Elomaa, Paula Riitta

English

Helsingin yliopiston digitaalinen arkisto

Journal of Experimental Botanydoi:10.1093/jxb/erw489This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details)FEATURED IMAGEMy favourite flowering image: a capitulum of AsteraceaePaula ElomaaDepartment of Agricultural Sciences, Viikki Plant Science Centre, PO Box 27, 00014 University of Helsinki, Finlandpaula.elomaa@helsinki.fiEditor: Lars Hennig, Swedish University of Agricultural Sciences I could have selected my favourite flowering image from thousands of astonishing images that have captured the geometric regularity of head-like inflorescences in Asteraceae. These unique inflorescences pack hun-dreds of flowers into precise spirals whose numbers follow a famous mathematical rule. Meanwhile, the whole structure may mislead a layman (or a pollinator) by mimicking a single solitary flower although it con-sists of morphologically and functionally distinct types of flowers.Regular, reproducible patterns in nature are fascinating and inspiring. They represent enigmatic mathematical and bio-logical problems but also provide inspiration and aesthetic delight that has impacted, for example, arts and architecture. Inflorescence architecture in terms of arrangement of flow-ers in branched systems provides an example of this geomet-ric regularity that is not only fascinating per se but affects crop yield, fitness, and adaptation of plants. The flowering image I selected represents a classical example of spiral phyl-lotaxis found in composite inflorescences such as sunflower (Helianthus sp.). This image (Fig. 1), however, is of a com-mercial cultivar of the ornamental crop Gerbera hybrida, the model species that our lab has worked on for more than 25 years. This structure keeps on bringing surprises and moments of joy year by year.The composite inflorescence, capitulum, or flower head in Asteraceae assembles multiple flowers into a single, highly compressed structure. It is a very effective reproductive unit and with an apparent selective value, considered to be the key innovation for diversification of  this largest family of flowering plants. In the case of  sunflower or gerbera, hun-dreds of  individual flowers are all attached to a flat enlarged receptacle. As beautifully visible in the image, the develop-ing flowers are organized into left- and right-winding spirals (parastichies). Intriguingly, the number of  these spirals fol-low two consecutive numbers of  Fibonacci series (1, 1, 2, 3, 5, 8, 13, 21, 34 … where each number is the sum of the two preceding numbers in the series). In the particular cultivar in my favourite image, there are 34 clockwise and 21 anti-clock-wise spirals (you may check this!) while our standard model cultivar, Terra Regina, typically shows 55 and 34 spirals, respectively. Interestingly, although the Fibonacci numbers clearly dominate, non-Fibonacci structures such as double Fibonacci numbers (2, 4, 6, 10, 16, 26…), Fibonacci ±1 or Lucas numbers (1, 3, 4, 7, 11, 18…) do appear, as recently demonstrated in a large citizen science experiment engag-ing the public to grow and count sunflower spirals (Swinton et  al., 2016). It seems that there are always exceptions to the rule; the experiment revealed cases where spirals were This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.© The Author 2017. Published by Oxford University Press on behalf of the Society for Experimental Biology.Fig. 1. A composite inflorescence of Gerbera hybrida showing spiral phyllotaxis of emerging flowers. Hundreds of flowers are packed into the capitulum that mimics a solitary flower and is surrounded by green, involucral bracts.Page 2 of 3 | Elomaacountable but not Fibonacci, as well as well-defined paras-tichies in only one direction or even uncountable structures. In a shoot apex, the spiral emergence of  leaf  primordia fol-lows an approximate golden angle (137.5°), and their posi-tioning in the fist available space between already existing primordia is associated with formation of  auxin maxima at incipient primordia and on subsequent depletion of  auxin in their vicinity (Reinhardt et al., 2003; Heisler et al., 2005). However, it is still unclear what are the developmental mech-anisms that regulate the organization of  the expanded capit-ulum that is much larger in its dimensions, and how they are linked to observed deviations of  the Fibonacci struc-ture. Mathematical modelling can reproduce many of  these remarkable patterns (e.g. Douady and Couder, 1996; Smith et al., 2006; Zagórska-Marek and Szpak, 2008; Owens et al., 2016), and have already provided inspiring hypotheses to be tested at the molecular level.The visual attractiveness of  composite inflorescences is further enhanced by the presence of  distinct flower types. Normally, gerbera (like