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My favourite flowering image: a capitulum of Asteraceae

My favourite flowering image: a capitulum of Asteraceae Downloaded from https://academic.oup.com/jxb/article/70/21/e6496/2964617 by DeepDyve user on 13 July 2022 Journal of Experimental Botany, Vol. 70, No. 21 pp. e6496–e6498, 2019 doi:10.1093/jxb/erw489 Advance Access publication 30 January 2017 This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details) COMMENTARY Paula Elomaa Department of Agricultural Sciences, Viikki Plant Science Centre, PO Box 27, 00014 University of Helsinki, Finland paula.elomaa@helsinki.fi Editor: Lars Hennig, Swedish University of Agricultural Sciences  I could have selected my favourite flowering image from preceding numbers in the series). In the particular cultivar in thousands of astonishing images that have captured my favourite image, there are 34 clockwise and 21 anti-clock- the geometric regularity of head-like inflorescences wise spirals (you may check this!) while our standard model in Asteraceae. These unique inflorescences pack hun- cultivar, Terra Regina, typically shows 55 and 34 spirals, dreds of flowers into precise spirals whose numbers respectively. Interestingly, although the Fibonacci numbers follow a famous mathematical rule. Meanwhile, the clearly dominate, non-Fibonacci structures such as double whole structure may mislead a layman (or a pollinator) Fibonacci numbers (2, 4, 6, 10, 16, 26…), Fibonacci ±1 or by mimicking a single solitary flower although it con- Lucas numbers (1, 3, 4, 7, 11, 18…) do appear, as recently sists of morphologically and functionally distinct types demonstrated in a large citizen science experiment engag- of flowers. ing the public to grow and count sunflower spirals (Swinton et  al., 2016). It seems that there are always exceptions to Regular, reproducible patterns in nature are fascinating and the rule; the experiment revealed cases where spirals were 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 o fl wer 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 o fl wering 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 Fig. 1. A composite inflorescence of Gerbera hybrida showing spiral (parastichies). Intriguingly, the number of these spirals fol- phyllotaxis of emerging flowers. Hundreds of flowers are packed into low two consecutive numbers of Fibonacci series (1, 1, 2, 3, the capitulum that mimics a solitary flower and is surrounded by green, involucral bracts. 5, 8, 13, 21, 34 … where each number is the sum of the two © The Author 2017. Published by Oxford University Press on behalf of the Society for Experimental Biology. 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. Downloaded from https://academic.oup.com/jxb/article/70/21/e6496/2964617 by DeepDyve user on 13 July 2022 My favourite flowering image | e6497 countable but not Fibonacci, as well as well-defined paras- across the naked inflorescence meristem, defining it as a tichies in only one direction or even uncountable structures. determinate structure. Loss of GhLFY expression led to In a shoot apex, the spiral emergence of leaf primordia fol- loss of determinacy of the capitulum and disrupted phyl- lows an approximate golden angle (137.5°), and their posi- lotaxis. In contrast, by ectopic expression of GhUFO, this tioning in the fist available space between already existing large structure gained floral fate; instead of flower primor - primordia is associated with formation of auxin maxima at dia, the meristem initiated numerous flower organ primor - incipient primordia and on subsequent depletion of auxin dia arranged in whorled phyllotaxis (Zhao et al., 2016). in their vicinity (Reinhardt et al., 2003; Heisler et al., 2005). Our studies also provided the first molecular evidence to However, it is still unclear what are the developmental mech- explain the evolutionary origin of flower types. Several anisms that regulate the organization of the expanded capit- botanical studies have indicated that although ray flowers ulum that is much larger in its dimensions, and how they are located along the Fibonacci spirals, they show delayed are linked to observed deviations of the Fibonacci struc- development compared with adjacent disc (or trans) flow- ture. Mathematical modelling can reproduce many of these ers (Harris, 1995; Bello et al., 2013). In an extreme case, remarkable patterns (e.g. Douady and Couder, 1996; Smith ray flowers initiate after the disc flowers and their devel- et al., 2006; Zagórska-Marek and Szpak, 2008; Owens et al., opment proceeds in a different direction, namely