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Keywords:

  • ornamentals;
  • genetic modification;
  • transgenic;
  • colour modification;
  • regulation;
  • harmonization

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Genetically modified ornamentals; pipeline and products
  5. Hurdles to commercialisation
  6. The regulatory environment
  7. Looking ahead
  8. Acknowledgements
  9. References

Plant transformation technology (hereafter abbreviated to GM, or genetic modification) has been used to develop many varieties of crop plants, but only a few varieties of ornamental plants. This disparity in the rate and extent of commercialisation, which has been noted for more than a decade, is not because there are no useful traits that can be engineered into ornamentals, is not due to market potential and is not due to a lack of research and development activity. The GM ornamental varieties which have been released commercially have been accepted in the marketplace. In this article, progress in the development of transgenic ornamentals is reviewed and traits useful to both consumers and producers are identified. In considering possible factors limiting the release of genetically modified ornamental products it is concluded that the most significant barrier to market is the difficulty of managing, and the high cost of obtaining, regulatory approval.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Genetically modified ornamentals; pipeline and products
  5. Hurdles to commercialisation
  6. The regulatory environment
  7. Looking ahead
  8. Acknowledgements
  9. References

Ornamentals in society

Ornamental plants play a fundamental part in the way humans interact with and modify the environment. Plants having no medicinal or food value have been gathered and domesticated for thousands of years, purely because of the ornamental value of their morphology or flowers. The economic, environmental and well-being benefits of the horticulture industry are well documented (Hall and Dickson, 2011). As European explorers gathered plants from around the world and breeders exploited the variation that could be generated from cross breeding and mutation breeding, the range and diversity of cultivated ornamental plants increased enormously. Now, thousands of varieties of cut-flowers, pot plants, hanging plants, bedding plants, shrubs, lawn and turf, ornamental tree and aquatic plants are available to the public. These are sold through a nursery and floriculture industry that plays a not insignificant part in the economy of most countries, and a significant part in several dozen. In the developed economies, ancillary industries have evolved around floristry, gardening, landscaping and environmental amenity industries, all based around the use of ornamental plants (Dobres, 2011; Hall and Hodges, 2011).

Economic value

Though statistics are diffuse and subject to the vagaries of definition, according to the UN COMTRADE statistics the 2010 trade in floricultural products alone was in the order of 8 billion USD. Reports from the US based national gardening association (http://www.gardenresearch.com) suggest that US consumers spend in the region of 35–45 billion USD per annum on professional lawn care, garden maintenance, landscaping and tree care services. Hall and Hodges (2011) estimated total sales in the U.S. for all aspects of lifestyle horticulture to be in excess of 175 billion USD, representing 0.76% of gross domestic product.

Taking into account domestic production of ornamentals and the value added from ancillary industries and trades, it is reasonable to estimate that the ornamentals sector of the horticulture industry has a global economic value of 250–400 billion USD (approximately 0.4%–0.6% of world gross domestic product).

Scope of this review

This review focuses on the application of genetic modification (transgenic: GM) technology to non-food ornamental products, which, in comparison to the major food crops, can be said to be minor, or speciality crops. It is not our intention to review specific transgenic traits. The review articles cited throughout provide such detail. Rather, our focus is on possible reasons why GM varieties of speciality ornamental crops have not been commercialized as widely as those in major crops. For a discussion of barriers and limitations to commercialising speciality food crops see Alston et al. (2006), Kalaitzandonakes et al. (2007), Miller and Bradford (2010), Rommens (2010) and Sexton and Zilberman (2011). In preparing this review we decided only to include ornamentals suited to the nursery, cut-flower and home garden. The potential application to grasses, as used in the lawn, sod and turf market is not covered. This is not only because this sector is outside our range of expertise, but also because the commercialisation of GM lawn and turf grasses presents a different set of considerations to other ornamental species. For example, the turf grass industry dwarfs other non-food ornamentals in its value (Harriman et al., 2006), but is dominated by just a few species. In contrast there are hundreds of species and thousands of varieties of cut flowers and pot and bedding plants in a very fragmented ornamentals industry (Dobres, 2011). The lawn and turf industry is an excellent target for GM technology (Harriman et al., 2006) with the potential to improve turf grass quality whilst significantly reducing chemical inputs.

The main groups of non-food ornamentals considered in the scope of this review, and important representative plants within these groups, are listed in Table 1. Table 1 provides only a glimpse of the huge range of plants species available to the ornamental industry. An impression of this diversity can be gained at any retail nursery or florist, or from any seed or plant catalogue.

Table 1.   Major groups and genera of ornamental plants
Cut-flowersOrnamental grassesPalmsPotted and indoorBedding plantsShrubsTreesMiscellaneous
Rose Festuca spp.Fan palm Phalaenopsis sppPetuniaRoseDogwoodBonsai
CarnationDeer grassDate palmRosePansy Hydrangea Rhododendron Azalea spp.CotoneasterCacti
ChrysanthemumTufted hair grassCanary Island date palm Kalanchoe spp. Impatiens spp.AbeliaMapleSucculents
Tulip Panicum spp.Sabal palm Campanula spp.BegoniaViburnumWillowAir plants
Lily Agrostis spp.Sago palmEnglish IvyToreniaAgapanthausBirchFerns
Gerbera Miscanthus sinensis Pindo palm Anthurium spp. Salvia spp. Camellia spp.AshBox
Babys breath Carex spp.Queen palm Dracaena spp. Calibrachoa spp.FuchsiasEucalyptus 
Peruvian lily  ChrysanthemumLobeliaGrevilliaLiquidambar 
Freesia spp.   Ficus spp. Osteospermum spp.LavenderCedar 
Cymbidium spp.   Spathiphyllum spp.Verbena Ficus spp.Mulberry Paulownia 
Anthurium spp.   Cyclamen spp.PinksMagnoliaPolar 
Lisianthus  LilyAfrican violetGrape myrtlePrunus 
Zantedeschia spp.  GeraniumCrocusPrivetOak 
Dendrobium spp.  Poinsettia Narcissus spp.IvyElm 
Phalaenopsis spp.  Heather Skimmia spp.Hibiscus Chamaecyparis spp. 
Narcissus spp.  Spider plantHelleboresHeather  
Hydrangea  Bromeliads  Skimmia spp.  
    Cacti  Gaultheria spp.  
   Bonsai    
   Amaryllis    
    Cattleya spp.    
   Hyacinth    

