- Email: [email protected]
The FLO-RE-S network for contemporary studies in flower structure and biology
Accepted Manuscript Title: The FLO-RE-S network for contemporary studies in flower structure and biology Author: Kester Bull-Here˜nu Regine Claßen-Bockhoff Louis Ronse de Craene PII: DOI: Reference:
S0367-2530(16)30015-9 http://dx.doi.org/doi:10.1016/j.flora.2016.02.005 FLORA 50935
To appear in: Received date: Accepted date:
5-2-2016 8-2-2016
Please cite this article as: Bull-Here˜nu, Kester, Classen-Bockhoff, Regine, Craene, Louis Ronse de, The FLO-RE-S network for contemporary studies in flower structure and biology.Flora http://dx.doi.org/10.1016/j.flora.2016.02.005 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
The FLO-RE-S network for contemporary studies in flower structure and biology Kester Bull-Hereñua,b,* [email protected], [email protected], Regine Claß[email protected], Louis Ronse de [email protected]
a
Departamento de Ecología, Pontificia Universidad Católica de Chile, Alameda 340, Santiago, Chile.
b
Fundación Flores, Ministro Carvajal 30, Providencia, Santiago, Chile.
c
Institut für Spezielle Botanik, Johannes Guntenberg Universität, 55099 Mainz, Germany. d Royal Botanic Garden
Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, United Kingdom. *
Corresponding author
Highlights
The FLO-RE-S network stimulates joint research on flowers.
Unraveling the causes of floral shape is central in botanical research.
Understanding floral shape can be addressed through many perspectives and methodologies.
Abstract The here presented compendium of papers on flower research is a contribution in answering the question “why are flowers what they are?” as presented by the recently created Flower Research Synectics network (FLO-RE-S). FLO-RE-S aims to bring plant scientists together to design and discuss joint research for the investigation of flower related questions. The inclusion of a diversity of perspectives and methodological approaches is crucial for the quality of the synthesis obtained. Investigations ranging from revealing the ontogeny to understanding the function of floral traits, and from experiments on floral genesis to the reconstruction of floral characters contribute to disentangling the nature and causes behind the floral shape. Keywords: Flower, Networking, Development, Morphology, Joint Research, FLO-RE-S
1
1. Introduction
Contemplating the natural diversity leads to an almost spontaneous urge to answer the question why are flowers what they are. To address this question was our main drive in setting up the Flower Research Synectics network (FLO-R-ES), to stimulate contacts and collaboration. Flowers are the evolutionary outcome of three main factors: the coevolution with pollinators, the intrinsic genetic divergence, and epigenetic influences linked with their development. These factors are intricately linked and necessitate a collaborative approach to understanding the diversity of flowers. Our purpose is to bring plant scientists together to design and discuss joint research for the investigation of flower related questions. The here presented compendium of papers is a contribution in answering this question and also forms part of the presentations at the 'Contemporary Studies in Flower Structure and Biology' symposium organized by the Flower Research Synectics network (FLO-RE-S) held in Santiago and Puerto Varas, Chile in November-December 2014. Flower related investigations have been an important area of botanical study since Linnaeus's Systema Naturae in 1735. Since that time, an enormous number of observations has contributed to the understanding of the quintessential angiosperm structure. However, the work is far from being completed, and research on and interpretations about the flower remain central to botanical investigations, adding new questions and revisiting older interpretations of structures. Improved understanding and new technologies make the study of flowers possible from different perspectives to understand their systematic diversity and functionality.