towards 2016), and have already provided inspiring hypotheses to be the margins of the head (Harris et al., 1991). We showed tested at the molecular level. that GhLFY has evolved a novel function in regulating the The visual attractiveness of composite inflorescences is early ontogeny of ray o fl wers in gerbera (Zhao et al., 2016). further enhanced by the presence of distinct flower types. Silencing of GhLFY converted ray o fl wers into branched Normally, gerbera (like sunflower) has showy, large and structures resembling those found in Calyceraceae, the bilaterally symmetrical marginal ray flowers, and smaller, phylogenetically closest relatives of Asteraceae (Pozner et more radially symmetrical central disc flowers. The image al., 2012). Our data thus indicated that, during evolution, I selected is taken from a cultivar that only develops male GhLFY has played a major role in contributing to the gain sterile ray-like flowers (so-called crested phenotype; Kloos of floral fate for these peripheral branches still found in et al. 2004; Broholm et al., 2014 ; Juntheikki-Palovaara et capitula of Calyceraceae, and that the differential devel- al., 2014). The image represents an early developmental opment of ray flowers relates to their different ontogenic stage of the inflorescence and, therefore, the showy petals origin from separate branching systems. have not yet reached their full size. The famous painting Although some details on the gene functions and molecu- by Vincent van Gogh with double-flowered sunflower heads lar networks controlling capitulum architecture and flower has preserved a similar mutant phenotype in the history type differentiation have been revealed, the future chal- of art (Chapman et al., 2012). The molecular studies in lenge is to understand the dynamics of early patterning of gerbera (Broholm et al., 2008), Senecio (Kim et al., 2008), the inflorescence meristem and establishment of the spi- as well as sunflower (Chapman et al., 2012) all indicated ral phyllotaxis. Classical experiments in sunflower already that CYCLOIDEA-like TCP domain transcription fac- showed that patterning can be disrupted by wounding tors, among the key developmental regulators in plants, (Palmer and Marc, 1982; Hernandez and Palmer, 1988, have been recruited to regulate capitulum architecture. This 1990). Interestingly, wounding creates a new margin that gene family has expanded in Asteraceae and consequently resets patterning and initiates successive formation of new evolved novel functions in regulating ray identity. In the bracts, rays, and discs, in this particular order. This raises a crested gerbera as well as in double-flowered sunflower, still unresolved fundamental question; how does the margin up-regulation of a CYC-like TCP gene converted the disc specify initiation of organ/flower primordia and what is the o fl wers into ray-like flowers by affecting the growth of the nature of the signal that it creates? Furthermore, an extra petals, and disrupting stamen development (Chapman et level of complexity in species developing capitula within al., 2012; Juntheikki-Palovaara et al., 2014). capitula (syncephalium) surely adds to the number of vari- The Asteraceae inflorescences are false flowers (pseudan- ations on a theme. thia) that mimic solitary flowers. As visible from the image, the capitulum is surrounded by involucral bracts (the Acknowledgements bright green leaf-like organs) that perform a sepal-like, protective function. The showy ray flowers can be seen to My special thanks go to Dr Sari Tähtiharju for the inspiring image of Gerbera hybrida. I  am especially grateful to my colleague Professor Teemu be analogous to attractive petals in solitary flowers, and Teeri for his continuous support and contribution to gerbera research. We the hermaphrodite disc flowers to reproductive organs have worked on the gerbera model for more than 25 years starting from a sin- (carpels/stamens). By conducting functional analyses gle promoter, but hopefully seeing the genome soon. I also want to acknowl- edge Professor Victor Albert for fruitful collaboration and for guiding us for the gerbera orthologues of flower meristem identity (molecular biologists) to the world of evo-devo! During the years, many col- genes LEAFY (LFY) and UNUSUAL FLORAL ORGANS leagues and friends have devoted their enthusiasm, valuable ideas, and con- (UFO), we recently discovered that the capitulum resem- tribution to this research. Thank you all. bles a solitary flower also at the molecular level (Zhao et al., 2016). As in single flower meristems in Arabidopsis, Key words: