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Flower Heads in Asteraceae—Recruitment of Conserved Elomaa et al. Horticulture Research (2018) 5:36 Horticulture Research DOI 10.1038/s41438-018-0056-8 www.nature.com/hortres REVIEW ARTICLE Open Access Flower heads in Asteraceae—recruitment of conserved developmental regulators to control the flower-like inflorescence architecture Paula Elomaa 1,YafeiZhao1 and Teng Zhang 1 Abstract Inflorescences in the Asteraceae plant family, flower heads, or capitula, mimic single flowers but are highly compressed structures composed of multiple flowers. This transference of a flower-like appearance into an inflorescence level is considered as the key innovation for the rapid tribal radiation of Asteraceae. Recent molecular data indicate that Asteraceae flower heads resemble single flowers not only morphologically but also at molecular level. We summarize this data giving examples of how rewiring of conserved floral regulators have led to evolution of morphological innovations in Asteraceae. Functional diversification of the highly conserved flower meristem identity regulator LEAFY has shown a major role in the evolution of the capitulum architecture. Furthermore, gene duplication and subsequent sub- and neofunctionalization of SEPALLATA- and CYCLOIDEA-like genes in Asteraceae have been shown to contribute to meristem determinacy, as well as flower type differentiation—key traits that specify this large family. Future challenge is to integrate genomic, as well as evolutionary developmental studies in a wider selection of Asteraceae fl 1234567890():,; 1234567890():,; 1234567890():,; 1234567890():,; species to understand the detailed gene regulatory networks behind the elaborate in orescence architecture, and to promote our understanding of how changes in regulatory mechanisms shape development. Introduction have proposed scenarios that the split of Asteraceae from Asteraceae, commonly referred as the sunflower or its ancestor occurred in Patagonia, southern South daisy family, has a prominent place in our daily life as it America some time before the Eocene 56–34 million includes many economically important food crops (sun- years ago, and it spread to Africa before the two con- flower, lettuce, artichoke, endive, and safflower), herbal tinents became geographically isolated3,4. The family then and medicinal species (Calendula, Artemisia, Echinacea), rapidly diversified and colonized the earth. This explosive as well as popular ornamentals (gerbera, chrysanthemum, tribal radiation has been associated with complex history aster, dahlia, zinnia, and marigold). Also some noxious of whole-genome duplication events, and especially with a weeds, such as dandelion or thistle are members of the paleopolyploidization event shared with Asteraceae and family. Asteraceae represents the largest family of flow- its sister family Calycearaceae, as well as a second round ering plants with around 25,000 species that are wide- of genome duplications among the core Asteraceae spread into nearly all terrestrial habitats except of the tribes5,6. At the genetic level, functional analyses are Antarctica1,2. From evolutionary perspective, Asteraceae necessary to explore how the ancestral polyploidization is a young family. Relatively recent discoveries of fossils has contributed to the evolution of the extensive diversity of developmental traits, secondary metabolites, as well as life histories discovered in Asteraceae. Correspondence: Paula Elomaa (paula.elomaa@helsinki.fi) 1Department of Agricultural Sciences, Viikki Plant Science Centre, University of Helsinki, P.O.Box 27, 00014 Helsinki, Finland © The Author(s) 2018 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a linktotheCreativeCommons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Elomaa et al. Horticulture Research (2018) 5:36 Page 2 of 10 The key morphological innovation that has been asso- several capitula may also form synflorescences being ciated with the evolutionary success of Asteraceae is the arranged in distinct branched systems, such as racemes unique head-like inflorescence, capitulum that is the (e.g., Artemisia pycnocephala), cymes (e.g., Senecio vul- distinguishing feature of the whole family. Capitulum is a garis), or corymbs (e.g., Achillea millefolium)13. Another pseudanthium, a false flower that superficially mimics a hierarchical level of complexity is generated when flower single flower but is a highly aggregated structure com- heads are aggregated onto a single receptacle, and form prised of multiple flowers with specialized functions. higher order structures, ‘heads within heads’, also known Asteraceae is largely pollinated by insects (rarely by birds), as capitulescence or syncephalium (e.g., Craspedia, Echi- – and several studies have indicated that the unique orga- nops, Lagascea)14 16 (Fig. 1d–f). nization of the capitulum has selective advantage to pol- A characteristic feature shared by distinct head-like – linator attraction and plant vigor7 9. Moreover, the showy inflorescences is the spatial arrangement of individual capitulum with all the diversity in shapes and colors flowers on the expanded receptacle (Fig. 1c). They appear generated by breeders is surely a key attraction to con- in a phyllotactic pattern that follow strict clockwise and sumers contributing to the economic significance of this counterclockwise spirals (contact parastichies), the num- family in the ornamental industry. In this review, we aim bers of which always follow the two consecutive numbers to summarize the recent research in Asteraceae models to in the mathematical Fibonacci series: 1, 1, 2, 3, 5, 8, 13, 21, understand genetic regulation of capitulum development, 34, etc. where each number is a sum of the two previous as well as its organization and evolution. Altogether, the ones. The spirals can usually reach high numbers; for data demonstrate novel gene functions for both conserved example flowers on gerbera and sunflower heads are floral regulators as well as duplicated genes that through typically arranged in 34/55 and 55/89 spirals, respectively. sub- and neofunctionalization have gained specific roles The initiation of individual flowers in a capitulum has in regulation of the elaborate inflorescence architecture. been thought to occur in an acropetal manner, from the margins toward the center of the capitulum. This is Organization of Asteraceae heads indeed the case in homogamous heads with only single- Asteraceae flower heads combine multiple flowers flower types, however, morphological studies have indi- attached on a single receptacle (Fig. 1). After induction of cated that in heterogamous heads the early ontogeny of flowering, the early ontogeny of the head is characterized marginal ray flower primordia is distinct10,13. In fact, in by rapid expansion of the inflorescence meristem extreme cases, ray flower development may proceed (receptacle), while later the meristematic area gradually basipetally toward the margins of the head (instead of the shrinks and is fully consumed by emerging flower pri- center), or in milder cases ray primordia show a devel- mordia10,11. In simple heterogamous, or radiate flower opmental arrest compared to the development of an – heads, the margin of the capitulum is occupied by showy adjacent disc or trans flower primordia10,13,17 19. This ray flowers and the center with less conspicuous disc differential early ontogeny has turned out to be crucial for flowers. In sunflower (Helianthus), the marginal ray understanding how distinct flower types have evolved (see flowers are sterile and they develop extended ligules while below). the central disc flowers are perfect, and produce pollen. In gerbera (Gerbera) the ray flowers are female, and it may Flower meristem identity gene functions give also develop intermediate trans flowers that resemble rays light for understanding the evolution of the but are just smaller in size (Fig. 1a, b). In contrast, the capitulum architecture homogamous heads are formed of only single-flower Inflorescences are typically branched structures that types. For example, the heads of lettuce (Lactuca) are bear flowers. As known from the conventional model composed of only ligulate ray flowers while the discoid species, the major difference between the two basic types heads in thistles, representing several genera in Aster- of inflorescences, racemes in Arabidopsis or Antirrhinum, aceae, develop solely disc flowers. The discoid capitula and cymes in Solanaceae species such as petunia or have been considered as an ancestral condition in Aster- tomato, is in their determinacy20. The elongating, inde- aceae1,12 where the emergence of ray flowers has occurred terminate racemes continuously produce flowers in the multiple times independently. The entire head is sur- flanks of the inflorescence meristem (IM) while in cymes rounded by involucral bracts that behave like sepals in the meristem always terminates in a flower, but forms a single
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