Genetically modified ornamentals; pipeline and products

  1. Top of page
  2. Summary
  3. Introduction
  4. Genetically modified ornamentals; pipeline and products
  5. Hurdles to commercialisation
  6. The regulatory environment
  7. Looking ahead
  8. Acknowledgements
  9. References

Genetic modification has been incorporated into the development of herbicide and insect resistant varieties of Zea mays (maize), Glycine max (soybean), Brassica napus (canola), Gossypium spp. (cotton) and other important food species for two decades. This development has been supported by significant public and private research in many countries and has been proven to increase the profitability of growers and to reduce impacts on the environment (Alston et al., 2006). In the case of ornamentals, there is also a research effort underway, and the main areas in which this research is being undertaken are outlined in this section. In some ornamentals, development of new varieties through hybridization or mutagenesis is very difficult or lengthy, or is not an option if varieties are completely sterile, as in orchids (Da Silva et al., 2011). In these cases, GM provides an avenue for variety improvement. In other ornamentals there are particularly good varieties with excellent post-harvest qualities, disease resistance and productivity. Using GM techniques these characteristics can be retained in the transgenic lines, whilst at the same time increasing the product range (through flower colour manipulation, for example). These and similar advantages of GM technology in ornamentals have been outlined by Chandler and Brugliera (2011), Debener and Winkelmann (2010), Dobres (2008, 2011), Hsiao et al. (2011) and Underwood and Clarke (2011).

Transformation

Fifty or so ornamental plants can now be transformed (Brand, 2006; Shibata, 2008) and the challenges associated with the transformation of ornamentals are the same as those faced in any plant species. These include the resistance to infection by Agrobacterium in monocot species, variety-variety variability in regeneration capacity and transformation efficiency, somaclonal variation and the difficulties associated with regeneration from mature plant tissues in woody plants.

Flower colour modification

The only GM ornamental products which have so far been released to the market are flower colour modified varieties of carnation (Dianthus caryophyllus) and rose (Rosa × hybrida).1 Colour modification dominates the GM research that has so far been carried out in ornamentals (Auer, 2008; Underwood and Clarke, 2011). That novel colours are the first products from the ornamental area is a reflection of the facts that, commercially, flower colour is one of the most important characters of many ornamental plant types and that research on the genetics of flower colour has a long history. Additionally, in many ornamentals colour range is limited by the genetics of the plant species (Debener and Winkelmann, 2010) and GM is the only effective way to overcome this limitation (Tanaka et al., 2010). GM of flower colour was first demonstrated more than 20 years ago (Meyer et al., 1987) and in 1993 the gene encoding flavonoid 3′5′-hydroxylase was isolated (Holton et al., 1993), providing the tool to allow development of the colour-modified D. caryophyllus and R. × hybrida now on the market. Figure 1 provides an example of colour modification in flowers of transgenic D. caryophyllus. The keys genes of the anthocyanin (Nishihara and Nakatsuka, 2011; Tanaka et al., 2010), flavonoid (Ono et al., 2006; Togami et al., 2011) and carotenoid (Cazzonelli and Pogson, 2010; Sandmann et al., 2006) biosynthesis and metabolism pathways have been identified, allowing modification of flower colour in many ways. Transcription factors regulating the anthocyanin pathway have also been identified (Century et al., 2008) and as more is learned of the spatial regulation of flavonoid biosynthesis, opportunities will arise for the modification of pigmentation patterns in plants (Hichri et al., 2011) and for GM with transcription factors for up- and down-regulation of pigment biosynthesis pathways (Han et al., 2009).

image

Figure 1.  Colour modification in Dianthus caryophyllus (carnation). Flowers are shown from a control plant (right) and from a transgenic plant (left) expressing the flavonoid 3′5′-hydroxylase gene from Viola tricolor (pansy).

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Genetic modification of flower colour has been extensively reviewed recently (Chandler and Brugliera, 2011; Nishihara and Nakatsuka, 2010, 2011; Rosati and Simoneau, 2008; Tanaka and Ohmiya, 2008; Tanaka et al., 2009, 2010) These reviews also address efforts to modify colour through manipulation of co-pigments, vacuole acidity and metal ion transportation.

Research on colour modification continues, and manipulation of anthocyanin and carotenoid concentration and types has recently been demonstrated in several transgenic plants (Table 2). Modification of carotenoid biosynthesis in transgenic Lilium X formolongi (lily) lead to the isolation of some strongly orange coloured calli and plantlets, which later reverted to a greener colour, despite the high levels of carotenoids that persisted in the transgenics (Azadi et al., 2010). This illustrates the complexity of the regulation of carotenoid biosynthesis and metabolism.

Table 2.   Recent examples of flower colour modification using GM
SpeciesColour changeCitation
  1. GM, genetic modification.

