Sugar regulates flowering

Posted on April 29, 2013 by

Soraya Pelaz
Institució Catalana de Recerca i Estudis Avançats (ICREA) and Centre for Research in Agricultural Genomics (CRAG), 08193 Barcelona, Spain. soraya.pelaz@cragenomica.es

It has been said for a long time and repeated as a mantra that plants do not flower even under inductive conditions until they get enough reserves for flowering. Such statement has finally been supported with experimental data. Wahl et al. (2013) have shown how the trehalose-6-phosphate (T6P) pathway controls flowering by regulating the levels of FLOWERING LOCUS T (FT), a known florigen that responds to inductive day-length conditions, and by interacting with the recently described age pathway, regulating the levels of the microRNA156 (miR156). Flowering is controlled by many different genetic pathways that respond to the environment such as light or temperature, and to endogenous conditions like hormone levels or age (Fornara et al. 2010; Wellmer et al. 2010). Now a metabolic pathway has been added to these known genetic pathways. T6P has been proposed to relay information about carbohydrate availability acting as a central hub in carbon signalling (Lunn et al. 2006). Accordingly, null alleles of TREHALOSE PHOSPHATE SYNTHASE 1 (TPS1), encoding the enzyme that catalyzes the formation of T6P, cause embryo lethality (Eastmond et al. 2002). Low expression of TPS1 results in T6P reduction and in a late-flowering phenotype, whereas activation of TPS1 in the shoot apical meristem (SAM) promotes extremely early flowering.

Flowering is induced through the activation of a few genes called floral pathway integrators where all genetic pathways converge; among them FT and SOC1 play central roles (Fornara et al. 2010; Wellmer et al. 2010). Environmental conditions are sensed in the leaves and some mobile signals such as the FT protein or the hormones gibberellins move to the SAM, where flowers are produced, to induce flowering (Bernier 1988; Fornara et al. 2010; Wellmer et al. 2010). Wahl and collaborators (2013) have shown that most of the late flowering phenotype of plants with reduced levels of TPS1 was due to low FT levels, as constitutive expression of FT almost completely suppressed the late flowering of TPS1-downregulated plants. The fact that plants with reduced levels of T6P also flowered late under non inductive day-length conditions prompted the researchers to study other affected pathways. The age pathway has been proposed to function directly at the SAM and to repress precocious flowering. miR156 targets a set of SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes, which promote flowering through the activation of the floral pathway integrators. The miR156 is highly expressed early in development and decays as the plant ages, allowing the activation of floral inducers (Yamaguchi et al. 2009; Wang et al. 2009; Wu et al. 2009). This ensures flowering in the event of non inductive environmental conditions. It is still unknown what regulates miR156 expression, but Wahl and collaborators (2013) show that T6P somehow controls miR156 levels as reduction on the biosynthetic T6P enzyme results in an early increase of miR156 levels, although these still gradually declined along development.

Taken together, T6P signalling acts both in leaves and in the SAM and integrates environmental (day length) and physiological (carbohydrate levels) signals together with the age pathway to promote flowering.

References

Bernier G. 1988. The control of floral evocation and morphogenesis. Annual Review of Plant Physiology and Plant Molecular Biology 39:177-219.

Eastmond PJ, Van Dijken AJH, Spielman M, Kerr A, Tissier AF, Dickinson HG, Jones JDG, Smeekens SC and Graham IA. 2002. Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. The Plant Journal 29: 225-235.

Fornara F, de Montaigu A. and Coupland G. 2010. SnapShot: Control of flowering in Arabidopsis. Cell 141, 550: 550 e1-2.

Lunn JE, Feil R, Hendriks JHM, Gibon Y, Morcuende R, Osuna D, Scheible W-R, Carillo P, Hajirezaei M-R and Stitt M. 2006. Sugar-induced increases in trehalose 6-phosphate are correlated with redox activation of ADPglucose pyrophosphorylase and higher rates of Storch synthesis in Arabidopsis thaliana. Biochem J. 397: 139-148

Wahl V, Ponnu J, Schlereth A, Arrivault S, Langenecker T, Franke A, Feil R, Lunn JE, Stitt M and Schmid M. 2013. Regulation of flowering by trehalose-6-phospate signaling in Arabidopsis thaliana. Science 339: 704-707.

Wang J-W, Czech B and Weigel D. 2009. miR156-Regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138(4): 738-749.

Wellmer F and Riechmann JL. 2010. Gene networks controlling the initiation of flower development. Trends in Genetics 26: 519-27.