2. Topics and questions approached by FLO-RE-S 2.1 Morphogenesis of the flower Flower development is central to the understanding of the nature of flowers. Traditionally, the unravelling of how floral organs arise in the ontogeny has helped explaining the morphology of flowers, since organ arrangement in the young bud shows a clearer spatial disposition than in the mature state. Consequently this clarifies the relationships of taxa based on similar developmental patterns. The sequence of organ initiation and growth, and the interaction between organs is also responsible for diverse floral morphologies, as Dos Santos and Ronse De Craene (2016: this issue) reveal in their study on the flower of Lewisia (Montiaceae). By comparing ontogenies among different
2
Lewisia species, the authors show how the involucrum causes a delay in the growth and development of the median perianth members (petaloids) and an increase in the number of stamens and median petaloids. Also inferring causes for the shaping of floral morphologies is possible by comparison of ontogenies of different species, with the premise that a shift in the ontogeny can be the reason for the resulting diverging phenotypes. Based on thorough observations on the development of short-styled and long-styled Oxalis flowers, Bull-Hereñu et al. (2016: this issue) suggest that meristematic size plays a role in determining heterostylous morphotypes. Larger flower meristems allocate more tissue for gynoecial inception, which may ultimately result in larger gynoecia with longer styles. Similarly, Ronse de Craene (2016: this issue) demonstrates that evolutionary change in merism can also depend on the relative size proportion among different primordia. For instance, the reduction of the diameter of outer perianth organs may lead to an increase in organ number on a flower meristem of the same size. Similarily, Ajani et al. (2016: this issue) discuss the sequential vs. simultaneous and centripetal vs. divergent primordia initiation in the Apiaceae-Apioideae as a consequence of meristem size and spatial constraints. Comparisons of flower developmental evidence in a much broader context can lead to more general assertions about the identity of the flower. In her contribution, Claßen-Bockhoff (2016: this issue) challenges the shoot concept of the flower by analysing the flower meristem properties and highlighting determinism, ongoing intercalary expansion, and high differential activity as novel features compared to vegetative meristems.
2.2. Unravelling genetic and epigenetic factors that influence flower shape An experimental testing of these mechanistic inferences can help in understanding the mechanisms of the shaping of the flower itself, i.e. through controlled addition or removal of a given 'factor' during flower genesis, such as hormones, proteins, genes, or by epigenetic factors. By far the most successful approaches in experimentation nowadays are the genetic manipulations. The reason of this enormous success and focus of attention relies probably on the exquisite manipulative power that a researcher can gain for generating controlled flower phenotypes. Possible conclusions discussed in the present gene-evolutionary framework are reviewed by Jabbour et al. (2016: this issue) on the example of genetic pathways leading to different Ranunculaceae terata. On the other hand, abiotic facto+----rs may play a role in the plasticity of the phenotype, and
3
also contribute to the understanding of the flower. Dworacek and Claßen-Bockhoff (2016: this issue) investigate the effect of gravity on the torsion of flower-pairs in two Thalia species (Marantaceae), one with erect and one with hanging inflorescences.
2.3. Phenotypic integration, correlations and synorganization of the flower The flower as a mature construction is the outcome of concerted ontogenetic processes, which lead to a synorganized structure (Endress, 2015). Chinga and Pérez (2016: this issue) show how far coordinated growth of flower parts may switch off during development, giving rise to various degrees in flower integration among different Schizanthus (Solanaceae) species. Even a sole observation and diagnosis of character correlations in mature flowers among closely related species can ultimatively serve as a primary source of hypotheses that explain how flowers are constructed, as Jabbour et al. (2016: this issue) also show in their work by classifying changes that give rise to different Ranunculacean terata. The close link between carpel increase or reduction with the androecium may lead to highly divergent floral morphs, as discussed by Ronse De Craene (2016: this issue).
2.4. Reconstruction of floral character states and their evolution The identification of useful characters and their character states, including the reconstruction of character states on a well-supported phylogeny clarifies how far correlations of characters have evolved repeatedly in different groups, leading to evolutionary tendencies (Endress and Matthews, 2006; Ronse De Craene, 2010). The very common (and controversial) parallel evolution of flower phenotypes may rely on recruiting developmental programmes that are available due to a common genetic potential which is not necessarily expressed in the ancestors' phenotype (i.e. “deep homology"). Thus the mapping of ontogenetic sequences on a phylogenetic tree might be even more clarifying at this point (Hufford, 1997, 2001). The here presented works showing increase of petaloids and stamens in Lewisia (Dos Santos and Ronse De Craene, 2016: this issue) is a contributions in this direction.