Cyclamen persicum (cyclamen)Purple to red/pink Boase et al. (2010)
Gentiana triflora (Japanese gentian)Blue to white Nakatsuka et al. (2010, 2011)
Lotus japonicus Light yellow to Yellow/orange Suzuki et al. (2007)
Phalaenopsis spp. (phalaenopsis)Pink to light pink Chen et al. (2011)
Torenia × hybrida (torenia)Blue/Violet to pink Nakamura et al. (2010)
Tricyrtis spp. (toad lily)Red to white Kamiishi et al. (2011)

Commercialized products

The two GM ornamental plants that are on the market have colour modified flowers, and both have been developed by Florigene Pty. Ltd./Suntory Ltd. (Dobres, 2011). The product range comprises eight varieties of transgenic D. caryophyllus and one variety of R. × hybrida. The colour modification is the result of manipulation of the anthocyanin biosynthetic pathway (for details see Tanaka et al., 2009, 2010). In nature, D. caryophyllus and R. × hybrida do not contain delphinidin-derived anthocyanins, due to absence of flavonoid 3′5′-hydroxylase (Holton et al., 1993). Introduction of this gene from Petunia × hybrida (petunia) or Viola tricolor (pansy), in conjunction with other modifications to the endogenous anthocyanin biosynthesis pathway (to minimize substrate competition) results in accumulation of delphinidin-related anthocyanins in flowers, conferring a unique colour (Figure 1). GM D. caryophyllus products were first marketed in Australia in 1997 and are now grown in South America, Australia and Japan. Exported cut flowers are primarily sold in North America, but also in Europe and Japan. Figure 2 shows commercial production of colour-modified GM D. caryophyllus and R. × hybrida in South America.

image

Figure 2.  Colour-modified genetically modified (GM) Dianthus caryophyllus (carnation) and Rosa × hybrida (rose) in South America. Plates show annual selection of GM carnation (1), commerical planting of GM carnation (2,4) and rose (3), post-harvest processing of different GM carnation varieties (5) and post-harvest quality control of carnation (6).

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Fragrance modification

Key genes related to the production (Colquhoun et al., 2010; Guterman et al., 2002) and regulation (Spitzer-Rimon et al., 2010) of fragrance have been identified and this presents, conceptually at least, the possibility of transferring fragrance from one species to another. The introduction of fragrance without impacting the post-harvest quality and productivity of an ornamental could well result in viable new products because some very desirable fragrances occur in only a limited number of species (Potera, 2007) and because some important cut flowers are devoid of fragrance altogether, probably because of the selection for good vase life by breeders (Gudin, 2010). Fragrance is also important in certain pot and bedding plants, and there is an example where potentially improved products have been obtained after the transformation process (Saxena et al., 2007). The potential for fragrance modification in ornamentals has been reviewed by several authors (Dudareva and Pichersky, 2008; Dudareva et al., 2006; Underwood and Clarke, 2011; Yu and Utsumi, 2009).

Abiotic stress resistance

For growers and consumers of ornamental plants, heat, light intensity, humidity and frost have an impact on the ability to produce a marketable product on schedule. Research on GM for improved abiotic stress resistance is being explored for pot plants by Ornamental Biosciences (Stuttgart, Germany) (Potera, 2007), utilizing genes known to be involved in drought tolerance. Frost tolerance in Petunia × hybrida (petunia) may be increased by transfer of the CBF3 gene from Arabidopsis thaliana (arabidopsis; Warner, 2011) and this would potentially increase the range of environments in which this bedding plant could be grown.

Disease resistance

Fungal, bacterial and viral pathogens can have a devastating effect on ornamentals during production, storage, distribution and end-consumer use. Some ornamentals have no or very low natural resistance to some of the pathogens commonly encountered in production and distribution, and their control through chemical treatment is a significant cost for producers. Control, or the lack of it, is either a cost or nuisance to the consumer and home gardener. Disease is also a problem in food crops, and as research efforts to improve disease resistance in the major crops progresses, it can be expected that useful genes will also be tested in ornamentals (Hammond et al., 2006; Hsiao et al., 2011). Rosa × hybrida has been genetically modified for mildew resistance (Li et al., 2003), and caffeine production in transgenic Dendranthema grandiflorum (chrysanthemum) was shown to confer resistance to grey mould (Kim et al., 2011b). Clarke et al. (2008) reported GM virus resistant lines of the pot plant Euphorbia pulcherrima (poinsettia) and Chang et al. (2005) and Liao et al. (2004) reported virus resistant GM lines of the pot and cut flower orchids Phalaenopsis spp. and Dendrobium spp.

The expectations for a disease resistance phenotype in an ornamental plant are far greater than for a crop plant. This is because any symptoms of disease make an ornamental product either unmarketable to the discerning consumer, or unacceptable for export due to zero tolerance during phytosanitary inspection. Therefore, whether or not the disease resistance level achieved will match that possible by chemical treatment will determine if it is worthwhile developing GM varieties. A partial resistance phenotype could be offset to some extent by reduced chemical and application costs, or the fact that fewer chemicals are released into the environment. The latter benefit is a significant issue as government policies compelling growers to stop using some chemicals on ornamentals reduces chemical treatment options for disease control (Lutken et al., 2010).

Pest resistance

Both commercial and amateur growers face a continuous threat of insect infestation when growing ornamentals. Populations of aphids, thrips, leaf miners, caterpillars, moths, spider mites and other pests can explode in the nursery and greenhouse, where plants are at their optimal attractiveness to an insect pest (Gatehouse, 2008). In the garden, untended plants will soon succumb to pests. Pests not only reduce the attractiveness and marketability of foliage and flowers but are potential vectors of pathogens and viruses. The insect resistance genes currently utilized in GM food crops are primarily based on the cry endotoxin genes from Bacillus thuringensis. Though these are effective against a relatively narrow range of pests, tolerance to susceptible insects has been demonstrated in transgenic plants of D. grandiflorum carrying the cry1Ab of Bacillus thuringiensis var. kurstaki HD-1 (Shinoyama and Mochizuki, 2006). The demonstration of aphid resistance in D. grandiflorum modified to produce caffeine (Kim et al., 2011a) is a recent significant development.