Wu G, Park MY, Conway SR, Wang J-W, Weigel D and Poethig RS. 2009. The sequential sction of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138: 750-759.

Yamaguchi A, Wu M-F, Yang L, Wu G, Poethig RS and Wagner D. 2009. The MicroRNA-Regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Developmental Cell 17: 268-278.

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Toxic nectar to improve pollinator fidelity?

Posted on March 22, 2013 by

Amy L. Parachnowitsch
Plant Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden 75236. email: amyparachnowitsch@gmail.com

Maybe because so many of us rely and enjoy caffeine (I’m sipping a large cup of tea as I write this), a recent Science paper on flowers dosing their nectar with caffeine has made quite an impact in popular media. You can find accounts of the paper at New York Times, National Geographic, ScienceNews and pretty much any news source you care to read. The blog world also is a buzz (excuse the pun) with this paper. Everything from science blogs such as Scientific American, Discover, Addiction to food/barista sites (Home-Barista, Foodbeast, Champagnewhisky) are talking about this research.

What makes this particular article so interesting to so many? On the surface, this story touches upon things which people are generally intrigued about: drugs and improving memory. It doesn’t hurt that the drug involved, caffeine, is one people are familiar with and most have directly experienced. There are plenty of good descriptions of this research (including the original article and its summary), and I suggest taking the time to read the full story. In short, Geraldine Wright and coauthors discovered that bees could remember floral cues (scent) better if the reward they received contained caffeine via the caffeine’s action of stimulating the bees’ brain cells. Moreover, plants that produce caffeine in their nectar seem to do this at a level that is active but not so high that bees will reject the nectar because of the bitter taste.

Beyond our interest in drugs and memory, I think what makes these kinds of stories resonate so strongly with non-scientists is that plants are often viewed as static things that we (or other animals) exploit. Rarely do people consider that plants might actually be exploiting us (or other animals), although Mikael Pollan popularized this concept in his best seller The Botany of Desire. Of course, those studying plants have no difficulty seeing that plants do behave, and that evolutionarily, they have been selected to exploit animals in all kinds of ways.

Image courtesy of Geraldine Wright

Bee on citrus flower. Image courtesy of Geraldine Wright

As a pollination biologist and evolutionary ecologist, I’m interested in these findings because the work adds to our understanding of the co-evolutionary interactions between flowers and their pollinators. By improving memory of pollinators these plants may increase pollinator fidelity, suggesting that an important function of ‘toxic nectar’ may be to manipulate pollinators. However, secondary compounds in nectar are common (e.g. toxic nectar), and much work remains to understand the ecological and evolutionary roles of these different components of floral reward. I am excited to see research programmes such as those of this group (and others) proceed because their work hints at the growing trend of approaching floral phenotypes in a holistic way. In this study, caffeine found in the floral nectar enhanced bees memory of floral scent. Thus, to appreciate the role of reward (nectar), secondary compounds found in the reward (caffeine) and scent, it was necessary to study all of these components together. The more we integrate different aspects of floral phenotypes into research programmes, the better we will be able to understand the amazing floral diversity we see.

References

Adler LS. (2000), The ecological significance of toxic nectar. Oikos, 91: 409–420. doi: 10.1034/j.1600-0706.2000.910301.x

Chittka L and Peng F. Caffeine Boosts Bees’ Memories. Sciences. 2013. Vol. 339 no. 6124 pp. 1157-1159. DOI: 10.1126/science.1234411

Wright GA, Baker DD, Palmer MJ, Stabler D, Mustard JA, Power EF, Borland AM, Stevenson PC. Caffeine in Floral Nectar Enhances a Pollinator’s Memory of Reward. Science. 2013. Vol. 339 no. 6124 pp. 1202-1204.

Pollan M. The Botany of Desire (2001). Random House, hardcover: ISBN 0-375-50129-0, 2002 paperback: ISBN 0-375-76039-3

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How flowers excel in their hospitality: the evolution of papillate conical cells in petals is linked with accommodating the right visitors

Posted on March 5, 2013 by

Louis Ronse De Craene
Royal Botanic Garden Edinburgh, Edinburgh EH3 5LR, Scotland, UK. l.ronsedecraene@rbge.ac.uk

Most flowers rely on animal pollinators for the transfer of their genes. As a result, flowers have developed different strategies to attract and reward pollinators, including variable shapes, specific scent, colour, and nectar production.

Petals are the main visual attractant for floral visitors and have evolved repeatedly in the angiosperms (Ronse De Craene and Brockington 2013). Petals can be generally distinguished from sepals by their bright colour, but also by the development of a specific cell type. These cells, called papillate conical cells, are generally concentrated mainly on the ventral side of the petal. Conical cells have been considered as a distinctive trait for petals that are found in the majority of angiosperms and several authors consider the conical cells as a defining marker for petal identity (Irish 2009).