2.5. Flowers as functional units Analysing the interactions among flowers and their environment, in particular the relation to pollinators, increases our knowledge on adaptation in floral traits. Changes in floral morphology are intimately linked with the exploitation of the behaviour of pollinators, and this interaction has much
4
reciprocal importance in the evolution of phenotypes. An interesting case of flower construction and pollinator behaviour is delivered by Salvia apiana (Lamiaceae), characterised by a bulged lower lip restricting access to nectar. Ott et al. (2016: this issue) analyse the floral construction linked to the pollination mechanism of this Californian species, regarding frequency and effectiveness of visits of honeybees and Xylocopa species. Stöbbe et al. (2016: this issue) test the significance of barriers in flowers for food plant selection by potential pollinators. They conduct choice experiments with artificial flowers presenting or lacking movable levers. The foraging preference of bees is also analysed in the study by Díaz-Forestier et al. (2016: this issue) on the morphological nature of nectaries in four endemic Chilean plants. El Ottra et al. (2016: this issue) address the phenotypic specialization to lepidopteran pollination in two Galipeinae species (Rutaceae) including the description of functional staminodes for the first time in this group.
3. Conclusions FLO-RE-S intends to create a medium for dialogue and cooperation towards understanding the dynamics of shape and function in flowers. Revisiting flowers requires a deepened dialogue between more traditional descriptive approaches and experimental investigations in the causes of their wonderful diversity. This effort represents a continuation of a renewed interest in flowers, starting with the symposium “Flowers — Diversity, Development, and Evolution” in Zurich in 2002 (Schönenberger et al., 2003), and continued at the Bio Syst Eu conference in Leiden in 2009 (Wanntorp and Ronse De Craene, 2011). We hope that this volume will effectively feed into a renewed discussion that places floral morphology in a central position and allows for the elaboration of above-mentioned contrasting yet complimentary viewpoints. 4. Acknowledgements This volume has been prepared based on a symposium presented both at the Pontificia Universidad Católica de Chile in Santiago and at the LVIIth annual meeting of the Sociedad Chilena de Biología de Chile in Puerto Varas. We thank the financial support given by VRI of the Pontificia Universidad Católica de Chile, Sociedad Chilena de Botánica, Sociedad de Biología de Chile and Instituto Milenio de Ecología y Biodiversidad grant to Fernanda Pérez and the Fondecyt grant 3130417. We appreciate the kind collaboration in the symposium organization given by Fundación
5
Flores, Valeria Oppliger, Diego Bustamante, Daniela Mora, Rosario, Edita, Isabel Mujica, Javiera Chinga and Maureen Murúa.
5. References Ajani, Y., Bull-Hereñu, K., Claßen-Bockhoff, R., 2016. Pattern of floral development in ApiaceaeApioideae. This issue xx-xx. Bull-Hereñu, K., Ronse de Craene, L.P., Pérez, F., 2016. Meristematic size change is responsible for heterostyly in the case of two Chilean Oxalis L. species. This issue xx-xx. Chinga, J., Pérez, F., 2016. Ontogenetic integration in two Schizanthus species (Solanaceae): linking development to morphological integration studies in flowers. This issue xx-xx. Classen-Bockhoff, R., 2016. The shoot concept of the flower: still up to date? This issue xx-xx. Díaz-Forestier, J., Gómez, M., Celis, J.L., Montenegro, G., 2016. Morphology and structure of the nectaries of four plants native to Chile. This issue xx-xx. Dos Santos P., Ronse De Craene, L.P, 2016. Floral development of Lewisia (Montiaceae): investigating patterns of perianth and stamen. diversity. This issue xx-xx. Dworaczek, E., Claßen-Bockhoff, R., 2016. False resupination in the flower-pairs of Thalia L. (Marantaceae). This issue xx-xx. Endress, P. K., Matthews, M. L., 2006. First steps towards a floral structural characterization of the major rosid subclades. Plant Syst. Evol. 260, 223–251. Endress, P., 2015. Development and evolution of extreme synorganization in angiosperm flowers and diversity: a comparison of Apocynaceae and Orchidaceae. Ann. Bot. In press. doi: 10.1093/aob/mcv119 Jabbour, F., Nadot, S., Espinosa, F., Damerval, C., 2016. Ranunculacean flower terata: records, a classification, and some clues about floral developmental genetics and evolution. This issue xxxx. Hufford, L.D., 1997. The roles of ontogenetic evolution in the origins of floral homoplasies. Int. J. Plant Sci. 158 (6 Suppl): S65-S80. Hufford, L., 2001. Ontogenetic sequences: homology, evolution, and the patterning of clade diversity. In: Zelditch. M.L. (ed) Beyond heterochrony: the evolution of development. Wiley-Liss, Inc. Leite El Ottra, J., Rubens Pirani, J., Ricardo Pansarin, E., 2016. Floral biology and pollination of two sympatric species of Galipeinae (Galipeeae, Rutaceae) endemic to the Brazilian Atlantic Forest.