As for disease resistance, the ‘phenotype expectation’ for an insect resistant GM ornamental variety will be high. This is because even minor symptoms of insect damage can make ornamental products unacceptable for export.

Vase life and ‘keeping’ quality

Underwood and Clarke (2011) have recently reviewed the potential for GM to improve leaf and flower longevity in transgenic ornamental crops. In cut flowers, long vase life is a critical characteristic and is selected for during breeding. Most cut flowers are also chemically treated by producers to optimize vase life. As cut flowers must have the capacity to survive several weeks in the distribution chain before they reach consumers’ hands, resistance of flowers to senescence promoting factors such as ethylene and bacterial infection is very important. Efforts by several groups to use GM to improve vase life in D. caryophyllus (carnation) were technically very successful, to the extent that the transgenic varieties no longer required treatment with chemical preservatives (Chandler, 2007). Enhanced vase life could be obtained by the introduction of resistance to ethylene or by the inhibition of expression of endogenous ethylene biosynthesis genes. Introduction of a mutated ethylene receptor gene also reduced ethylene sensitivity in the orchids Oncidium spp. and Odontoglossum spp. (Raffeiner et al., 2009).

Post-harvest longevity of flowering pot plants is also important (Potera, 2007) and there are ethylene sensitive pot plant species which have been genetically modified for reduced ethylene sensitivity (Milbus et al., 2009; Sanikhani et al., 2008).

Leaf yellowing is a negative attribute in both cut flowers and pot plants and GM technology to inhibit leaf senescence, such as demonstrated in D. grandiflorum (Satoh et al., 2008) is potentially very useful.

In petunia plants transformed with the etr1-1gene delayed senescence was also accompanied by a commercially unacceptable reduction in rooting of cuttings (Gubrium et al., 2000). This observation emphasizes the need for tissue specific expression of genes affecting processes of central importance to a plant, such as ethylene perception.

Other possible applications of GM

Other improvements to ornamental plants could be possible through GM. These include manipulation of the form and architecture of plants and/or flowers (Aida et al., 2008; Khodakovskaya et al., 2009; Lutken et al., 2011; Meng et al., 2009; Narumi et al., 2008; Sun et al., 2011; Thiruvengadam and Yang, 2009), modification of response to day length (Franklin and Whitelam, 2006; Shulga et al., 2009), modification of flowering time (Hsiao et al., 2011; Shulga et al., 2011) or introduction of herbicide tolerance (Harriman et al., 2006). As an example in a cut flower, transgenic plants of Gypsophila paniculata (baby’s breath) exhibited increased lateral branch and bud formation when transformed with the rol C gene (Zvi et al.,2008b). Growth regulators are used in several types of pot plants to prevent stem elongation. Kalanchoe spp. is one such product and Lutken et al. (2010) produced compact plants by transformation with a GA biosynthesis inhibition gene or with rol genes (Christensen et al., 2008). Utilization of homeotic genes regulating flower development (Shikata and Ohme-Takagi, 2008) may be particularly interesting in ornamental flower crops in which flower morphology variation can be marketable. GM Cyclamen spp. was produced by suppression of floral-organ identity genes (Ohtsubo, 2011) as part of a research effort in a transcription factor-based gene silencing system (the Flower CRES-T Project).

Morandini et al. (2011) have recently reviewed the use of non-food plants for the production of pharmaceuticals. There is potential for ornamentals to be used in this way, as some plants are produced on a large scale in relatively intensively managed facilities and conditions.

Pipeline

A reasonable measure of the pipeline of GM ornamentals is the current situation with trial releases. That analysis suggests that commercialisation of GM horticultural crops significantly lags development in food crops (Sexton and Zilberman, 2011; Strauss, 2011). In Japan, release of ornamentals is restricted to colour-modified D. caryophyllus (carnation) and R. × hybrida (rose) though according to Ohtsubo (2011)Cyclamen spp. (cyclamen) with complete sterility will be released in the near future. In the EU, only colour-modified D. caryophyllus varieties have been released under the European directives bought into place since 2002. More activity with GM ornamentals has occurred in the USA. Dobres (2008) analysed the permits issued from 1985 through the US system regulating GMOs (genetically modified organisms). Excluding permits for turf grass species, he identified six potted/foliage plants, six bedding plant species and two shrub plant species for which permits had been issued. In the last 3 years, permits have been issued for Castanea dentata (American chestnut), Ulmus americana (American elm), Anthurium spp., Populus spp., Ipomoea quamoclit (cypress vine), Lilium longiflorum (Easter lily), Iris graminea (iris), Calendula officinalis (marigold), Petunia × hybrida (petunia), R. × hybrida and Liquidambar styraciflua (sweetgum). However, again aside from turf grasses, colour-modified R. × hybrida is the only non-food GM ornamental in the USA to so far have been determined to have non-regulated status after petition (http://www.aphis.usda.gov/biotechnology/not_reg.html). The registry of Living Modified Organisms (LMOs) held by the Biosafety Clearing house (Mackenzie et al., 2006) lists the following ornamental LMOs; colour- modified D. caryophyllus, colour-modified R. × hybrida and D. caryophyllus modified for improved vase life.

Hurdles to commercialisation

  1. Top of page
  2. Summary
  3. Introduction
  4. Genetically modified ornamentals; pipeline and products
  5. Hurdles to commercialisation
  6. The regulatory environment
  7. Looking ahead
  8. Acknowledgements
  9. References

Rommens (2010) has defined barriers to market entry as a means to explain the disparity between the amount of development on GM plants at the research level and what is actually in the marketplace. Though that analysis was directed at transgenic crops, these potential barriers, or hurdles, also encapsulate the main issues in relation to the potential commercialization of a GM ornamental product. Barriers to commercialization have also been identified by Dobres (2011), Sexton and Zilberman (2011) and Strauss (2011).