sunflower) has showy, large and bilaterally symmetrical marginal ray flowers, and smaller, more radially symmetrical central disc flowers. The image I selected is taken from a cultivar that only develops male sterile ray-like flowers (so-called crested phenotype; Kloos et al. 2004; Broholm et al., 2014 ; Juntheikki-Palovaara et al., 2014). The image represents an early developmental stage of  the inflorescence and, therefore, the showy petals have not yet reached their full size. The famous painting by Vincent van Gogh with double-flowered sunflower heads has preserved a similar mutant phenotype in the history of  art (Chapman et al., 2012). The molecular studies in gerbera (Broholm et al., 2008), Senecio (Kim et al., 2008), as well as sunflower (Chapman et al., 2012) all indicated that CYCLOIDEA-like TCP domain transcription fac-tors, among the key developmental regulators in plants, have been recruited to regulate capitulum architecture. This gene family has expanded in Asteraceae and consequently evolved novel functions in regulating ray identity. In the crested gerbera as well as in double-flowered sunflower, up-regulation of  a CYC-like TCP gene converted the disc flowers into ray-like flowers by affecting the growth of  the petals, and disrupting stamen development (Chapman et al., 2012; Juntheikki-Palovaara et al., 2014).The Asteraceae inflorescences are false flowers (pseudan-thia) that mimic solitary flowers. As visible from the image, the capitulum is surrounded by involucral bracts (the bright green leaf-like organs) that perform a sepal-like, protective function. The showy ray flowers can be seen to be analogous to attractive petals in solitary flowers, and the hermaphrodite disc flowers to reproductive organs (carpels/stamens). By conducting functional analyses for the gerbera orthologues of  flower meristem identity genes LEAFY (LFY) and UNUSUAL FLORAL ORGANS (UFO), we recently discovered that the capitulum resem-bles a solitary flower also at the molecular level (Zhao et al., 2016). As in single flower meristems in Arabidopsis, the gerbera GhLFY expression was found to be uniform across the naked inflorescence meristem, defining it as a determinate structure. Loss of  GhLFY expression led to loss of  determinacy of  the capitulum and disrupted phyl-lotaxis. In contrast, by ectopic expression of  GhUFO, this large structure gained floral fate; instead of  flower primor-dia, the meristem initiated numerous flower organ primor-dia arranged in whorled phyllotaxis (Zhao et al., 2016). Our studies also provided the first molecular evidence to explain the evolutionary origin of  flower types. Several botanical studies have indicated that although ray flowers are located along the Fibonacci spirals, they show delayed development compared with adjacent disc (or trans) flow-ers (Harris, 1995; Bello et al., 2013). In an extreme case, ray flowers initiate after the disc flowers and their devel-opment proceeds in a different direction, namely towards the margins of  the head (Harris et al., 1991). We showed that GhLFY has evolved a novel function in regulating the early ontogeny of  ray flowers in gerbera (Zhao et al., 2016). Silencing of  GhLFY converted ray flowers into branched structures resembling those found in Calyceraceae, the phylogenetically closest relatives of  Asteraceae (Pozner et al., 2012). Our data thus indicated that, during evolution, GhLFY has played a major role in contributing to the gain of  floral fate for these peripheral branches still found in capitula of  Calyceraceae, and that the differential devel-opment of  ray flowers relates to their different ontogenic origin from separate branching systems.Although some details on the gene functions and molecu-lar networks controlling capitulum architecture and flower type differentiation have been revealed, the future chal-lenge is to understand the dynamics of  early patterning of the inflorescence meristem and establishment of  the spi-ral phyllotaxis. Classical experiments in sunflower already showed that patterning can be disrupted by wounding (Palmer and Marc, 1982; Hernandez and Palmer, 1988, 1990). Interestingly, wounding creates a new margin that resets patterning and initiates successive formation of  new bracts, rays, and discs, in this particular order. This raises a still unresolved fundamental question; how does the margin specify initiation of  organ/flower primordia and what is the nature of  the signal that it creates? Furthermore, an extra level of  complexity in species developing capitula within capitula (syncephalium) surely adds to the number of  vari-ations on a theme.AcknowledgementsMy special thanks go to Dr Sari Tähtiharju for the inspiring image of Gerbera hybrida. I am especially grateful to my colleague Professor Teemu Teeri for his continuous