The Plant Cell, November. 2017, American Society of Plant Biologists. All rights reserved
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1 The Genetics of Floral Development Teaching Guide Overview The development of flowers in angiosperm plants provided a critical evolutionary advantage, allowing more options for pollen dispersal and seed dispersal. In addition, the resulting fruits and grains provide important food sources for humans and other animals. Floral organs usually form in a series of concentric whorls from the stem cells of the floral meristem. This process depends on the activation of a core set of transcription factors, most of which encode MADS box proteins. Evolutionary changes in these regulators, including gene duplications, appear to account for some of the diversity of floral form. Learning objectives By the end of this module, students should be able to: Diagram the placement of whorls of floral organs in a wild-type Arabidopsis flower Summarize the role of gene regulation in control of floral development Identify which floral development genes specify each whorl of floral organs Recognize the role of forward and reverse genetics in elucidation of the ABC model Compare the roles of floral development genes across various plant species Observe differences in floral morphology and predict how these changes may relate to altered function or expression of key floral development genes Study/ exam questions What are the four types of floral organ in Arabidopsis? Which organs are described by the perianth? What structures are formed by the vegetative shoot apical meristem, the inflorescence meristem and the floral meristem? A seedling is not capable of producing flowers as the genes that promote the transition to flowering are silenced. What external factors can promote the transition to flowering? What might be the consequences of flowering prematurely? Forward genetic studies of both Arabidopsis thaliana and Antirrhium majus led to the development of the ABC model. Describe what is meant by a forward genetic study. What can you learn about a gene s function from such a study? Diagram a rice flower and how its organs are specified by A, B and C genes. What type of protein is encoded by most of the identified floral homeotic genes? What is the floral quartet model and how is it supported by the genetic data? Some flowers like lilies have two whorls of tepals (petal-like organs) rather than sepals and petals. Given the predictions of the ABC model, how might you expect gene expression to be different in a lily in order to produce tepals? Contrast this to what you might expect in a clematis, which produces two whorls of sepals in the perianth, rather than sepals and petals. Flower development extends beyond the ABC genes. What genes specify the dorsal and ventral pattern of snapdragon? How do loss-of-function mutants of these genes support your statement? ABCDE genes control the fate of flower organs, but they do so by changing expression of other genes. Describe two methods used by researchers to identify transcription factor targets genes.
2 Discussion questions The genes controlling the transition to flowering are also well known, and described in the review by Wils and Kaufmann (2017) Biochim. Biophys. Acta /j.bbagrm In what ways do these genes interact with the ABCDE genes involved in flower development? Look at the papers that initially characterized A, B, and C genes. What methods were used to identify where the genes are expressed in wild-type plants? How do these data support the results from loss-of-function mutant phenotypes? The classic ABC model is drawn with the A and C genes falling on the same line, and the B genes occupying a separate line. Why is it drawn in this way? We now know that the original ideas behind the antagonism between A and C genes is an oversimplification. How are the expression domains controlled [hint, look at Figure 4 of Ó'Maoiléidigh et al. (2013) New Phytol /nph.12444]. In the early studies of flower development, E gene function was not identified. In Arabidopsis, E gene function is contributed by the four Sepellata genes. Knowing this, can you speculate on why the E genes were not initially identified as critical for flower formation? How have reverse genetics approaches aided our understanding of the roles of MADS box genes in flower development? If expression of B and C genes is sufficient to specify petal identity in whorl 3, what might happen if these B and C genes were expressed ectopically elsewhere in the plant? The article states that MADS box genes are present in all land plants. What roles do they have in non-flowering plants? (Hint see Gramzow and Theissen (2010), Genome Biology /gb ) Imagine you have identified a new, previously uncharacterized gene encoding a MADS-box transcription factor. Describe experiments you could do to address 1) where your gene is expressed, 2) whether the encoded MADS-box protein can bind to DNA and what sequences it preferentially binds to, 3) how its expression or lack of expression affects mrna accumulation, and 4) what biological processes your gene contributes to. Dubois et al. looked at differences in flower development in wild and cultivated roses [Dubois et al. (2010) PLoS One 5. e9288]. Explain how their findings about the relative expression patterns of A and C genes suggest how many-petalled roses arose. Flower development has also been studied in the monocot order Zingiberales that includes birdof-paradise, ginger and banana. How do E genes contribute to floral diversification in this group of plants? [See Yockteng et al (2013) Mol. Evol /molbev/mst137]. Read more about one of the downstream genes described in the lesson (NOZZLE/ SPOROCYTELESS, RABBIT EARS, OR SUPERMAN). Write a one-page summary of how this gene is regulated by ABCDE genes, and its function in flower formation. Daffodils are another form of flower that doesn t follow the simple rules described by the ABCDE model. Waters et al (2013), Plant J /tpj describe the development of the corona in Narcissus bulbocodium, the hoop-coat daffodil. What do their findings suggest about the origins of this structure?