Selection of products

In reality, given the cost of research and development GM programs will only be applied to those ornamental crops which currently dominate the marketplace. In the case of cut flowers, this means the most widely grown cut flower species. Rose is the most widely grown cut flower globally, but carnation, chrysanthemum, tulip, gerbera, lily and gypsophila are also important (Table 1). In pot and bedding plants geranium, petunia, begonia and orchids are all reasonable targets for GM. A long-term strategy is to use transgenic breeding lines to introduce useful traits into a wider range of varieties, and this could be most suited for producer traits such as disease resistance, insect resistance and vase life.

Intellectual property and freedom to operate

Though it is correct that freedom to operate requirements unique to genetically modified plants do impose additional cost to developers (Dobres, 2008; Sexton and Zilberman, 2011), in our experience the impact is not necessarily significant. This is because holders of intellectual property rights may understand that upfront payments, if any, should be proportional to the potential market for the new products and should not be so high as to deter investment in research and development. After a product has been successfully commercialized royalties may also be required, but breeder royalties are common in the ornamental industry and it can again be expected that a reasonable fee will be negotiated so as to maximize market potential. The negotiation process is not necessarily straightforward and can be complicated by difficulty in accessing the right contact people in large organizations, or dealing with multiple parties.

Identity preservation

In GM varieties of crop plants identity preservation and the related stewardship procedures are becoming more critical as various export markets move to strengthen zero tolerance for unapproved transgenic events (Davison, 2010), or a zero or minimal tolerance for the presence of adventitious GM events in organic or non-genetically modified seed lots (Areal et al., 2011). In the major crop plants, such preservation brings with it additional cost and resistance to this cost from some parts of the food supply chain (Sexton and Zilberman, 2011). In the case of GM ornamentals, identity preservation (if required) is unlikely to be a significant obstacle to commercialization. One reason for this is that identity preservation is an inherent part of trade in ornamentals already. As ornamentals are often vegetatively propagated, and are grown over small areas in discrete, often contained facilities, segregation is straightforward. A grower of a particular cut flower or pot plant species grows many varieties and must ensure these are managed by variety to meet specific customer orders. This is the case for the colour modified D. caryophyllus, where eight different varieties are grown side by side at the same grower in Colombia (Figure 2). The segregation is enforced by the way ornamental product is normally distributed. In cut flowers for example, flowers are distributed in boxes which are labelled to the extent that every box, and every bunch within the box, is identified by variety.

A second reason identity preservation is unlikely to be a significant obstacle to developing a GM ornamental product is that in the market variety identification is necessary to the customer and is also actively pursued as part of the marketing strategy.

In the case of the GM D. caryophyllus and GM R. × hybrida there have been no measures introduced, or requested to be introduced, to ensure that the GM flowers are segregated from other products or that the flowers should be distributed through a segregated distribution system.

It is impractical to be able to guarantee that any labelling and identity preservation will be carried through to the end-consumer. In the case of cut flowers, packaging and labels are usually removed by the florist as they make arrangements, and for pot plants, labels may be discarded once plants are planted or passed on as gifts.

Acceptance in the marketplace

Where surveys are available the public perception of GM ornamental plants is generally as or more positive than the perception toward foods derived from GM plants (Biotechnology Australia, 2007; Kikuchi et al., 2008). Anecdotal and industry opinion also suggests the public is less concerned over genetically modified ornamentals than over GM food (Dobres, 2008; Potera, 2007). In Australia, there was less awareness of the potential application of GM to non-food crops, but 70% of respondents felt such applications could be useful, and were just as acceptable as applications in food crops (Biotechnology Australia, 2007).

So far, the only test of acceptance in the marketplace has been the colour modified D. caryophyllus and R. × hybrida, and in the case of these products there has been no resistance to introduction into the marketplace, and relatively little media and nongovernmental organization interest. No legal challenges have been made to authorizations, and the industry (wholesalers and florists) has not embarked on any actions to remove genetically modified cut flowers from the marketplace. Klingeman and Babbit (2006) undertook a survey of master gardeners in Tennessee to determine attitudes to a number of modifications in GM ornamentals, including colour modification. At the time of the survey the GM D. caryophyllus had been on the market in the US for 3 years, and the majority of responders stated they were likely or very likely to buy GM ornamentals. The most positive response was to possible improvement of disease or insect resistance. One conclusion of the survey carried out by Klingeman and Babbit (2006) was that voluntary labelling of GM ornamentals was desired by consumers and would be a positive marketing approach. Ohtsubo (2011), from the experience in Japan, has also emphasized the importance of public education and information sharing.

Use of GM technology to generate disease and pest resistance in some of the more popular home grown plants has been suggested by some as likely to be well received by the public, as there is already a demand for such varieties (Dobres, 2011) and the benefits can be clearly seen by the end consumer (Klingeman and Hall, 2006).

The experience with the GM D. caryophyllus does not tally with the opinion (Auer, 2008; Debener and Winkelmann, 2010) that introduced GM plants must have benefits beyond novel phenotype to be accepted by the public. This is not to say GM ornamentals may not be accepted by some sectors of the market. There may be suppliers who, in response to demand from distributors and retailers for 100% freedom from any type of GMO, will not carry GM ornamentals. Campaigns against GM ornamental products may also be of concern to breeders and growers with an existing range of conventionally bred varieties.

Regulation

Other articles have eloquently examined the reasons why genetically modified organisms, including plants, are tightly regulated around the world (Strauss, 2011). In many countries, regulations have been drawn up in line with the guidelines and directives of the Cartagena protocol (Mackenzie et al., 2006). Whereas a breeder of a promising new ornamental variety may normally quickly plant trials in several different countries to evaluate commercial potential, for a genetically modified plant this is not possible without regulatory approval (Dobres, 2011; Underwood and Clarke, 2011). This barrier is a major constraint to developing new GM varieties. Regulations exist in all the major markets for ornamental production and/or sale and our experience leads us to agree with the view of others (Strauss, 2011) that regulatory approval is the biggest hurdle to the introduction of a new GM ornamental.