6
This issue xx-xx. Ott, D., Hühn, P., Claßen-Bockhoff, R., 2016. Salvia apiana - a carpenter bee flower? This issue xx-xx. Ronse De Craene, L.P., 2010. Floral diagrams. An aid to understanding flower morphology and evolution, Cambridge University Press, Cambridge. Ronse De Craene LP - Meristic changes in flowering plants: how flowers play with numbers. This issue xx-xx. Schönenberger, J., von Balthazar, M., Matthews, M., 2013. Flowers - diversity, development and Evolution. introduction. Int. J. Pl. Sci. 164, (Suppl) S197-S199. Smith, S.D., 2015. Pleiotropy and the evolution of floral integration. New. Phyt. 209, 80–85. Stöbbe J, Jürgen Schramme, Regine Claßen-Bockhoff - Training experiments with Bombus terrestris and Apis mellifera on artificial 'Salvia' flowers. This issue xx-xx. Wanntorp, L. and Ronse De Craene, L.P. (eds.) 2011. Flowers on the tree of life. The Systematics Association Special volume 80, Cambridge University Press, Cambridge.
7
S0367-2530(16)30015-9 http://dx.doi.org/doi:10.1016/j.flora.2016.02.005 FLORA 50935
To appear in: Received date: Accepted date:
5-2-2016 8-2-2016
Please cite this article as: Bull-Here˜nu, Kester, Classen-Bockhoff, Regine, Craene, Louis Ronse de, The FLO-RE-S network for contemporary studies in flower structure and biology.Flora http://dx.doi.org/10.1016/j.flora.2016.02.005 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
The FLO-RE-S network for contemporary studies in flower structure and biology Kester Bull-Hereñua,b,* [email protected], [email protected], Regine Claß[email protected], Louis Ronse de [email protected]
a
Departamento de Ecología, Pontificia Universidad Católica de Chile, Alameda 340, Santiago, Chile.
b
Fundación Flores, Ministro Carvajal 30, Providencia, Santiago, Chile.
c
Institut für Spezielle Botanik, Johannes Guntenberg Universität, 55099 Mainz, Germany. d Royal Botanic Garden
Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, United Kingdom. *
Corresponding author
Highlights
The FLO-RE-S network stimulates joint research on flowers.
Unraveling the causes of floral shape is central in botanical research.
Understanding floral shape can be addressed through many perspectives and methodologies.
