA-sequencing data. Moreover, we found the flower development-related genes PbAGL9 and PbCAL-A1 were significantly upregulated and PbTFL1 was significantly downregulated in 'Abbé Fetel'/'Yunnan' quince apical buds. To further clarify the relationship between hormones and flowering-related genes, a hormone response assay was carried out. We found the expression levels of PbCAl-A1, PbTFL1 and PbAGL9 were regulated by hormones including GA3, CPPU and NAA. Y1H and dual-luciferase assays indicated that PbAGL9 significantly decreased the promoter activity of PbTFL1. In summary, 'Yunnan' quince upregulated PbCAL-A1 and PbAGL9, and downregulated PbTFL1 expression by decreasing the GA3 content and increasing the cytokinin/auxin ratio in 'Abbé Fetel' pear apical buds. Additionally, 'Yunnan' quince down-regulate PbTFL1 by upregulating the expression of PbAGL9, and eventually promoted floral induction in 'Abbé Fetel' pear.
Sorbitol is an important signaling molecule in fruit trees. Here, we observed that sorbitol increased during flower bud differentiation (FBD) in loquat (Eriobotrya japonica Lindl.). Transcriptomic analysis suggested that bud formation was associated with the expression of the MADS‐box transcription factor (TF) family gene, EjCAL. RNA fluorescence in situ hybridization showed that EjCAL was enriched in flower primordia but hardly detected in the shoot apical meristem. Heterologous expression of EjCAL in Nicotiana benthamiana plants resulted in early FBD. Yeast‐one‐hybrid analysis identified the ERF12 TF as a binding partner of the EjCAL promoter. Chromatin immunoprecipitation‐PCR confirmed that EjERF12 binds to the EjCAL promoter, and β‐glucuronidase activity assays indicated that EjERF12 regulates EjCAL expression. Spraying loquat trees with sorbitol promoted flower bud formation and was associated with increased expression of EjERF12 and EjCAL. Furthermore, we identified EjUF3GaT1 as a target gene of EjCAL and its expression was activated by EjCAL. Function characterization via overexpression and RNAi reveals that EjUF3GaT1 is a biosynthetic gene of flavonoid hyperoside. The concentration of the flavonoid hyperoside mirrored that of sorbitol during FBD and exogenous hyperoside treatment also promoted loquat bud formation. We identified a mechanism whereby EjCAL might regulate hyperoside biosynthesis and confirmed the involvement of EjCAL in flower bud formation in planta. Together, these results provide insight into bud formation in loquat and may be used in efforts to increase yield.
Transcription factors (TFs) are key nodes of gene regulatory networks that specify plant morphogenesis and control specific pathways such as stress responses. TFs directly interact the genome by recognizing specific DNA sequence, in terms of a complex system to fine-tune spatiotemporal gene expression. The combinatorial interaction among TFs determines regulatory specificity and defines the set of target genes to orchestrate their expression during developmental switches. In this chapter, we provide a catalog of plant-specific TFs and a comprehensive assessment of whether genome-wide analyses have so far been used for identifying potential direct target genes for each TFs. We further construct comprehensive TF-associated regulatory networks in the model plant Arabidopsis thaliana using genome-wide datasets from our ChIP-Hub database (http://www.chiphub.org/). We discuss how to dissect the network structure to identify potentially important cross-regulatory loops in the control of developmental switches in plants.
Vegetal fractals
Cauliflower, along with dahlias and daisies, develop as phyllotactic spirals. Azpeitia et al . combined modeling with experimental investigation to clarify the gene-regulatory network that sets up a multitude of undeveloped flowers to form a cauliflower curd. Irrepressible inflorescence identity genes in the context of dysfunctional meristems and slow internode elongation results in piles of incomplete flowers. If meristem size drifts during organogenesis, then the conical structures of the Romanesco form emerge in fractal formation. —PJH
Phylogenetic analyses of angiosperm MADS-box genes suggest that this gene family has undergone multiple duplication events followed by sequence divergence. To determine when such events have taken place and to understand the relationships of particular MADS-box gene lineages, we have identified APETALA1/FRUITFULL-like MADS-box genes from a variety of angiosperm species. Our phylogenetic analyses show two gene clades within the core eudicots, euAP1 (including Arabidopsis APETALA1 and Antirrhinum SQUAMOSA) and euFUL (including Arabidopsis FRUITFULL). Non-core eudicot species have only sequences similar to euFUL genes (FUL-like). The predicted protein products of euFUL and FUL-like genes share a conserved C-terminal motif. In contrast, predicted products of members of the euAP1 gene clade contain a different C terminus that includes an acidic transcription activation domain and a farnesylation signal. Sequence analyses indicate that the euAP1 amino acid motifs may have arisen via a translational frameshift from the euFUL/FUL-like motif. The euAP1 gene clade includes key regulators of floral development that have been implicated in the specification of perianth identity. However, the presence of euAP1 genes only in core eudicots suggests that there may have been changes in mechanisms of floral development that are correlated with the fixation of floral structure seen in this clade.