SEM of conical cells, Solanum. Courtesy of B. Glovers.

SEM image of the ventral petal surface of Solanum sp. (Solanaceae) showing the conical epidermal cells. Courtesy of B. Glovers.

As such they are used as evidence for explaining homeotic conversions between petals and other organs. The petal epidermal micromorphology is increasingly investigated as a marker of petal identity (e.g. Logacheva et al. 2008, Ojeda et al. 2009, Landis et al. 2012).

The genetic basis for conical cells is complex. Conical cells in Antirrhinum and Petunia are regulated by MIXTA and MIXTA-like genes (Noda et al. 1994, Baumann et al. 2007), which have also been linked to hair formation. In petals, MIXTA is expressed when the cells do not divide, and so they differentiate as conical cells. However, in leaves of transgenic plants ectopically expressing MIXTA the cells divide and produce trichomes (Glower et al. 1988). In the bilaterally symmetric flowers of Lotus japonicus (Leguminosae), homologues of CYCLOIDEA are responsible for the differentiation of the dorsal petal and the activation of MIXTA genes linked with the development of papillate conical cells (Feng et al. 2006, Wang et al. 2010). However, in Arabidopsis it is not known which genes are responsible for the conical cell formation (Glover and Martin 2002).

In a recent review Whitney et al. (2011) explained that conical cells are important in changing the optical properties of the petals, as well as their wettability, temperature and the production of scent. The most important attributes, however, are optical and mechanical, in advertising the flower and in providing a foothold for visitors (Kay et al. 1981, Whitney et al. 2009, Alcorn et al. 2012). Bees are known to grasp the petals, especially in vertical bilaterally symmetrical flowers, and this is the main function of the conical cells, next to light absorption. Birds, on the other hand, do not need a foothold, as they can hover in front of the flower (the case of hummingbirds), or visit the flower from a neighbouring perch (most honeycreepers and sunbirds) (Proctor et al. 1996). Thomson and Wilson (2008) reviewed the mechanisms leading to a shift between bee and hummingbird pollination in closely related species, such as Mimulus and Penstemon. However, they did not consider the presence or absence of conical cells. Attributes of bird pollination are different, and one could be the absence of conical cells.

Aphelandra scabra: bird pollinated flower. Courtesy of L Ronse de Craene

Aphelandra scabra: bird pollinated flower. Courtesy of L Ronse de Craene

Indeed, Ojeda et al. (2012) investigated the presence of conical cells on petals of Macaronesian Lotus (Leguminosae), using established knowledge of the phylogenetic relationships in the genus. They demonstrated that conical cells are lost when flowers shift from bee pollination to bird pollination. While most bee-pollinated Lotus species are characterized by abundant conical cells, especially on the standard petal and to a lesser extent on the wings, bird-pollinated species, such as L. berthelotii have the papillate cells replaced by tabular rugose cells. The authors also found a higher concentration of trichomes on the standard and wing petals and suggested that a shift to bird pollination was accompanied by a shift in petal identity. The known gene expression in Lotus japonicus shows the requirement of LjCYC2 for standard petal development and the differentiation of conical cells, while LjCYC3 appears to regulate the development of wings and tabular rugose cells (Feng et al 2006. 2006, Weng et al. 2011). In bird pollinated Lotus LjCYC3 would have a more expanded expression at the expense of LjCYC2. The driving force in this change must be the pollinator preferences.

The example of Lotus shows the flexibility of flowers to adapt to different pollinators. The transition functions as a means to exclude one kind of visitor to the advantage of another. That conical cells have a major function as providing a foothold for visitors comes from observations in other groups of plants. It is not only the bird pollination syndrome that leads to a loss of conical cells. Case studies in Solanaceae have shown that conical cells are variously present in the genera Solanum and Nicotiana (Glover pers. comm.). An important factor for loss of conical cells besides bird pollination could be a shift to buzz-pollination. The mechanism of buzz-pollination implies that pollen is released from the anthers by the vibration of wings of visiting insects.