3 Lecture Synopsis Overview and general background (1 6) Most flowers are made of concentric whorls of organs, including the outer perianth (non-reproductive structures such as petals and sepals) and inner reproductive structures (stamen and/ or carpels). Within that pattern, flowers occur in many forms, with varying organ number and shape, although all have a perianth and male and/or female reproductive structures. Flower structures are important for their reproductive success including interactions with pollinators. Molecular control of the transition to flowering (7 18) Reproductive development occurs after a period of vegetative growth. Meristems are specialized tissues that produce cells and maintain populations of undifferentiated cells. During the transition to reproductive growth, a leaf-producing vegetative shoot meristem forms an inflorescence meristem, which produces floral meristems. Floral meristems produce floral organs. The transition to reproductive growth involves a change in gene expression. Genes that promote reproduction are kept in a silent state through epigenetic signals until the time is right. At that time the silencing signals are removed and genes that promote flowering switch on. ABC(DE) model of flower development (19 41) The ABC model of flower development was derived from studies of Arabidopsis thaliana and Antirrhinum majus (snapdragon). According to this model, the 1 st whorl (sepals) is specified by A genes, the 2 nd whorl (petals) is specified by A+B genes, the 3 rd whorl (stamens) is specified by B+C genes and the 4 th whorl (carpel) is specified by C genes, an example of combinatorial control, in which different combinations of a small group of genes results in different patterns of gene activation. When one of these sets of genes is mis-regulated or missing, one type of floral organ can be converted to another, in a homeotic transformation. Similar patterns are found in many other plant species, including crop plants such as rice (Oryza sativa). The ABC model was later modified to add D genes, which specify ovaries, and E genes, which work together with A, B and C genes to specify each floral organ type. MADS box proteins (42 51) Most of the ABCDE genes belong to a family that encodes MADS box proteins. These proteins share a conserved amino acid sequence that allows them to bind to other MADS box proteins and to DNA. They work in groups of two to four proteins to activate specific target genes. MADS box proteins specifically bind DNA regions with a CArG box, a conserved sequence of nucleotides. MADS box proteins can also regulate each other. Floral diversity (52 73) MADS box genes are present in all land plants, but angiosperms (flowering plants) often have many more MADS box genes than other plants. Changes in expression of ABC genes can change floral morphology. Broader or narrower expression domains of B genes can result in missing or extra whorls of petals (such as in tulip or clematis). Similarly, changes in C gene expression can result in extra whorls of petals, which is often desirable in ornamental plants such as roses. Other aspects of flower morphology (74 83) There are additional variations in flower form beyond changes in the main whorls of floral organs. Composite flowers such as daisies have multiple flower types within a single flower head. A gradient CYC gene expression helps specify which type of flower will form where within the flower head. Zygomorphic flowers like snapdragon have a single axis of symmetry. CYC and partner genes help to specify the difference between the top (dorsal) and bottom (ventral) side of these flowers. Finally, some
4 flowers can be only male or only female, whereas most are both male and female. While the specification of male vs female flowers seems to depend on factors other than the ABC genes, changes in B gene expression does correlate with the difference between male and female flowers. Finally duplications in MADS box genes appears to correlate with differences in floral form within plant families. Downstream targets of ABCE genes (84 93) The ABCE regulators act by turning on or off transcription of specific target genes, which help to specify organ identity and boundaries between organ types. Targets of the ABCE genes include other transcription factors, signaling molecules and plant growth hormones. A few key examples are discussed here. Many additional targets have been identified in large scale gene expression studies but their functions and interactions are not all fully understood. Future directions (94) While many floral development regulators have been identified, there are many more open questions. Some of these include identifying additional genetic changes that account for differences in floral form across species, understanding the roles of plant growth hormones as downstream targets of the ABCE genes, and further developing our understanding of the gene regulatory networks that are regulated by the ABCE genes.