The enlarged inflorescence (curd) of cauliflower and broccoli provide not only a popular vegetable for human consumption, but also a unique opportunity for scientists who seek to understand the genetic basis of plant growth and development. By the comparison of quantitative trait loci (QTL) maps constructed from three different F2 populations, we identified a total of 86 QTL that control eight curd-related traits in Brassica oleracea. The 86 QTL may reflect allelic variation in as few as 67 different genetic loci and 54 ancestral genes. Although the locations of QTL affecting a trait occasionally corresponded between different populations or between different homeologous Brassica chromosomes, our data supported other molecular and morphological data in suggesting that the Brassica genus is rapidly evolving. Comparative data enabled us to identify a number of candidate genes from Arabidopsis that warrant further investigation to determine if some of them might account for Brassica QTL. The Arabidopsis/Brassica system is an important example of both the challenges and opportunities associated with extrapolation of genomic information from facile models to large-genome taxa including major crops.
Morphotypes of Brassica oleracea are the result of a dynamic interaction between genes that regulate the transition between vegetative and reproductive stages and those that regulate leaf morphology and plant architecture. In kales ornate leaves, delayed flowering, and nutritional quality are some of the characters potentially selected by humans during domestication.
We used a combination of developmental studies and transcriptomics to understand the vegetative domestication syndrome of kale. To identify candidate genes that are responsible for the evolution of domestic kale we searched for transcriptome-wide differences among three vegetative B. oleracea morphotypes. RNAseq experiments were used to understand the global pattern of expressed genes during one single phase of development in kale, cabbage and the rapid cycling kale line TO1000.
We identified gene expression patterns that differ among morphotypes, and estimate the contribution of morphotype-specific gene expression that sets kale apart (3958 differentially expressed genes). Differentially expressed genes that regulate the vegetative to reproductive transition were abundant in all morphotypes. Genes involved in leaf morphology, plan architecture, defense and nutrition were differentially expressed in kale.
RNA-Seq experiments allow the discovery of novel candidate genes involved in the kale domestication syndrome. We identified candidate genes differentially expressed in kale that could be responsible for variation in flowering times, taste and herbivore defense, variation in leaf morphology, plant architecture, and nutritional value. Understanding candidate genes responsible for kale domestication is of importance to ultimately improve Cole crop production.
The sections in this article are
Introduction
Floral Induction and Flowering Time
Floral Induction and Flower Initiation
Floral Patterning
Perspectives
Acknowledgments
Mutations in the APETALA1 gene disturb two phases of flower development, flower meristem specification and floral organ specification. These effects become manifest as a partial conversion of flowers into inflorescence shoots and a disruption of sepal and petal development. We describe the changes in an allelic series of nine apetala1 mutants and show that the two functions of APETALA1 are separable. We have also studied the interaction between APETALA1 and other floral genes by examining the phenotypes of multiply mutant plants and by in situ hybridization using probes for several floral control genes. The results suggest that the products of APETALA1 and another gene, LEAFY, are required to ensure that primordia arising on the flanks of the inflorescence apex adopt a floral fate, as opposed to becoming an inflorescence shoot. APETALA1 and LEAFY have distinct as well as overlapping functions and they appear to reinforce each other's action. CAULIFLOWER is a newly discovered gene which positively regulates both APETALA1 and LEAFY expression. All functions of CAULIFLOWER are redundant with those of APETALA1. APETALA2 also has an early function in reinforcing the action of APETALA1 and LEAFY, especially if the activity of either is compromised by mutation. After the identity of a flower primordium is specified, APETALA1 interacts with APETALA2 in controlling the development of the outer two whorls of floral organs.