Abstract The here presented compendium of papers on flower research is a contribution in answering the question “why are flowers what they are?” as presented by the recently created Flower Research Synectics network (FLO-RE-S). FLO-RE-S aims to bring plant scientists together to design and discuss joint research for the investigation of flower related questions. The inclusion of a diversity of perspectives and methodological approaches is crucial for the quality of the synthesis obtained. Investigations ranging from revealing the ontogeny to understanding the function of floral traits, and from experiments on floral genesis to the reconstruction of floral characters contribute to disentangling the nature and causes behind the floral shape. Keywords: Flower, Networking, Development, Morphology, Joint Research, FLO-RE-S
1
1. Introduction
Contemplating the natural diversity leads to an almost spontaneous urge to answer the question why are flowers what they are. To address this question was our main drive in setting up the Flower Research Synectics network (FLO-R-ES), to stimulate contacts and collaboration. Flowers are the evolutionary outcome of three main factors: the coevolution with pollinators, the intrinsic genetic divergence, and epigenetic influences linked with their development. These factors are intricately linked and necessitate a collaborative approach to understanding the diversity of flowers. Our purpose is to bring plant scientists together to design and discuss joint research for the investigation of flower related questions. The here presented compendium of papers is a contribution in answering this question and also forms part of the presentations at the 'Contemporary Studies in Flower Structure and Biology' symposium organized by the Flower Research Synectics network (FLO-RE-S) held in Santiago and Puerto Varas, Chile in November-December 2014. Flower related investigations have been an important area of botanical study since Linnaeus's Systema Naturae in 1735. Since that time, an enormous number of observations has contributed to the understanding of the quintessential angiosperm structure. However, the work is far from being completed, and research on and interpretations about the flower remain central to botanical investigations, adding new questions and revisiting older interpretations of structures. Improved understanding and new technologies make the study of flowers possible from different perspectives to understand their systematic diversity and functionality.
2. Topics and questions approached by FLO-RE-S 2.1 Morphogenesis of the flower Flower development is central to the understanding of the nature of flowers. Traditionally, the unravelling of how floral organs arise in the ontogeny has helped explaining the morphology of flowers, since organ arrangement in the young bud shows a clearer spatial disposition than in the mature state. Consequently this clarifies the relationships of taxa based on similar developmental patterns. The sequence of organ initiation and growth, and the interaction between organs is also responsible for diverse floral morphologies, as Dos Santos and Ronse De Craene (2016: this issue) reveal in their study on the flower of Lewisia (Montiaceae). By comparing ontogenies among different
2
Lewisia species, the authors show how the involucrum causes a delay in the growth and development of the median perianth members (petaloids) and an increase in the number of stamens and median petaloids. Also inferring causes for the shaping of floral morphologies is possible by comparison of ontogenies of different species, with the premise that a shift in the ontogeny can be the reason for the resulting diverging phenotypes. Based on thorough observations on the development of short-styled and long-styled Oxalis flowers, Bull-Hereñu et al. (2016: this issue) suggest that meristematic size plays a role in determining heterostylous morphotypes. Larger flower meristems allocate more tissue for gynoecial inception, which may ultimately result in larger gynoecia with longer styles. Similarly, Ronse de Craene (2016: this issue) demonstrates that evolutionary change in merism can also depend on the relative size proportion among different primordia. For instance, the reduction of the diameter of outer perianth organs may lead to an increase in organ number on a flower meristem of the same size. Similarily, Ajani et al. (2016: this issue) discuss the sequential vs. simultaneous and centripetal vs. divergent primordia initiation in the Apiaceae-Apioideae as a consequence of meristem size and spatial constraints. Comparisons of flower developmental evidence in a much broader context can lead to more general assertions about the identity of the flower. In her contribution, Claßen-Bockhoff (2016: this issue) challenges the shoot concept of the flower by analysing the flower meristem properties and highlighting determinism, ongoing intercalary expansion, and high differential activity as novel features compared to vegetative meristems.
2.2. Unravelling genetic and epigenetic factors that influence flower shape An experimental testing of these mechanistic inferences can help in understanding the mechanisms of the shaping of the flower itself, i.e. through controlled addition or removal of a given 'factor' during flower genesis, such as hormones, proteins, genes, or by epigenetic factors. By far the most successful approaches in experimentation nowadays are the genetic manipulations. The reason of this enormous success and focus of attention relies probably on the exquisite manipulative power that a researcher can gain for generating controlled flower phenotypes. Possible conclusions discussed in the present gene-evolutionary framework are reviewed by Jabbour et al. (2016: this issue) on the example of genetic pathways leading to different Ranunculaceae terata. On the other hand, abiotic facto+----rs may play a role in the plasticity of the phenotype, and
3
also contribute to the understanding of the flower. Dworacek and Claßen-Bockhoff (2016: this issue) investigate the effect of gravity on the torsion of flower-pairs in two Thalia species (Marantaceae), one with erect and one with hanging inflorescences.