Asteraceae, capitulum, gerbera, inflorescence, the gerbera GhLFY expression was found to be uniform phyllotaxis, sunflower. Downloaded from https://academic.oup.com/jxb/article/70/21/e6496/2964617 by DeepDyve user on 13 July 2022 e6498 | Elomaa Juntheikki-Palovaara I, Tähtiharju S, Lan T, Broholm SK, Rijpkema References AS, Ruonala R, Kale L, Albert VA, Teeri TH, Elomaa P. 2014. Bello MA, Álvarez I, Torices R, Fuertes-Aguilar J. 2013. Floral Functional diversification of duplicated CYC2 clade genes in regulation development and evolution of capitulum structure in Anacyclus of inflorescence development in Gerbera hybrida (Asteraceae). The Plant (Anthemideae, Asteraceae). Annals of Botany 112, 1597–1612. Journal 79, 783–796. Broholm SK, Tähtiharju S, Laitinen RAE, Albert VA, Teeri TH, Elomaa Kim M, Cui ML, Cubas P, Gillies A, Lee K, Chapman MA, Abbott P. 2008. A TCP domain transcription factor controls flower type specification RJ, Coen E. 2008. Regulatory genes control a key morphological and along the radial axis of the Gerbera (Asteraceae) inflorescence. Proceedings ecological trait transferred between species. Science 322, 1116–1119. of the National Academy of Sciences, USA 105, 9117–9122. Kloos WE, George CG, Sorge LK. 2004. Inheritance of flower types of Broholm SK, Teeri TH, Elomaa P. 2014. Molecular control of Gerbera hybrida. Journal of the American Society for Horticultural Science inflorescence development in Asteraceae. In: Jacquot J-P, Gadal P, 129, 802–810. Fornara F eds. The molecular genetics of floral transition and flower Owens A, Cieslak M, Hart J, Classen-Bockhoff R, Prusinkiewicz P. development. Advances in Botanical Research, Vol. 72. Amsterdam: 2016. Modeling dense inflorescences. ACM Transactions on Graphics 35, Elsevier, 297–334. Chapman MA, Tang S, Draeger D, Nambeesan S, Shaffer H, Barb Palmer JH, Marc J. 1982. Wound-induced initiation of involucral bracts JG, Knapp SJ, Burke JM. 2012. Genetic analysis of floral symmetry in and florets in the developing sunflower inflorescence. Plant and Cell Van Gogh’s sunflowers reveals independent recruitment of CYCLOIDEA Physiology 23, 1401–1409. genes in the Asteraceae. PLoS Genetics 8, e1002628. Pozner R, Zanotti C, Johnson LA. 2012. Evolutionary origin of the Douady S, Couder Y. 1996. Phyllotaxis as a dynamical self organizing Asteraceae capitulum: insights from Calyceraceae. American Journal of process part I: the spiral modes resulting from time-periodic iterations. Botany 99, 1–13. Journal of Theoretical Biology 178, 255–274. Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Harris EM. 1995. Inflorescence and floral ontogeny in Asteraceae: a Bennett M, Traas J, Friml J, Kuhlemeier C. 2003. Regulation of synthesis of historical and current concepts. Botanical Review 61, 93–278. phyllotaxis by polar auxin transport. Nature 426, 255–260. Harris EM, Tucker SC, Urbatsch LE. 1991. Floral initiation and early development in Erigeron philadelphicus (Asteraceae). American Journal of Smith RS, Guyomarc’h S, Mandel T, Reinhardt D, Kuhlemeier C, Botany 78, 108–121. Prusinkiewicz P. 2006. A plausible model of phyllotaxis. Proceedings of the National Academy of Sciences, USA 103, 1301–1306. Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM. 2005. Patterns of auxin transport and gene expression Swinton J, Ochu E; MSI Turing’s Sunflower Consortium. 2016. Novel during primordium development revealed by live imaging of the Fibonacci and non-Fibonacci structure in the sunflower: results of a citizen Arabidopsis inflorescence meristem. Current Biology 15, 1899–1911. science experiment. Royal Society Open Science 3, 160091. Hernandez LF, Palmer JH. 1988. Regeneration of the sunflower Zagórska-Marek B, Szpak M. 2008. Virtual phyllotaxis and real plant capitulum after cylindrical wounding of the receptacle. American Journal of model cases. Functional Plant Biology 25, 1025–1033. Botany 75, 1253–1261. Zhao Y, Zhang T, Broholm SK, Tähtiharju S, Mouhu K, Albert VA, Hernandez LF, Palmer JH. 1990. Colchicine-induced displacement Teeri TH, Elomaa P. 2016. Evolutionary co-option of floral meristem of floral organ regeneration sites in the wounded sunflower capitulum. identity genes for patterning of the flower-like Asteraceae inflorescence. Microscopía Electrónica y Biología Celular 14, 159–164. Plant Physiology 172, 284–296. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Experimental Botany Oxford University Press

My favourite flowering image: a capitulum of Asteraceae

Journal of Experimental Botany , Volume 70 (21) – Nov 18, 2019

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Oxford University Press