The process of obtaining regulatory approval for a commercial GM product takes several years. This is a problem for a research program developing new products from a pipeline. If the pipeline is generating new products on a 3–5 year cycle, new products may be generated before regulatory approval is granted for their predecessors. This means regulatory cost is spent on a product which will soon be replaced, and that this will be a continual process.

The regulatory environment

  1. Top of page
  2. Summary
  3. Introduction
  4. Genetically modified ornamentals; pipeline and products
  5. Hurdles to commercialisation
  6. The regulatory environment
  7. Looking ahead
  8. Acknowledgements
  9. References

A pertinent and comprehensive review of risk assessment and regulation as applied to genetically modified ornamentals has been published by Auer (2008). The requirements for most transgenic ornamentals are, aside from the need for food safety assessments, generally similar to those for food crops. In most regimes, trials, or a series of trials, are necessary to secure authorization (Dobres, 2011). A trial of a GM ornamental is not the same as a field trial of a crop plant, where many large scale outdoor trials are usually required to properly measure the effectiveness and expression of the introduced gene and possible impacts on the environment and non-target organisms. In an ornamental, the phenotype change may be qualitative (such as a change in flower colour or absence of disease symptoms) the crop itself will normally be produced over a small area (possibly in a greenhouse anyway) and under conditions where insect and pathogen control is normally strictly adhered to. Therefore, fewer trials can be established to meet the obligations of the regulatory procedure and can usually be integrated with the trials used for product development. There are of course cases where more extensive assessment will be required. For example, where there is a potential for out-crossing to weed species, or when a perennial ornamental will be grown outdoors, and this is discussed later in this review. In our own trials we have always grown putative transgenic lines next to the parental lines used for transformation, to ensure that no performance characteristics have been negatively impacted during transformation (Shinoyama et al., 2008). Regulation is applied to ornamental plants at the national and international level, and ornamental plants fall under the same legislative constraints, such as bans and GM-free zones, as other GM plants. Dobres (2011) provides an overview of the regulatory process as implemented by those areas and countries representing the major production and consumption centres for ornamentals.

Plants which have been generated by mutagenesis or somaclonal variation are not subject to the same regulatory scrutiny as transgenic plants. Variant plants can be generated from transgenic ornamental plants subjected to mutagenesis treatment (Sasaki et al., 2008). Whether these variants, or variants produced from a transgenic line by natural mutation, would be subject to separate regulatory approval processes depends on the specific wording of legislation regulating GMOs.

Environmental risk assessment and GM ornamentals

Although ornamentals are not grown over as wide an area as field crops, and are often grown under closely managed conditions, some ornamental species have become environmental pests because of their invasive nature (Anderson, 2007; Dehnen-Schmutz et al., 2007; Strauss, 2011). Humans have spread ornamental species across the globe and careless use has resulted in some plants quickly adapting to new environments and out competing native species (Dehnen-Schmutz et al., 2007). In the case of a GM ornamental, an important question is therefore whether there is any difference in the invasive potential of the GM variety compared to non-GM varieties of the same species. As Auer (2008) has summarized there are ornamental species in North America where gene flow from non-native species has already occurred, including the genera Rosa, Quercus and Rhododendron. Rosa × hybrida is an important cut-flower, shrub and pot plant and potential cross-compatibility to naturally occurring wild Rosa populations may be of particular concern in some parts of the world (Debener and Winkelmann, 2010). An interesting observation in transgenic R. × hybrida has therefore been that some transgenic lines are genetic chimeras and the transgene cannot be transmitted in the pollen (Nakamura et al., 2011b).

Dendranthema grandiflorum is a very important ornamental for the Asian marketplace, but Asia is geographically also the centre of biodiversity for the genus Dendranthema. Shinoyama et al. (2012) were able to produce transgenic lines of D. grandiflorum with reduced male sterility by transformation with the ethylene receptor gene and suggested this could be a way to increase the acceptability of GM varieties of this species in the eyes of regulators. Utilizing a GM approach for minimizing gene flow (Shinoyama et al., 2008) relies of course on complete expression of sterility under all possible growing conditions. The possibility of plastid transformation, as has been demonstrated in Petunia × hybrida (Zubko et al., 2004) may also be considered one route to minimize gene flow. The release of genetically modified trees for ornamental purposes presents unique regulatory issues, in terms of the assessment of risk and monitoring over very long time frames (Kikuchi et al., 2008).

Though the amount of bench line information for many ornamentals is lower than for food crops, there is a good case for reducing the regulatory scrutiny of plants with certain characteristics, many of which are exhibited by ornamentals. For example, plants which are vegetatively propagated, or which are completely sterile (Dobres, 2011). In our experience, a history of safe use is not adequately included in the risk assessment process. Some of the colour modified D. caryophyllus varieties have now been commercially available for more than 12 years, and have a proven history of safe use. However, these varieties cannot be sold in Europe or Japan because of the cost constraint associated with the need for a detailed technical dossier for each event. In GM D. caryophyllus, there are also examples of varieties that were previously sold in Europe with no negative impact that had to be withdrawn from the marketplace due to the difficulty of providing molecular characterization data not required when the varieties were first approved.

Rosa × hybrida and Dianthus caryophyllus

Our direct experience has been in obtaining regulatory approval for commercial release of two ornamental species, rose and carnation. Nakamura et al. (2011a,b) have provided an overview of the regulatory work that was carried out in Japan on the colour-modified R. × hybrida (Katsumoto et al., 2007). Details of the regulatory process as applied to D. caryophyllus is contained in Auer (2008), EFSA (2006, 2008), Kikuchi et al. (2008) and Terdich and Chandler (2009). Our experience has been that the regulatory process varies significantly in time and complexity, depending on the country of application. For the EU and Japan, which require a detailed molecular characterization, the complexity of insertion patterns in certain events excludes them from the regulatory process, by our choice. Some commercial varieties are therefore only available in some parts of the global marketplace. The most critical lesson has therefore been to screen potential commercial events at an early stage of the product development process.