2.3. Phenotypic integration, correlations and synorganization of the flower The flower as a mature construction is the outcome of concerted ontogenetic processes, which lead to a synorganized structure (Endress, 2015). Chinga and Pérez (2016: this issue) show how far coordinated growth of flower parts may switch off during development, giving rise to various degrees in flower integration among different Schizanthus (Solanaceae) species. Even a sole observation and diagnosis of character correlations in mature flowers among closely related species can ultimatively serve as a primary source of hypotheses that explain how flowers are constructed, as Jabbour et al. (2016: this issue) also show in their work by classifying changes that give rise to different Ranunculacean terata. The close link between carpel increase or reduction with the androecium may lead to highly divergent floral morphs, as discussed by Ronse De Craene (2016: this issue).
2.4. Reconstruction of floral character states and their evolution The identification of useful characters and their character states, including the reconstruction of character states on a well-supported phylogeny clarifies how far correlations of characters have evolved repeatedly in different groups, leading to evolutionary tendencies (Endress and Matthews, 2006; Ronse De Craene, 2010). The very common (and controversial) parallel evolution of flower phenotypes may rely on recruiting developmental programmes that are available due to a common genetic potential which is not necessarily expressed in the ancestors' phenotype (i.e. “deep homology"). Thus the mapping of ontogenetic sequences on a phylogenetic tree might be even more clarifying at this point (Hufford, 1997, 2001). The here presented works showing increase of petaloids and stamens in Lewisia (Dos Santos and Ronse De Craene, 2016: this issue) is a contributions in this direction.
2.5. Flowers as functional units Analysing the interactions among flowers and their environment, in particular the relation to pollinators, increases our knowledge on adaptation in floral traits. Changes in floral morphology are intimately linked with the exploitation of the behaviour of pollinators, and this interaction has much
4
reciprocal importance in the evolution of phenotypes. An interesting case of flower construction and pollinator behaviour is delivered by Salvia apiana (Lamiaceae), characterised by a bulged lower lip restricting access to nectar. Ott et al. (2016: this issue) analyse the floral construction linked to the pollination mechanism of this Californian species, regarding frequency and effectiveness of visits of honeybees and Xylocopa species. Stöbbe et al. (2016: this issue) test the significance of barriers in flowers for food plant selection by potential pollinators. They conduct choice experiments with artificial flowers presenting or lacking movable levers. The foraging preference of bees is also analysed in the study by Díaz-Forestier et al. (2016: this issue) on the morphological nature of nectaries in four endemic Chilean plants. El Ottra et al. (2016: this issue) address the phenotypic specialization to lepidopteran pollination in two Galipeinae species (Rutaceae) including the description of functional staminodes for the first time in this group.
3. Conclusions FLO-RE-S intends to create a medium for dialogue and cooperation towards understanding the dynamics of shape and function in flowers. Revisiting flowers requires a deepened dialogue between more traditional descriptive approaches and experimental investigations in the causes of their wonderful diversity. This effort represents a continuation of a renewed interest in flowers, starting with the symposium “Flowers — Diversity, Development, and Evolution” in Zurich in 2002 (Schönenberger et al., 2003), and continued at the Bio Syst Eu conference in Leiden in 2009 (Wanntorp and Ronse De Craene, 2011). We hope that this volume will effectively feed into a renewed discussion that places floral morphology in a central position and allows for the elaboration of above-mentioned contrasting yet complimentary viewpoints. 4. Acknowledgements This volume has been prepared based on a symposium presented both at the Pontificia Universidad Católica de Chile in Santiago and at the LVIIth annual meeting of the Sociedad Chilena de Biología de Chile in Puerto Varas. We thank the financial support given by VRI of the Pontificia Universidad Católica de Chile, Sociedad Chilena de Botánica, Sociedad de Biología de Chile and Instituto Milenio de Ecología y Biodiversidad grant to Fernanda Pérez and the Fondecyt grant 3130417. We appreciate the kind collaboration in the symposium organization given by Fundación
5
Flores, Valeria Oppliger, Diego Bustamante, Daniela Mora, Rosario, Edita, Isabel Mujica, Javiera Chinga and Maureen Murúa.