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Copyright © 2022 Society for Experimental Biology
ISSN
0022-0957
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1460-2431
DOI
10.1093/jxb/erw489
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Abstract

Downloaded from https://academic.oup.com/jxb/article/70/21/e6496/2964617 by DeepDyve user on 13 July 2022 Journal of Experimental Botany, Vol. 70, No. 21 pp. e6496–e6498, 2019 doi:10.1093/jxb/erw489 Advance Access publication 30 January 2017 This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details) COMMENTARY Paula Elomaa Department of Agricultural Sciences, Viikki Plant Science Centre, PO Box 27, 00014 University of Helsinki, Finland paula.elomaa@helsinki.fi Editor: Lars Hennig, Swedish University of Agricultural Sciences  I could have selected my favourite flowering image from preceding numbers in the series). In the particular cultivar in thousands of astonishing images that have captured my favourite image, there are 34 clockwise and 21 anti-clock- the geometric regularity of head-like inflorescences wise spirals (you may check this!) while our standard model in Asteraceae. These unique inflorescences pack hun- cultivar, Terra Regina, typically shows 55 and 34 spirals, dreds of flowers into precise spirals whose numbers respectively. Interestingly, although the Fibonacci numbers follow a famous mathematical rule. Meanwhile, the clearly dominate, non-Fibonacci structures such as double whole structure may mislead a layman (or a pollinator) Fibonacci numbers (2, 4, 6, 10, 16, 26…), Fibonacci ±1 or by mimicking a single solitary flower although it con- Lucas numbers (1, 3, 4, 7, 11, 18…) do appear, as recently sists of morphologically and functionally distinct types demonstrated in a large citizen science experiment engag- of flowers. ing the public to grow and count sunflower spirals (Swinton et  al., 2016). It seems that there are always exceptions to Regular, reproducible patterns in nature are fascinating and the rule; the experiment revealed cases where spirals were 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 o fl wer 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 o fl wering 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 Fig. 1. A composite inflorescence of Gerbera hybrida showing spiral (parastichies). Intriguingly, the number of these spirals fol- phyllotaxis of emerging flowers. Hundreds of flowers are packed into low two consecutive numbers of Fibonacci series (1, 1, 2, 3, the capitulum that mimics a solitary flower and is surrounded by green, involucral bracts. 5, 8, 13, 21, 34 … where each number is the sum of the two © The Author 2017. Published by Oxford University Press on behalf of the Society for Experimental Biology. 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. Downloaded from https://academic.oup.com/jxb/article/70/21/e6496/2964617 by DeepDyve user on 13 July 2022 My favourite flowering image | e6497 countable but not Fibonacci, as well as well-defined paras- across the naked inflorescence meristem, defining it as a tichies in only one direction or even uncountable structures. determinate structure. Loss of GhLFY expression led to In a shoot apex, the spiral emergence of leaf primordia fol- loss of determinacy of the capitulum and disrupted phyl- lows an approximate golden angle (137.5°), and their posi- lotaxis. In contrast, by ectopic expression of GhUFO, this tioning in the fist available space between already existing large structure gained floral fate; instead of flower primor - primordia is associated with formation of auxin maxima at dia, the meristem initiated numerous flower organ primor - incipient primordia and on subsequent depletion of auxin dia arranged in whorled phyllotaxis (Zhao et al., 2016). in their vicinity (Reinhardt et al., 2003; Heisler et al., 2005). Our studies also provided the first molecular evidence to However, it is still unclear what are the developmental mech- explain the evolutionary origin of flower types. Several anisms that regulate the organization of the expanded capit- botanical studies have indicated that although ray flowers ulum that is much larger in its dimensions, and how they are located along the Fibonacci spirals, they show delayed are linked to observed deviations of the Fibonacci struc- development compared with adjacent disc (or trans) flow- ture. Mathematical modelling can reproduce many of these ers (Harris, 1995; Bello et al., 2013). In an extreme case, remarkable patterns (e.g. Douady and Couder, 1996; Smith ray flowers initiate after the disc flowers and their devel- et