Ramonda myconi(Gesneriaceae): buzz-pollinated flower with exposed anthers and reflexed petals. Courtesy of L Ronse de Craene

Ramonda myconi (Gesneriaceae): buzz-pollinated flower with exposed anthers and reflexed petals. Courtesy of L Ronse de Craene

In buzz-pollinated flowers petals are usually reflexed and visitors either hover below the flower or grasp the anthers to shake out the pollen (Proctor et al. 1996). In a broader study of Leguminosae, Ojeda et al. (2009) also found that conical cells are not distributed evenly among different subfamilies. While Faboideae generally have conical cells, these are not always present in Caesalpinoids, and are generally absent in Mimosoids. Flowers of Mimosoids have their flowers grouped in heads and the main attractant are long showy stamens (so-called brush flowers: Ronse De Craene 2010). As a result the smaller petals lack the conical papillate cells.

These observations indicate that conical cells are very specifically correlated with specific pollination systems as suggested by Kay et al. (1981) and that shifts in pollinators could lead to their disappearance. A current project at RBGE is investigating the evolution of conical cells in the Gesneriaceae, a large mainly tropical family that has evolved different modes of pollination. The understanding of the phylogeny of this large family (e.g. Möller et al. 2009) and known pollination mechanisms (e.g. Harisson et al. 1999) is important to postulate evolutionary changes and the drivers for change in the floral morphology.

Flowers have a tremendous ability to adapt to changes in requirements from visitors and – in a striking analogy with the human world – are truly experts in changing the accommodation and shifting the menu on offer to full satisfaction of the customer.

References

Alcorn, K., Whitney, H. and B.J. Glover. 2012. Flower movement increases pollinator preference for flowers with better grip. Functional Ecology 26: 941-947.

Bauman, K., Perez-Rodriguez, M., Bradley, D., Venail, J., Bailey, P., Hailing, J. et al. 2007. Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development 134: 1691-1701.

Feng, X., Zhao, Z., Tian, Z., Xu, S., Luo, Y., Ca, Z., Wang, Y. et al. 2006. Control of petal shape and flower zygomorphy in Lotus japonicus. Proceedings of the National Academy of Science USA 103: 4970-4975.

Glover, B.J., and C. Martin. 2002. Evolution of adaptive petal cell morphology. In Q.C.B. Cronk, R.M. Bateman, and J.A. Hawkins, eds., Developmental Genetics and Plant Evolution. Taylor & Francis, London, 160-172.

Glover, B.J., Perez-Rodriguez, M., and C. Martin. 1998. Development of several epidermal cell types can be specified by the same MYB-related plant transcription factor. Development 125: 3497-3508.

Harrison, C.J., Möller, M., and Q.C.B. Cronk. 1999. Evolution and development of floral diversity in Streptocarpus and Saintpaulia. Annals of Botany 84: 49-60.

Irish, V. 2009. Evolution of petal indentity. Journal of Experimental Botany 60: 2517-2527.

Kay, Q.O.N., Daoud, H.S., and C.H. Stirton. 1981. Pigment distribution, light reflection and cell structure in petals. Botanical Journal of the Linnean Society 83: 57-84.

Landis, J.B., Barnett, L.L., and L.C. Hileman. 2012.  Evolution of petaloid sepals independent of shifts in B-class MADS box gene expression. Development Genes and Evolution 222: 19-28.

Logacheva, M.D., Fesenko, I.V., Fesenko A.N., and A.A. Penin. 2008. Genetic and morphological analysis of floral homeotic mutants tepal-like bract and fagopyrum apetala of Fagopyrum esculentum. Botany 86: 367-375.

Möller, M., et al. 2009. A preliminary phylogeny of the ‘Didymocarpoid Gesneriaceae’ based on three molecular datasets: incongruence with available tribal classifications. American Journal of Botany 96: 989-1010.

Noda, K.I., Glover, B.J., Linstead, P., and C. Martin. 1994. Flower colour intensity depends on specialized cell shape controlled by a Myb-related transcription factor. Nature 369: 661-664.

Ojeda, I., Francisco-Ortega, J., and Q.C.B. Cronk. 2009. Evolution of petal epidermal micromorphology in Leguminosae and its use as a marker of petal identity. Annals of Botany 104: 1099-1110

Ojeda, I. Santos-Guerra, A., Caujapé-Castells, J., Jaén-Molina, R., Marrero, A., and Q.C.B. Cronk. 2012. Comparative micromorphology of petals in macaronesian Lotus (Leguminosae) reveals a loss of papillose conical cells during the evolution of bird pollination. International Journal of Plant Sciences 173: 365-374.

Proctor, M., Yeo, P., and A. Lack. 1996. The Natural History of pollination. Timber Press, Portland, Oregon.

Ronse De Craene, L.P. 2010. Floral diagrams. An aid to understanding flower morphology and evolution. Cambridge, Cambridge University Press.