5 Slide concepts (summaries in gold, key topics in bold) Slides Table of contents/ concept 1 Transcriptional control of floral development 2 LEARNING OBJECTIVES 3 Overview: Most plants have whorls of floral organs arranged in concentric circles 4 Flowers occur in many different forms, with varying organ number and shape 5 Flowers share a perianth (non-reproductive structures) and male and/ or female reproductive structures 6 Why floral structure matters 7 Molecular control of the transition to flowering 8 Plants develop new structures partly through expression of different developmental genes 9-10 Development is promoted by different types of meristems 11 Pools of stem cells receive signals that promote the development of specific tissue types 12 Before the plant is ready to flower, floral development genes are kept in check 13 Chromatin packaging affects gene expression 14 Epigenetic signals can repress flower development genes 15 PRC can inactivate, while TrxG can activate, target genes 16 When it is time to flower, cells become specified from the meristem via activation of specific genes in response to internal and external cues 17 Transcription factors in the inflorescence meristem activate genes that specify the floral meristem 18 Summary of flower initiation 19 Introduction to the ABC(DE) model of flower development 20 Floral development models were fist built from studies in Arabidopsis thaliana and Antirrhinum majus 21 Early studies used scanning electron microscopy (SEM) to observe changes in the floral meristem 22 In the classic ABC model, key transcription factors produce the 4 whorls of floral organs 23 Homeotic mutations convert one floral organ to another 24 These mutants were used in a forward genetic approach, in which phenotype is used to help understand gene function 25 DISCUSSION QUESTIONS 26 Missing B gene function results in no petals or stamen, and produces extra sepals and carpels 27 MADS box genes can regulate each other 28 DISCUSSION QUESTIONS 29 Missing C gene function results in no stamen or carpels, and produces extra sepals and petals in repeating whorls 30 Missing A gene function results in missing petals, and can result in sepals converted to carpel-like organs 31 MADS box genes can regulate each other: A and C genes can inhibit each
6 other s expression, affecting associated organs 32 Missing A gene function can also cause buds where petals would normally form 33 ABC model in rice Rice lacking A function show homeotic changes Modification of ABC model: D and E 39 Floral meristems form leaf-like structures when E gene function is lost 40 ABCDE genes in Arabidopsis, Antirrhinum and Petunia 41 Summary of ABC model 42 Most floral development genes encode MADS domain proteins 43 DNA and protein sequences allow a reverse genetics approach, in which sequence is used to understand gene function 44 The floral ABCDE genes bind DNA to regulate transcription 45 MADS domain proteins share a conserved amino acid sequence motif 46 ABCE proteins function in combinations 47 DISCUSSION QUESTIONS 48 Overexpression of B and C genes is sufficient to convert Arabidopsis leaves into petal-like structures 49 MADS box genes bind to specific DNA sequences and bend DNA 50 MADS box genes also perform other functions 51 Summary of MADS box function 52 Molecular foundations of floral diversity 53 Genetic and evolutionary studies can help us learn about origins of floral diversity 54 MADS box genes cluster into various groups 55 MADS box genes are present in all land plants 56 Amplification of MADS box genes in flowering plants may lead to new functions and altered flower morphology 57 DISCUSSION QUESTIONS 58 Modifying expression of the ABC genes can change flower morphology 59 Limiting the location of B gene expression can result in plants with no true petals 60 B-class gene expression affects presence or absence of petals in different species of Clematis 61 Expansion of B gene expression can result in two whorls of petals or tepals 62 Tulips express B genes in both of their outer whorls 63 Partially reduced expression of B or C genes could affect tulip morphology 64 Orchid morphology may be due to duplications of B genes 65 Changes in floral development affect economically important plants 66 C-gene expression is restricted in roses with double-petal phenotype 67 Changing expression of C genes may shift the boundary between whorls of organs Changes in floral development genes may promote new species formation 70 Zingiberales (including ginger and banana) show many different flower morphologies 71 Duplications of class E genes may contribute to differences in flower
7 morphology 72 Homologs of ABCE genes have also been identified in other agriculturally important plants 73 Summary: Role of MADS box genes in variations of floral morphology 74 Introduction to other variations in flower form: ray vs disc flowers, radially vs bilaterally symmetrical flowers, male vs female flowers and more 75 Composite flowers have multiple flower types within a flower head 76 Daisies show differences in expression of B and E genes in different flower types 77 Different flower types in a single flower head can be specified by the TCP gene CYC2 78 Flowers can have different types of symmetry 79 Different patterns of genes are expressed in the top (dorsal) and bottom (ventral) tissues 80 Loss of the dorsal-specifying CYC and DCH genes result in snapdragon flowers with radial symmetry 81 Flowers can be only male, only female, or both 82 Male and female flowers have different expression of B genes 83 Summary of variations in floral form 84 Introduction: ABCE genes activate transcription of downstream genes to promote floral organ development ABC proteins activate transcription of downstream genes to promote floral organ development 88 B genes promote their own expression in an example of auto-regulation 89 Nozzle/Sporocyteless is a direct target of AG and microsporogenesis and megaspore differentiation 90 Rabbit ears (RBE) promotes petal formation 91 Superman (SUP) separates the 3 rd and 4 th whorls 92 Plant growth hormones as targets of ABCE genes 93 Summary of transcriptional targets of ABCE genes 94 Future directions
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