International harmonization

Aside from the provisions that allow for the nomenclature of transgenic events, there is relatively little harmonization in the international sphere. By harmonization, we mean a mechanism by which regulatory decisions made by other countries can be adopted without the need for further assessment processes. This lack of harmonization has been recognized as hampering development of new varieties using GM (Durham et al., 2011; Ramessar et al., 2009; Strauss, 2011). Some large economies for ornamental products (notably the USA) have not signed the Cartagena protocol, limiting the prospects for harmonization (Mackenzie et al., 2006).

Although ornamentals are produced for the domestic market, there is also a significant intra- and inter-country trade in ornamental products, including tubers and bulbs, graft wood, cuttings, seedlings, established plants, shrubs and cut flowers. For some sectors, trade has become the dominant part of the industry. Examples include bulb growers in the Netherlands who export bulbs World Wide (Benschop et al., 2010) and the shift of cut flower production to South America and Africa. The vast majority of cut flowers consumed in North America are now largely imported on a daily basis from Colombia and Ecuador. On account of this trade, the harmonization of regulatory approval would be a great advantage to developers of minor ornamental crops (Alston et al., 2006; Strauss, 2011). In widely traded ornamental species, lack of synchrony in the regulatory process leads to the possibility of unapproved events reaching markets where regulatory approval has not been obtained (Stein and Rodriguez-Cerezo, 2010). Though the GM D. caryophyllus and GM R. × hybrida have been approved for full commercial use in Colombia, Japan, Australia and the USA, and GM D. caryophyllus has been grown for years, the requirements for molecular analysis make it economically infeasible to commercialise some varieties in the EU, even for import of cut flowers.

In some countries, if a particular phenotype or construct is approved in a species then a phenotype-based risk assessment is applied, and no further review is required for new events with that phenotype. Global harmonization of this policy would very significantly reduce the cost of regulation of GM ornamentals.

Post-release monitoring

Post-release monitoring as part of regulatory approval compliance is an important consideration in the development of a GM plant product. In Europe, post-release monitoring is mandatory and an annual reporting mechanism is required. For an ornamental product which is likely to be sold widely to the consumer (for example to home gardeners), precise monitoring is an impractical and potentially prohibitively expensive option, and a general monitoring protocol has to be employed. The purpose of monitoring is to provide information on potential unintended effects, such as establishment of volunteer populations, introgression with wild or cultivated species and varieties or changes to agricultural practices relating to chemical use. Throughout the world there are ornamental gardens and individual plants which are centuries old. Any commitments to monitoring based on the expected longevity of an ornamental GMO must therefore be a consideration in the product development phase.

The cost of regulation

Unlike costs associated with freedom to operate, costs associated with regulatory approval are largely borne before a product can be tested in the marketplace (Sexton and Zilberman, 2011). In addition, in the ornamental market regulatory cost is a significant relative cost because the marketplace is extremely diverse—even within a single species there may be thousands of varieties available (Dobres, 2008, 2011). Because of these two considerations, a new genetically modified variety must therefore have a good chance of becoming a ‘block-buster’ if regulatory costs are to be justified (Dobres, 2011). Where breeding is not an option, generation of multiple transgenic events to create a product range can impose a burdensome regulatory cost (Sexton and Zilberman, 2011).

Several authors have estimated the cost of regulatory approval for a transgenic event of a major crop plant in the millions of dollars (Alston et al., 2006; Bayer et al., 2010). This type of cost does not apply to an ornamental (for example no food safety tests are required). Nevertheless, there is still a significant cost, potentially running to hundreds of thousands of dollars per event (Potera, 2007). Dobres (2008) provides a detailed breakdown of costs, concluding that 1 million USD would be required for a hypothetical regulatory package to the US in which the regulatory authorities (USDA and EPA) required assessment over several years. In our experience, the majority of regulatory cost is associated with requirements for molecular analysis (Bayer et al., 2010; Kalaitzandonakes et al., 2007). Although some authorities simply require a transformation vector map, Southern blots, and minimal expression analysis there is no leeway in European legislation, which requires the same detail of molecular analysis for an ornamental as for a major food crop. This will require the complete sequence, including flanking areas, of every insert in each event and the provision of an independently verified PCR-based identification test unique for each event. In Europe, the applicant also incurs a significant fee for assessment and verification of this unique identification test. Unique ID protocols are not required in all countries and for GM ornamentals consideration could be given to the fact that ornamental varieties can be protected by Plant Breeders Rights (Dobres, 2011), a process by which detailed morphological descriptions, supplemented by Southern blots can be used to precisely identify varieties.

The cost of securing regulatory approval is not only associated with the provision of information on selected events, but the associated indirect costs that are incurred whilst managing product development. For example, in the development of the transgenic products it is necessary to select for, or develop strategies for, (Oltmanns et al., 2010; Ye et al., 2011) generation of simple integration events. As well as the cost of dossier preparation other regulatory costs include physical separation requirements imposed by regulators (though these may be impractical or unnecessary), documentation and inspection requirements during trials, waste disposal and staff training.

As stated earlier, the cost of regulation could be reduced for non-food ornamentals if assessment could be internationally uniformly based on phenotype rather than event (Alston et al., 2006; Sexton and Zilberman, 2011). In the case of the colour modified GM D. caryophyllus, all the events that have been commercialised to date have the same selectable marker, the same environmental impact and the same altered phenotype (production of delphinidin-related anthocyanins). It is a significant redundancy in both applicant’s and regulator’s time that some authorities require that every time this phenotype is generated in a new background a complete analysis of each event is produced and essentially the same environmental risk assessment presented.