Ronse De Craene, L.P., and S. Brockington. 2013. Origin and evolution of petals in the angiosperms. Plant Ecology and Evolution 146: in press.

Thomson, J.D., and P. Wilson. 2008. Explaining evolutionary shifts between bee and hummingbird pollination: convergence, divergence, and directionality. International Journal of Plant science 169: 23-38.

Wang, J. Wang, Y., and D. Luo. 2010. LjCYC gees constitnte floral dorsoventral asymmetry in Lotus japonicus. Journal of Integrative Plant Biology 52: 959-970.

Weng, L., Tian, Z., Feng, X., Li, X., Xu, S., Hu, X., Luo, D., and J. Yang. 2011. Petal development in Lotus japonicus. Journal of Integrative Plant Biology 53: 770-782.

Whitney, H., Chittka, L. Bruce, T., and B.J. Glover. 2009. Conical epidermal cells allow bees to grip flowers and increase foraging efficiency. Current Biology 19: 948-953.

Whitney, H.M., Bennett, K.M.V., Dorling, M., Sandbach, L., Prince, D., Chittka, L., and B.J. Glover. 2011. Why do so many petals have conical epidermal cells?  Annals of Botany 10: 609-616.

Thanks to Beverley Glover for helpful suggestions to improve the text.

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Does a petunia of any other name smell as sweet? Unraveling the complexity of floral scents
Amy L. Parachnowitsch
Plant Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden 75236. email: amyparachnowitsch@gmail.com

As the perfume industry and anyone who has ever dabbed on scent before a date are keenly aware, smells can help attract mates. Flowers use such volatile blends, which we, in turn, often use in our perfumes, to attract the pollinators that do their mating for them. However, much like other floral characters (Strauss and Whittall 2006), there is a growing appreciation that agents other than pollinators may drive the function and evolution of floral scents.

Diabrotica undecimpunctata on Petunia x hybrida

Diabrotica undecimpunctata on Petunia x hybrida

In Ecology Letters, Kessler et al. (2012) examine the possibility that some components of volatile blends might function to deter herbivores, rather than attract pollinators. The problem many plants may face with advertising floral rewards to pollinators with scent or really any showy trait, is that plants might inadvertently attract herbivores (e.g. Theis and Adler 2011). Thus, floral traits may represent a compromise between attracting mutualistic and antagonistic visitors. The conflict in scent production might be particularly important for night flowering plants that cannot rely on visual cues to attract pollinators. Kessler et al’s study builds on previous work that has shown volatiles can function to reduce herbivory (e.g. Kessler et al. 2008, Junker and Blüthgen 2010, Galen et al. 2011). Here, the authors take advantage of genetically transformed night flowering petunia (Petunia x hybrida) that were gene-silenced at different points in the shikimate and phenylpropaniod scent pathways. Using five different lines, they were able expose plants with different floral scent blends to herbivory and compare their performance. What makes their approach particularly powerful is that the genetically transformed plants were exposed to field conditions to assess the ecological impacts of the blends. Kessler et al. focused on florivore interactions because florivores are particularly likely to be sensitive to floral scents (florivores eat flowers), and are likely to exert selection on floral traits due to their more direct impact on fitness than leaf herbivores (McCall and Irwin 2006).

The authors found three petunia floral scents that were important in plant-florivore interactions. Methyl benzoate, an important attractant of petunia pollinators, was a host location cue for generalist florivores. Therefore, methyl benzoate production is likely under conflicting selection by mutualists and antagonists – a hypothesis that could be tested in wild populations of native petunias. Unfortunately, this study did not examine pollinator behaviour, so it is unknown whether pollinators would also avoid lines with reduced methyl benzoate. For two other compounds, isoeugenol and benzyl benzoate, increased emission acted as feeding deterrents for generalist florivores. In an elegant manipulation, the authors paired field and feeding trial results with a volatile-addition experiment. Adding the feeding deterrents to the volatile headspace of lines that lacked these compounds rescued the deterrent effect on florivores, confirming the function of these volatiles. Again, pollinator response is unknown. However, this set of experiments was able to definitively determine the functional role of these three compounds in generalist florivore interactions. These plants are not native to the habitat where they were tested, it is thus possible that interactions in the native range and for native plants could differ from what was observed here.
Nonetheless, these results suggest that complex floral volatile blends are likely the result of selection by multiple agents and function to both attract pollinators and repel herbivores.