support and contribution to gerbera research. We have worked on the gerbera model for more than 25 years starting from a sin-gle promoter, but hopefully seeing the genome soon. I also want to acknowl-edge Professor Victor Albert for fruitful collaboration and for guiding us (molecular biologists) to the world of evo-devo! During the years, many col-leagues and friends have devoted their enthusiasm, valuable ideas, and con-tribution to this research. Thank you all.Key words: Asteraceae, capitulum, gerbera, inflorescence, phyllotaxis, sunflower.My favourite flowering image | Page 3 of 3ReferencesBello MA, Álvarez I, Torices R, Fuertes-Aguilar J. 2013. Floral development and evolution of capitulum structure in Anacyclus (Anthemideae, Asteraceae). Annals of Botany 112, 1597–1612.Broholm SK, Tähtiharju S, Laitinen RAE, Albert VA, Teeri TH, Elomaa P. 2008. A TCP domain transcription factor controls flower type specification along the radial axis of the Gerbera (Asteraceae) inflorescence. Proceedings of the National Academy of Sciences, USA 105, 9117–9122.Broholm SK, Teeri TH, Elomaa P. 2014. Molecular control of inflorescence development in Asteraceae. In: Jacquot J-P, Gadal P, Fornara F eds. The molecular genetics of floral transition and flower development. Advances in Botanical Research, Vol. 72. Amsterdam: Elsevier, 297–334.Chapman MA, Tang S, Draeger D, Nambeesan S, Shaffer H, Barb JG, Knapp SJ, Burke JM. 2012. Genetic analysis of floral symmetry in Van Gogh’s sunflowers reveals independent recruitment of CYCLOIDEA genes in the Asteraceae. PLoS Genetics 8, e1002628.Douady S, Couder Y. 1996. Phyllotaxis as a dynamical self organizing process part I: the spiral modes resulting from time-periodic iterations. Journal of Theoretical Biology 178, 255–274.Harris EM. 1995. Inflorescence and floral ontogeny in Asteraceae: a synthesis of historical and current concepts. Botanical Review 61, 93–278.Harris EM, Tucker SC, Urbatsch LE. 1991. Floral initiation and early development in Erigeron philadelphicus (Asteraceae). American Journal of Botany 78, 108–121.Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM. 2005. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Current Biology 15, 1899–1911.Hernandez LF, Palmer JH. 1988. Regeneration of the sunflower capitulum after cylindrical wounding of the receptacle. American Journal of Botany 75, 1253–1261.Hernandez LF, Palmer JH. 1990. Colchicine-induced displacement of floral organ regeneration sites in the wounded sunflower capitulum. Microscopía Electrónica y Biología Celular 14, 159–164.Juntheikki-Palovaara I, Tähtiharju S, Lan T, Broholm SK, Rijpkema AS, Ruonala R, Kale L, Albert VA, Teeri TH, Elomaa P. 2014. Functional diversification of duplicated CYC2 clade genes in regulation of inflorescence development in Gerbera hybrida (Asteraceae). The Plant Journal 79, 783–796.Kim M, Cui ML, Cubas P, Gillies A, Lee K, Chapman MA, Abbott RJ, Coen E. 2008. Regulatory genes control a key morphological and ecological trait transferred between species. Science 322, 1116–1119.Kloos WE, George CG, Sorge LK. 2004. Inheritance of flower types of Gerbera hybrida. Journal of the American Society for Horticultural Science 129, 802–810.Owens A, Cieslak M, Hart J, Classen-Bockhoff R, Prusinkiewicz P. 2016. Modeling dense inflorescences. ACM Transactions on Graphics 35, 136.Palmer JH, Marc J. 1982. Wound-induced initiation of involucral bracts and florets in the developing sunflower inflorescence. Plant and Cell Physiology 23, 1401–1409.Pozner R, Zanotti C, Johnson LA. 2012. Evolutionary origin of the Asteraceae capitulum: insights from Calyceraceae. American Journal of Botany 99, 1–13.Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C. 2003. Regulation of phyllotaxis by polar auxin transport. Nature 426, 255–260.Smith RS, Guyomarc’h S, Mandel T, Reinhardt D, Kuhlemeier C, Prusinkiewicz P. 2006. A plausible model of phyllotaxis. Proceedings of the National Academy of Sciences, USA 103, 1301–1306.Swinton J, Ochu E; MSI Turing’s Sunflower Consortium. 2016. Novel Fibonacci and non-Fibonacci structure in the sunflower: results of a citizen science experiment. Royal Society Open Science 3, 160091.Zagórska-Marek B, Szpak M. 2008. Virtual phyllotaxis and real plant model cases. Functional Plant Biology 25, 1025–1033.Zhao Y, Zhang T, Broholm SK, Tähtiharju S, Mouhu K, Albert VA, Teeri TH, Elomaa P. 2016. Evolutionary co-option of floral meristem identity genes for patterning of the flower-like Asteraceae inflorescence. Plant Physiology 172, 284–296.

My favourite flowering image: a capitulum of Asteraceae

https://helda.helsinki.fi/bitstream/10138/214814/1/erw489.pdf

My favourite flowering image: a capitulum of Asteraceae

Abstract

Similar works

Full text

Available Versions

Helsingin yliopiston digitaalinen arkisto