al., 2006; Zagórska-Marek and Szpak, 2008; Owens et al., opment proceeds in a different direction, namely towards 2016), and have already provided inspiring hypotheses to be the margins of the head (Harris et al., 1991). We showed tested at the molecular level. that GhLFY has evolved a novel function in regulating the The visual attractiveness of composite inflorescences is early ontogeny of ray o fl wers in gerbera (Zhao et al., 2016). further enhanced by the presence of distinct flower types. Silencing of GhLFY converted ray o fl wers into branched Normally, gerbera (like sunflower) has showy, large and structures resembling those found in Calyceraceae, the bilaterally symmetrical marginal ray flowers, and smaller, phylogenetically closest relatives of Asteraceae (Pozner et more radially symmetrical central disc flowers. The image al., 2012). Our data thus indicated that, during evolution, I selected is taken from a cultivar that only develops male GhLFY has played a major role in contributing to the gain sterile ray-like flowers (so-called crested phenotype; Kloos of floral fate for these peripheral branches still found in et al. 2004; Broholm et al., 2014 ; Juntheikki-Palovaara et capitula of Calyceraceae, and that the differential devel- al., 2014). The image represents an early developmental opment of ray flowers relates to their different ontogenic stage of the inflorescence and, therefore, the showy petals origin from separate branching systems. have not yet reached their full size. The famous painting Although some details on the gene functions and molecu- by Vincent van Gogh with double-flowered sunflower heads lar networks controlling capitulum architecture and flower has preserved a similar mutant phenotype in the history type differentiation have been revealed, the future chal- of art (Chapman et al., 2012). The molecular studies in lenge is to understand the dynamics of early patterning of gerbera (Broholm et al., 2008), Senecio (Kim et al., 2008), the inflorescence meristem and establishment of the spi- as well as sunflower (Chapman et al., 2012) all indicated ral phyllotaxis. Classical experiments in sunflower already that CYCLOIDEA-like TCP domain transcription fac- showed that patterning can be disrupted by wounding tors, among the key developmental regulators in plants, (Palmer and Marc, 1982; Hernandez and Palmer, 1988, have been recruited to regulate capitulum architecture. This 1990). Interestingly, wounding creates a new margin that gene family has expanded in Asteraceae and consequently resets patterning and initiates successive formation of new evolved novel functions in regulating ray identity. In the bracts, rays, and discs, in this particular order. This raises a crested gerbera as well as in double-flowered sunflower, still unresolved fundamental question; how does the margin up-regulation of a CYC-like TCP gene converted the disc specify initiation of organ/flower primordia and what is the o fl wers into ray-like flowers by affecting the growth of the nature of the signal that it creates? Furthermore, an extra petals, and disrupting stamen development (Chapman et level of complexity in species developing capitula within al., 2012; Juntheikki-Palovaara et al., 2014). capitula (syncephalium) surely adds to the number of vari- The Asteraceae inflorescences are false flowers (pseudan- ations on a theme. thia) that mimic solitary flowers. As visible from the image, the capitulum is surrounded by involucral bracts (the Acknowledgements bright green leaf-like organs) that perform a sepal-like, protective function. The showy ray flowers can be seen to My special thanks go to Dr Sari Tähtiharju for the inspiring image of Gerbera hybrida. I  am especially grateful to my colleague Professor Teemu be analogous to attractive petals in solitary flowers, and Teeri for his continuous support and contribution to gerbera research. We the hermaphrodite disc flowers to reproductive organs have worked on the gerbera model for more than 25 years starting from a sin- (carpels/stamens). By conducting functional analyses gle promoter, but hopefully seeing the genome soon. I also want to acknowl- edge Professor Victor Albert for fruitful collaboration and for guiding us for the gerbera orthologues of flower meristem identity (molecular biologists) to the world of evo-devo! During the years, many col- genes LEAFY (LFY) and UNUSUAL FLORAL ORGANS leagues and friends have devoted their enthusiasm, valuable ideas, and con- (UFO), we recently discovered that the capitulum resem- tribution to this research. Thank you all. bles a solitary flower also at