The first step in flower development is the generation of a floral meristem by the inflorescence meristem. We have analyzed how this process is affected by mutant alleles of the Arabidopsis gene LEAFY. We show that LEAFY interacts with another floral control gene, APETALA1, to promote the transition from inflorescence to floral meristem. We have cloned the LEAFY gene, and, consistent with the mutant phenotype, we find that LEAFY RNA is expressed strongly in young flower primordia. LEAFY expression procedes expression of the homeotic genes AGAMOUS and APETALA3, which specify organ identify within the flower. Furthermore, we demonstrate that LEAFY is the Arabidopsis homolog of the FLORICAULA gene, which controls floral meristem identity in the distantly related species Antirrhinum majus.
The predicted products of floral homeotic genes, AGAMOUS (AG) from Arabidopsis thaliana and DEFICIENS A (DEF A) from Antirrhinum majus, have been shown previously to share strong sequence similarity with transcription factors from humans (SRF) and yeast (MCM1). The conserved sequence between these proteins is localized within a domain known to be necessary for the DNA binding and for the dimerization of SRF. We have isolated six new genes from A. thaliana, AGL1-AGL6, which also have this conserved sequence motif. On the basis of the sequence comparison between the AG and AGL genes, they can be assigned to two subfamilies of a large gene family. RNA dot blot analysis indicates that five of these genes (AGL1, AGL2, AGL4, AGL5, and AGL6) are preferentially expressed in flowers. In addition, in situ RNA hybridization experiments with AGL1 and AGL2 show that their mRNAs are detected in some floral organs but not in others. Our results suggest that these genes may act to control many steps of Arabidopsis floral morphogenesis. In contrast, the AGL3 gene is expressed in vegetative tissues as well as in flowers, suggesting that it functions in a broader range of tissues. We discuss possible roles of this gene family during the evolution of flowers.
Mutations in the homeotic gene agamous of the plant Arabidopsis cause the transformation of the floral sex organs. Cloning and sequence analysis of agamous suggest that it encodes a protein with a high degree of sequence similarity to the DNA-binding region of transcription factors from yeast and humans and to the product of a homeotic gene from Antirrhinum. The agamous gene therefore probably encodes a transcription factor that regulates genes determining stamen and carpel development in wild-type flowers.
We have characterized the floral phenotypes produced by the recessive homeotic apetala 1-1 (ap1-1) mutation in Arabidopsis. Plants homozygous for this mutation display a homeotic conversion of sepsis into brachts and the concomitant formation of floral buds in the axil of each transformed sepal. In addition, these flowers lack petals. We show that the loss of petal phenotype is due to the failure of petal primordia to be initiated. We have also constructed double mutant combinations with ap1 and other mutations affecting floral development. Based on these results, we suggest that the AP1 and the apetala 2 (AP2) genes may encode similar functions that are required to define the pattern of where floral organs arise, as well as for determinate development of the floral meristem. We propose that the AP1 and AP2 gene products act in concert with the product of the agamous (AG) locus to establish a determinate floral meristem, whereas other homeotic gene products are required for cells to differentiate correctly according to their position. These results extend the proposed role of the homeotic genes in floral development and suggest new models for the establishment of floral pattern.
The early development of the flower of Arabidopsis thaliana is described from initiation until the opening of the bud. The morphogenesis, growth rate, and surface structure of floral organs were recorded in detail using scanning electron microscopy. Flower development has been divided into 12 stages using a series of landmark events. Stage 1 begins with the initiation of a floral buttress on the flank of the apical meristem. Stage 2 commences when the flower primordium becomes separate from the meristem. Sepal primordia then arise (stage 3) and grow to overlie the primordium (stage 4). Petal and stamen primordia appear next (stage 5) and are soon enclosed by the sepals (stage 6). During stage 6, petal primordia grow slowly, whereas stamen primordia enlarge more rapidly. Stage 7 begins when the medial stamens become stalked. These soon develop locules (stage 8). A long stage 9 then commences with the petal primordia becoming stalked. During this stage all organs lengthen rapidly. This includes the gynoecium, which commences growth as an open-ended tube during stage 6. When the petals reach the length of the lateral stamens, stage 10 begins. Stigmatic papillae appear soon after (stage 11), and the petals rapidly reach the height of the medial stamens (stage 12). This final stage ends when the 1-millimeter-long bud opens. Under our growing conditions 1.9 buds were initiated per day on average, and they took 13.25 days to progress through the 12 stages from initiation until opening.