It is an exciting time to be studying floral scents. As analyses of these traits becomes more accessible, we are gaining a more holistic understanding of floral scents and their role in plant-insect interactions (e.g. Schiestl 2010). A complete picture of the role of scent in floral diversity will come from studying floral phenotypes in an integrated fashion as well as studying the multiple agents that exert selection on floral traits. Combining mechanistic studies such as the example discussed here with studies of naturally occurring plant phenotypes (e.g. Galen et al. 2011, Parachnowitsch et al. 2012) will strengthen our understanding of function and evolution of scent in flowers.

References

Galen, C., R. Kaczorowski, S. L. Todd, J. Geib, and R. A. Raguso. 2011. Dosage dependent impacts of a floral volatile compound on pollinators, larcenists, and the potential for floral evolution in the alpine skypilot Polemonium viscosum. American Naturalist 177:258-272.

Junker, R. R. and N. Blüthgen. 2010. Floral scents repel facultative flower visitors, but attract obligate ones. Annals of Botany 105:777-782.

Kessler, D., C. Diezel, D. G. Clark, T. A. Colquhoun, and I. T. Baldwin. 2012. Petunia flowers solve the defence/apparency dilemma of pollinator attraction by deploying complex floral blends. Ecology Letters.

Kessler, D., K. Gase, and I. T. Baldwin. 2008. Field experiments with transformed plants reveal the sense of floral scents. Science 321:1200-1202.

McCall, A. C. and R. E. Irwin. 2006. Florivory: The intersection of pollination and herbivory. Ecology Letters 9:1351-1365.

Parachnowitsch, A. L., R. A. Raguso, and A. Kessler. 2012. Phenotypic selection to increase floral scent emission, but not flower size or colour in bee-pollinated Penstemon digitalis. New Phytologist 195:667-675.

Schiestl, F. P. 2010. The evolution of floral scent and insect chemical communication. Ecology Letters 13:643-656.

Strauss, S. Y. and J. B. Whittall. 2006. Non-pollinator agents of selection on floral traits. In: LD Harder and SC H. Barrett, editors. Ecology and Evolution of Flowers. Oxford University Press, Oxford, UK. pp. 120–138.

Theis, N. and L. S. Adler. 2011. Advertising to the enemy: enhanced floral fragrance increases beetle attraction and reduces plant reproduction. Ecology 93:430-435.

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Mutations in a circadian regulator contribute to crop adaptation

Posted on December 20, 2012 by

Ben Trevaskis CSIRO Plant Industry, Black Mountain ACT 2601, Australia

Plants growing in temperate regions respond to seasonal changes in day length and temperature to coordinate flowering with optimal conditions. Variation in sensitivity or responsiveness to seasonal cues contributes to adaptation to different latitudes and climates by adjusting seasonal flowering behaviour to suit local conditions, allowing some plant species to occupy broad geographical ranges. Variation in seasonal flowering behaviour has also been harnessed in agriculture to produce crop varieties suited to different climates and geographical regions, and also varying sowing dates in the case of annual crops.

A recent study by Weller et al. (2012) examined the molecular basis for different day length requirements in peas (Pisum sativum). The wild ancestral forms of pea typically germinate in autumn and grow vegetatively through winter before flowering in response to increasing day length in spring. Under controlled conditions, accessions with the ancestral flowering behaviour are late flowering in short days. Many modern field pea varieties have a reduced requirement for long days and so flower rapidly in either short or long days. This flowering behaviour allows crops to be grown where the requirement for long days would not be met, at low latitudes for example, or where rapid crop cycling is required irrespective of daylength; such as northern latitudes where crops are sown in spring to avoid harsh winter conditions.

By investigating the molecular basis for variation in day length sensitivity amongst different accessions of pea, Weller et al. (2012) identified two loci that contribute to reduced long-day requirement. One of these loci was mapped to a loss-of-function mutation in the pea orthologue of the Arabidopsis EARLY FLOWERING 3 (ELF3) gene. This is consistent with the functional role of ELF3 in Arabidopsis; loss-of-function mutations in ELF3 cause early flowering in Arabidopsis grown in short days (Zagotta et al., 1996).  Arabidopsis, like pea, is normally late flowering in short days. Haplotype analysis suggests that a loss-of-function mutation in ELF3 that is now broadly distributed in modern varieties arose in a common ancestor, and has been selected in peas grown in regions where crops are grown in short day lengths or where rapid cycling is beneficial. Weller et al. (2012) also showed that a loss-of-function mutation in ELF3 is linked to reduced long day requirement in lentils (Lens culinaris), another temperate legume crop.