the molecular level (Zhao et al., 2016). As in single flower meristems in Arabidopsis, Key words: Asteraceae, capitulum, gerbera, inflorescence, the gerbera GhLFY expression was found to be uniform phyllotaxis, sunflower. Downloaded from https://academic.oup.com/jxb/article/70/21/e6496/2964617 by DeepDyve user on 13 July 2022 e6498 | Elomaa Juntheikki-Palovaara I, Tähtiharju S, Lan T, Broholm SK, Rijpkema References AS, Ruonala R, Kale L, Albert VA, Teeri TH, Elomaa P. 2014. Bello MA, Álvarez I, Torices R, Fuertes-Aguilar J. 2013. Floral Functional diversification of duplicated CYC2 clade genes in regulation development and evolution of capitulum structure in Anacyclus of inflorescence development in Gerbera hybrida (Asteraceae). The Plant (Anthemideae, Asteraceae). Annals of Botany 112, 1597–1612. Journal 79, 783–796. Broholm SK, Tähtiharju S, Laitinen RAE, Albert VA, Teeri TH, Elomaa Kim M, Cui ML, Cubas P, Gillies A, Lee K, Chapman MA, Abbott P. 2008. A TCP domain transcription factor controls flower type specification RJ, Coen E. 2008. Regulatory genes control a key morphological and along the radial axis of the Gerbera (Asteraceae) inflorescence. Proceedings ecological trait transferred between species. Science 322, 1116–1119. of the National Academy of Sciences, USA 105, 9117–9122. Kloos WE, George CG, Sorge LK. 2004. Inheritance of flower types of Broholm SK, Teeri TH, Elomaa P. 2014. Molecular control of Gerbera hybrida. Journal of the American Society for Horticultural Science inflorescence development in Asteraceae. In: Jacquot J-P, Gadal P, 129, 802–810. Fornara F eds. The molecular genetics of floral transition and flower Owens A, Cieslak M, Hart J, Classen-Bockhoff R, Prusinkiewicz P. development. Advances in Botanical Research, Vol. 72. Amsterdam: 2016. Modeling dense inflorescences. ACM Transactions on Graphics 35, Elsevier, 297–334. Chapman MA, Tang S, Draeger D, Nambeesan S, Shaffer H, Barb Palmer JH, Marc J. 1982. Wound-induced initiation of involucral bracts JG, Knapp SJ, Burke JM. 2012. Genetic analysis of floral symmetry in and florets in the developing sunflower inflorescence. Plant and Cell Van Gogh’s sunflowers reveals independent recruitment of CYCLOIDEA Physiology 23, 1401–1409. genes in the Asteraceae. PLoS Genetics 8, e1002628. Pozner R, Zanotti C, Johnson LA. 2012. Evolutionary origin of the Douady S, Couder Y. 1996. Phyllotaxis as a dynamical self organizing Asteraceae capitulum: insights from Calyceraceae. American Journal of process part I: the spiral modes resulting from time-periodic iterations. Botany 99, 1–13. Journal of Theoretical Biology 178, 255–274. Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Harris EM. 1995. Inflorescence and floral ontogeny in Asteraceae: a Bennett M, Traas J, Friml J, Kuhlemeier C. 2003. Regulation of synthesis of historical and current concepts. Botanical Review 61, 93–278. phyllotaxis by polar auxin transport. Nature 426, 255–260. Harris EM, Tucker SC, Urbatsch LE. 1991. Floral initiation and early development in Erigeron philadelphicus (Asteraceae). American Journal of Smith RS, Guyomarc’h S, Mandel T, Reinhardt D, Kuhlemeier C, Botany 78, 108–121. Prusinkiewicz P. 2006. A plausible model of phyllotaxis. Proceedings of the National Academy of Sciences, USA 103, 1301–1306. Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM. 2005. Patterns of auxin transport and gene expression Swinton J, Ochu E; MSI Turing’s Sunflower Consortium. 2016. Novel during primordium development revealed by live imaging of the Fibonacci and non-Fibonacci structure in the sunflower: results of a citizen Arabidopsis inflorescence meristem. Current Biology 15, 1899–1911. science experiment. Royal Society Open Science 3, 160091. Hernandez LF, Palmer JH. 1988. Regeneration of the sunflower Zagórska-Marek B, Szpak M. 2008. Virtual phyllotaxis and real plant capitulum after cylindrical wounding of the receptacle. American Journal of model cases. Functional Plant Biology 25, 1025–1033. Botany 75, 1253–1261. Zhao Y, Zhang T, Broholm SK, Tähtiharju S, Mouhu K, Albert VA, Hernandez LF, Palmer JH. 1990. Colchicine-induced displacement Teeri TH, Elomaa P. 2016. Evolutionary co-option of floral meristem of floral organ regeneration sites in the wounded sunflower capitulum. identity genes for patterning of the flower-like Asteraceae inflorescence. Microscopía Electrónica y Biología Celular 14, 159–164. Plant Physiology 172, 284–296.

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Journal of Experimental BotanyOxford University Press

Published: Nov 18, 2019

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