Variation in plant shoot structure may be described as occurring through changes within a basic unit, the metamer. Using this terminology, the apical meristem of Arabidopsis produces three metameric types sequentially: type 1, rosette; type 2, coflorescence-bearing with bract; and type 3, flower-bearing without bract. We describe a mutant of Arabidopsis, Leafy, homozygous for a recessive allele of a nuclear gene LEAFY (LFY), that has an inflorescence composed only of type 2-like metamers. These data suggest that the LFY gene is required for the development of type 3 metamers and that the transition from type 2 to type 3 metamers is a developmental step distinct from that between vegetative and reproductive growth (type 1 to type 2 metamers). Results from double mutant analysis, showing that lfy-1 is epistatic to the floral organ homeotic gene ap2-6, are consistent with the hypothesis that a functional LFY gene is necessary for the expression of downstream genes controlling floral organ identity.
Sadik, Sidki. (U. California, Davis.) Morphology of the curd of cauliflower. Amer. Jour. Bot. 49(3): 290–297. Illus. 1962.—The development of the curd and inflorescence of cauliflower, Brassica oleracea Linn., var. botrytis D.C., is described. The cultivars ‘Snowball M’ and ‘February-Early-March’ were studied. The curd has a nonfasciated and monopodial type of branching. Curd initiation of ‘Snowball M’ is not dependent on vernalization, but the curd of ‘February-Early-March’ and the floral primordia of both cultivars are initiated only after vernalization. Associated with flowering is the disruption of the curd by the elongation of some of the inflorescence branches. The initiation of leaves, branches, and floral primordia follows a 5 + 8 phyllotaxy throughout all stages of development. This system of phyllotaxy changes at the time of initiation of floral parts.
A population of Arabidopsis thaliana recombinant inbred lines was constructed and used to develop a high-density genetic linkage map containing 252 random amplified polymorphic DNA markers and 60 previously mapped restriction fragment length polymorphisms. Linkage groups were correlated to the classical genetic map by inclusion of nine phenotypic markers in the mapping cross. We also applied a technique for local mapping that allows targeting of markers to a selected genome region by pooling DNA from recombinant inbred lines based on their genotype. We conclude that random amplified polymorphic DNAs, used in conjunction with a recombinant inbred population, can facilitate the genetic and physical characterization of the Arabidopsis genome and that this method is generally applicable to other organisms for which appropriate populations either are available or can be developed.
Mutations in the APETALA3 (AP3) gene of A. thaliana result in homeotic transformations of petals to sepals and stamens to carpels. We have cloned the AP3 gene from Arabidopsis based on its homology to the homeotic flower gene deficiens (DEFA) from the distantly related plant Antirrhinum majus. The sequence of four ap3 mutant alleles and genetic mapping analysis prove that the DEFA homolog is AP3. Like several other plant homeotic genes, the AP3 gene contains a MADS box and likely acts as a transcription factor. The region-specific spatial expression pattern of AP3 rules out certain types of sequential models of flower development and argues in favor of a spatial model based on positional information. Since DEFA and AP3 have very similar protein products, mutant phenotypes, and spatial expression patterns, it is likely that these genes are cognate homologs.
The first step in flower development is the transition of an inflorescence meristem into a floral meristem. Each floral meristem differentiates into a flower consisting of four organ types that occupy precisely defined positions within four concentric whorls. Genetic studies in Arabidopsis thaliana and Antirrhinum majus have identified early-acting genes that determine the identify of the floral meristem, and late-acting genes that determine floral organ identity. In Arabidopsis, at least two genes, APETALA1 and LEAFY, are required for the transition of an influorescence meristem into a floral meristem. We have cloned the APETALA1 gene and here we show that it encodes a putative transcription factor that contains a MADS-domain. APETALA1 RNA is uniformly expressed in young flower primordia, and later becomes localized to sepals and petals. Our results suggest that APETALA1 acts locally to specify the identity of the floral meristem, and to determine sepal and petal development.
We characterized the distribution of AGAMOUS (AG) RNA during early flower development in Arabidopsis. Mutations in this homeotic gene cause the transformation of stamens to petals in floral whorl 3 and of carpels to another ag flower in floral whorl 4. We found that AG RNA is present in the stamen and carpel primordia but is undetectable in sepal and petal primordia throughout early wild-type flower development, consistent with the mutant phenotype. We also analyzed the distribution of AG RNA in apetela2 (ap2) mutant flowers. AP2 is a floral homeotic gene that is necessary for the normal development of sepals and petals in floral whorls 1 and 2. In ap2 mutant flowers, AG RNA is present in the organ primordia of all floral whorls. These observations show that the expression patterns of the Arabidopsis floral homeotic genes are in part established by regulatory interactions between these genes.