The apparent contribution of a loss-of-function mutation in ELF3 to range expansion of pea has a parallel in temperate cereals. Loss-of-function mutations in the barley ELF3 gene cause early flowering in short days, and have been used to adapt barley cultivars to different growing regions (Faure et al., 2012; Zakhrabekova et al.,2012). For example, a ELF3 loss of function mutation generated in a Swedish mutagenesis breeding program was used to breed fast cycling, day length insensitive barleys that can be grown in areas with short spring/summer growing seasons in Nordic countries (Zakhrabekova et al., 2012).

The early flowering phenotype of Arabidopsis elf3 mutants is associated with elevated expression of the FLOWERING LOCUS T (FT) (Suarez-Lopez et al., 2001). FT is a potent promoter of flowering that is normally expressed in long days to trigger the long-day flowering response, so high levels of FT expression can explain the early flowering of elf3 mutants in short days. Although the molecular mechanism underlying the early flowering phenotype of the pea ELF3 loss-of-function mutants is unclear, a similar molecular mechanism seems likely (see Hecht et al., (2011) for more details of the role of FT–like genes in flowering time control in pea). Mutations in the Arabidopsis ELF3 gene also disrupt circadian rhythms (Hicks et al., 1996). Both pea and barley ELF3 mutants exhibit similar disruption of circadian rhythms (Faure et al., 2012, Weller et al., 2012; Zakhrabekova et al., 2012). This raises interesting questions:
How critical is the circadian clock for the cultivation of crops? How many circadian functions can be lost to produce different flowering behaviours before plant performance is compromised? Potentially the cultivation of crops in managed environments has allowed the loss of diurnal rhythms, at least in some growing regions. This will be an interesting area for future research.

The recent finding that the ELF3 gene is a major determinant of reduced long-day requirement in temperate legumes and temperate cereals is a fine example of how knowledge generated in model systems can be applied to increase our understanding of crop biology. This research will have direct impact on crop breeding programmes by facilitating marker assisted selection and by allowing rapid screening for allelic diversity through gene re-sequencing.

References

Faure S, Turner AS, Gruszka D, Christodoulou V, Davis SJ, von Korff M, Laurie DA. 2012. Mutation at the circadian clock gene EARLY MATURITY 8 adapts domesticated barley (Hordeum vulgare) to short growing seasons. PNAS 109, 8328-8333.

Hecht V, Laurie RE, Vander Schoor JK, Ridge S, Knowles CL, Liew LC, Sussmilch FC, Murfet IC, Macknight RC, Weller JL. 2011. The pea GIGAS gene is a FLOWERING LOCUS T homolog necessary for graft-transmissible specification of flowering but not for responsiveness to photoperiod. Plant Cell 23, 147-161.

Hicks KA, Millar AJ, Carré IA, Somers DE, Straume M, Meeks-Wagner DR, Kay SA. 1996. Conditional circadian dysfunction of the Arabidopsis early-flowering 3 mutant. Science 274, 790-792.

Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G. 2001. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410, 1116-1120.

Weller JL, Liew LC, Hecht VF, Rajandran V, Laurie RE, Ridge S, Wenden B, Vander Schoor JK, Jaminon O, Blassiau C, Dalmais M, Rameau C, Bendahmane A, Macknight RC, Lejeune-Hénaut I. 2012. A conserved molecular basis for photoperiod adaptation in two temperate legumes.www.pnas.org/cgi/doi/10.1073/pnas.1207943110.

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It’s about time – rapid evolution of flowering time in response to insect herbivores

Posted on December 7, 2012 by

 Amy L. Parachnowitsch
Plant Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden 75236. email: amyparachnowitsch@gmail.com

When to flower is an important life history decision for angiosperms, one that can influence both the abiotic and biotic environment of reproduction.  Therefore, it is not surprising that flowering time is frequently linked to plant fitness and is under phenotypic selection in many wild populations (Munguía-Rosas et al. 2011).  

A recent study by Agrawal and colleagues (Agrawal et al. 2012) has also highlighted the possibility for rapid evolution in flowering time. These authors set out to test experimentally  whether evening primrose (Oenothera biennis L.) would evolve in response to selection by herbivores.  Their field study is impressive because they examined evolutionary change in experimental populations.  To test for rapid evolution, they created replicate populations of the same O. biennis genotypes.  They then experimentally manipulated insect herbivory in these populations by spraying half with insecticide and monitored changes in genotypic frequency and phenotypic traits for the next three generations.

Oenothera biennis. Photo by AA Agrawal.
Oenothera biennis. Photo by AA Agrawal.