5. References Ajani, Y., Bull-Hereñu, K., Claßen-Bockhoff, R., 2016. Pattern of floral development in ApiaceaeApioideae. This issue xx-xx. Bull-Hereñu, K., Ronse de Craene, L.P., Pérez, F., 2016. Meristematic size change is responsible for heterostyly in the case of two Chilean Oxalis L. species. This issue xx-xx. Chinga, J., Pérez, F., 2016. Ontogenetic integration in two Schizanthus species (Solanaceae): linking development to morphological integration studies in flowers. This issue xx-xx. Classen-Bockhoff, R., 2016. The shoot concept of the flower: still up to date? This issue xx-xx. Díaz-Forestier, J., Gómez, M., Celis, J.L., Montenegro, G., 2016. Morphology and structure of the nectaries of four plants native to Chile. This issue xx-xx. Dos Santos P., Ronse De Craene, L.P, 2016. Floral development of Lewisia (Montiaceae): investigating patterns of perianth and stamen. diversity. This issue xx-xx. Dworaczek, E., Claßen-Bockhoff, R., 2016. False resupination in the flower-pairs of Thalia L. (Marantaceae). This issue xx-xx. Endress, P. K., Matthews, M. L., 2006. First steps towards a floral structural characterization of the major rosid subclades. Plant Syst. Evol. 260, 223–251. Endress, P., 2015. Development and evolution of extreme synorganization in angiosperm flowers and diversity: a comparison of Apocynaceae and Orchidaceae. Ann. Bot. In press. doi: 10.1093/aob/mcv119 Jabbour, F., Nadot, S., Espinosa, F., Damerval, C., 2016. Ranunculacean flower terata: records, a classification, and some clues about floral developmental genetics and evolution. This issue xxxx. Hufford, L.D., 1997. The roles of ontogenetic evolution in the origins of floral homoplasies. Int. J. Plant Sci. 158 (6 Suppl): S65-S80. Hufford, L., 2001. Ontogenetic sequences: homology, evolution, and the patterning of clade diversity. In: Zelditch. M.L. (ed) Beyond heterochrony: the evolution of development. Wiley-Liss, Inc. Leite El Ottra, J., Rubens Pirani, J., Ricardo Pansarin, E., 2016. Floral biology and pollination of two sympatric species of Galipeinae (Galipeeae, Rutaceae) endemic to the Brazilian Atlantic Forest.
6
This issue xx-xx. Ott, D., Hühn, P., Claßen-Bockhoff, R., 2016. Salvia apiana - a carpenter bee flower? This issue xx-xx. Ronse De Craene, L.P., 2010. Floral diagrams. An aid to understanding flower morphology and evolution, Cambridge University Press, Cambridge. Ronse De Craene LP - Meristic changes in flowering plants: how flowers play with numbers. This issue xx-xx. Schönenberger, J., von Balthazar, M., Matthews, M., 2013. Flowers - diversity, development and Evolution. introduction. Int. J. Pl. Sci. 164, (Suppl) S197-S199. Smith, S.D., 2015. Pleiotropy and the evolution of floral integration. New. Phyt. 209, 80–85. Stöbbe J, Jürgen Schramme, Regine Claßen-Bockhoff - Training experiments with Bombus terrestris and Apis mellifera on artificial 'Salvia' flowers. This issue xx-xx. Wanntorp, L. and Ronse De Craene, L.P. (eds.) 2011. Flowers on the tree of life. The Systematics Association Special volume 80, Cambridge University Press, Cambridge.
7