The Arabidopsis floral homeotic gene APETALA1 (AP1) encodes a putative transcription factor that acts locally to specify the identity of the floral meristem and to determine sepal and petal development. RNA tissue in situ hybridization studies show that AP1 RNA accumulates uniformly throughout young floral primordia, but is absent from the inflorescence meristem. Later in development, AP1 RNA is excluded from cells that will give rise to the two inner whorls of organs. Here we show that AP1 expression is under the control of two negative regulators: the meristem identity gene TERMINAL FLOWER represses AP1 RNA accumulation in the inflorescence meristem, and the organ identity gene AGAMOUS prevents AP1 RNA accumulation in the two inner whorls of wild-type flowers. These and other data presented here lead to a revised model for the regulatory interactions among the genes specifying floral organ identity in Arabidopsis.
In Arabidopsis, floral meristems arise in continuous succession directly on the flanks of the inflorescence meristem. Thus, the pathways that regulate inflorescence and floral meristem identity must operate both simultaneously and in close spatial proximity. The TERMINAL FLOWER 1 (TFL1) gene of Arabidopsis is required for normal inflorescence meristem function, and the LEAFY (LFY), APETALA 1 (AP1), and APETALA 2 (AP2) genes are required for normal floral meristem function. We present evidence that inflorescence meristem identity is promoted by TFL1 and that floral meristem identity is promoted by parallel developmental pathways, one defined by LFY and the other defined by AP1/AP2. Our analysis suggests that the acquisition of meristem identity during inflorescence development is mediated by antagonistic interactions between TFL1 and LFY and between TFL1 and AP1/AP2. Based on this study, we propose a simple model for the genetic regulation of inflorescence development in Arabidopsis. This model is discussed in relation to the proposed interactions between the inflorescence and the floral meristem identity genes and in regard to other genes that are likely to be part of the genetic hierarchy regulating the establishment and maintenance of inflorescence and floral meristems.
Culture conditions were developed that induce Arabidopsis thaliana (L.) Heynh. root cuttings to regenerate shoots rapidly and at 100% efficiency. The shoots produce viable seeds in vitro or after rooting in soil. A transformation procedure for Arabidopsis root explants based on kanamycin selection was established. By using this regeneration procedure and an Agrobacterium tumor-inducing Ti plasmid carrying a chimeric neomycin phosphotransferase II gene (neo), transformed seed-producing plants were obtained with an efficiency between 20% and 80% within 3 months after gene transfer. F(1) seedlings of these transformants showed Mendelian segregation of the kanamycin-resistance trait. The transformation method could be applied to three different Arabidopsis ecotypes. In addition to the neo gene, a chimeric bar gene conferring resistance to the herbicide Basta was introduced into Arabidopsis. The expression of the bar gene was shown by enzymatic assay.
Homeotic mutants have been useful for the study of animal development. Such mutants are also known in plants. The isolation and molecular analysis of several homeotic genes in Antirrhinum majus provide insights into the underlying molecular regulatory mechanisms of flower development. A model is presented of how the characteristic sequential pattern of developing organs, comprising the flower, is established in the process of morphogenesis.
Rapid-cycling populations of six economically important species in the genus Brassica have unusual potential for resolving many problems in plant biology and for use in education. Rapid-cycling brassicas can
produce up to ten generations of seed per year and serve as models for research in genetics, host-parasite relations, molecular
biology, cell biology, plant biochemistry, population biology, and plant breeding. Brassicas are a highly diverse group of
crop plants that have great economic value as vegetables and as sources of condiment mustard, edible and industrial oil, animal
fodder, and green manure. These plants can also be used in the classroom as convenient, rapidly responding, living plant materials
for "hands on" learning at all levels of our educational system.
- Bowman
- S Shannon
- Genetic Interactions
- Regulate
- Development In
- Arabidopsis
- E A Schultz
- A Homeotic Gene That Regulates Inflorescence Development In Leafy
- Arabidopsis
- J L Bowman
- Control Of Flower
- Development In Arabidopsis-Thaliana
- By
- Genes