For Oenothera biennis, flowering time is a key trait that predicts specialist pre-dispersal seed predation; later flowering plants avoid such damage.  Even on such a short time scale (4 years), populations relatively herbivore-free evolved earlier flowering times than those with herbivores.  Insect suppression also led to reduced chemical defence in fruits, and changes in community composition with insect suppression also affected evolution in competitive ability of O. biennis.  Taken together, these results emphasise the complex nature of plant-insect interactions and their eco-evolutionary effects. 

What makes the O. biennis example different from many flowering plants is that despite its showy flowers, O. biennis does not rely on pollinators for seed production.  Furthermore, O. biennis has a genetic system to prevent outcrossing, although outcrossing can occur rarely (one such cross was detected in this study).  However, we can exclude pollinators as a major contributor to the evolutionary patterns of flowering time that Agrawal et al. observed.  For outcrossing plants, the importance of flowering time is often considered in terms of its effect on plant-pollinator synchronization and availability of mates.  Therefore, we might predict flowering time to be under pollinator-mediated selection in outcrossing plants. However, my own work and others (Elzinga et al. 2007, Parachnowitsch and Caruso 2008, Parachnowitsch et al. 2012) suggest that herbivores might also be important agents of selection on flowering time, even in systems where pollinators are necessary for seed production.  An exciting future possibility would be to examine this kind of rapid evolution in flowering time in species where multiple interactions are influenced by flowering time.  Ultimately, experimental evolution studies in field conditions such as Agrawal et al. will allow us to understand better the causal agents of selection, and how these interactions lead to evolutionary change.  For now, Agrawal et al. provide an enlightening study furthering our understanding of how ecological interactions can influence rapid evolutionary change and the feedback mechanisms between these processes.

References

Agrawal, A. A., A. P. Hastings, M. T. J. Johnson, J. L. Maron, and J.-P. Salminen. 2012. Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338:113-116.

Elzinga, J. A., A. Atlan, A. Biere, L. Gigord, A. E. Weis, and G. Bernasconi. 2007. Time after time: flowering phenology and biotic interactions. Trends in Ecology & Evolution 22:432-439.

Munguía-Rosas, M. A., J. Ollerton, V. Parra-Tabla, and J. A. De-Nova. 2011. Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured. Ecology Letters 14:511-521.

Parachnowitsch, A. L. and C. M. Caruso. 2008. Predispersal seed herbivores, not pollinators, exert selection on floral traits via female fitness. Ecology 89:1802-1810.

Parachnowitsch, A. L., C. M. Caruso, S. A. Campbell, and A. Kessler. 2012. Lobelia siphilitica plants that escape herbivory in time also have reduced latex production. PLoS ONE 7:e37745.

Oenothera biennis L.

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Flowering Highlights

Posted on December 4, 2012 by

Flowers are beautiful, scientifically fascinating and economically important. Not surprisingly, much focus in plant biology aims to unravel flower biology: from signals that induce or prevent flower formation, to mechanisms of floral development and interactions with pollinators, to evolution of new morphological structures.
The diversity of research on flowering rivals that of flowers themselves! Given that diversity, can you be certain that you did not miss the latest paper introducing a new concept or questioning a long-standing hypothesis? Would you like to receive alerts of the latest big developments in the field? Flowering Highlights is designed to bring you authoritative commentaries on the most fascinating articles and developments on flowering research.
Flowering Highlights will be posted online (www.floweringhighlights.org) with an e-alert service to subscribers of the Flowering Newsletter. A selection of the monthly highlights will be published in the annual issue of the Flowering Newsletter.

I am indebted to a great group of colleagues who agreed to contribute to this new development of the Flowering Newsletter. They aim to bring you exciting, unexpected, paradigm-shifting or simply particularly elegant studies on flowering, and I am curious to see their selections.

The current members of the editorial board of Flowering Highlights are:
Ben Trevaskis (Black Mountain, Australia), Aalt-Jan van Dijk (Wageningen, Netherlands), Amy Parachnowitsch (Uppsala, Sweden), Beverley Clover (Cambridge, UK), Cristina Ferrandiz (Valencia, Spain), Günther Theißen (Jena, Germany), John Stinchcombe (Toronto, Canada), Maria Albani (Cologne, Germany), Maria von Korf (Cologne, Germany), Martin Lascoux (Shanghai, China and Uppsala, Sweden), Raphaël Mercier (Versailles, France), Soraya Pelaz Herrero (Bellaterra, Spain), Louis Ronse De Craene (Royal Botanic Garden Edinburgh, UK).

I look forward to reading about the diversity of research on flowering and I encourage you to be curious and go back to the original article, but also feel free to discuss topics and comment on controversial findings!

And finally, do not forget to subscribe!

Lars Hennig
Flowering Newsletter Editor
Journal of Experimental Botany

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