As previously mentioned in this review, genetically modified D. caryophyllus with improved vase life has been developed in several laboratories, but these varieties have never been commercialised (Chandler, 2007). A colour modified Torenia × hybrida was developed and this also has not been commercialised (Tanaka et al., 2010). In both these cases the cost of obtaining regulatory approval was the major factor in not proceeding to commercialisation.

Regulatory requirements for exported cut flowers

There are a number of reasons why imported genetically modified cut flowers should not be subject to the same regulatory scrutiny as would be imposed if the same product were to be grown. In some countries (not all) this is the case for D. caryophyllus and R. × hybrida. It does not make sense to impose the same regulatory requirements on imports as local production because the gene flow risk, if any, is greater at production sites and it is there that intensity of handling and human contact is also greatest.

Molecular characterization

Where it is required by the authority, a considerable part of the cost of obtaining regulatory approval is likely to be molecular characterization. If a cut flower product has a low inherent risk of allergenicity then general information about the modification, such as transformation vector map, Southern analysis, northern (RNA) analysis and proof of absence of extra border integration should be adequate for evaluation of imported GM cut flowers. A complete analysis of each insert may be irrelevant (EFSA, 2009). Florigene has analysed seven colour modifed GM D. caryophyllus lines with seventeen integration loci and were unable to identify open reading frames generated at integration sites. Genome sequence differences between cultivars generated using classical breeding techniques can be greater than between a transgenic line and parent organism (Batista et al., 2008; Morris and Spillane, 2008; Ricroch et al., 2011).

If certain criteria are met then there is adequate ‘case-by-case’ provision in most legislation (EFSA, 2009) for reducing molecular analysis.

Looking ahead

  1. Top of page
  2. Summary
  3. Introduction
  4. Genetically modified ornamentals; pipeline and products
  5. Hurdles to commercialisation
  6. The regulatory environment
  7. Looking ahead
  8. Acknowledgements
  9. References

Commercialisation of GM food and industrial crops will continue to outpace horticulture (Sexton and Zilberman, 2011) and there will probably continue to be just a trickle of new GM ornamentals reaching the marketplace. These are likely to be colour modified cut flowers. Some years ago Dunwell (1999) predicted that GM ornamentals would be widespread by 2020. This does not appear to be likely to eventuate, and put simply the high cost of securing regulatory approval makes the development of genetically modified ornamentals challenging, or, to quote Dobres (2008), ‘unattractive from a business perspective’. Unless the cost of regulatory approval can be reduced, breeders of ornamental plants will continue to shy away from GM techniques to develop new varieties (Dobres, 2011) due to the fragmented nature of the market (Harriman et al., 2006) limiting the capacity for new products to recover costs via sales (Miller and Bradford, 2010; Sexton and Zilberman, 2011).

In the USA recent developments impacting transgenic lines of geranium, petunia and Poa pratensis (Kentucky bluegrass) have suggested that the regulatory process can be shortened by use of ‘non-plant pest’ genetic components in transformation vectors (Waltz, 2011). The potential of this development to reduce regulatory costs in an ornamental is a moot point (Waltz, 2011), and it will depend on whether the US is the sole market of interest. For example, as most cut-flowers are exported, the regulatory process will need to be carried out to meet the legislative requirements of both the exporting and the importing countries.

If the costs of regulatory approval can be reduced, there are numerous opportunities for GM ornamentals in the marketplace. Dobrare selected (Underwood and Clarke, 2011), the possibility emerges of developing transgenic ornamentals with more than one trait, such as altered scent and altered colour (Zvi et al., 2008a). This could be achieved through use of complex transformation vectors, transformation with two different selectable markers, or where possible, breeding with different transgenic lines.

Although it is naive to think that the current legislation around the world can be readily modified to meet the needs of the GM ornamental industry, some countries need to modify policies or legislation if the bottleneck to commercialisation is to be widened (Dobres, 2011; Strauss, 2011). For example, other authors have suggested new models for regulation and international harmonization including ‘fast track’ (Durham et al., 2011), and these initiatives should be supported for regulation of GM ornamentals. It would help accelerate the commercialisation process if all countries could allow regulation on the basis of phenotype, not process (Sexton and Zilberman, 2011). In practical terms, reduced regulatory cost could be achieved by international harmonization, increased flexibility for environmental risk assessment and reduced requirements for molecular characterization.

As the European regulatory environment provides a greater barrier to the development and commercialisation of genetically modified ornamentals it is likely to be the case that innovation with GM ornamentals will be most advanced in other parts of the globe, particularly North America. Although there are some voices calling for more relaxed regulations in Europe (Drobnik, 2008; Durham et al., 2011) there are no signs of legislative change in the near future. This is a pity, as Europe remains the largest market for ornamentals and it is the home of some of the largest and longest established flower and pot plant breeders.

Footnotes
  • 1

    In this review we have adopted the convention of the use of × hybrida for hybrids of uncertain botanical origin.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Genetically modified ornamentals; pipeline and products
  5. Hurdles to commercialisation
  6. The regulatory environment
  7. Looking ahead
  8. Acknowledgements
  9. References

In compiling this review, our thoughts turn to the dozens of colleagues who have passed through the laboratories and greenhouses of Florigene Pty. Ltd. and Suntory Ltd. We acknowledge each and every one of them for their contribution and thank Dr. Yoshi Tanaka for his critical review of this manuscript. Our special thoughts go to the family of the late Dr Michael Dalling, who tragically passed away in 2010. Mike was a major driving force behind the development and eventual commercialization of the worlds first genetically modified flowers and he is sorely missed.

Both authors have financial interests in Florigene Pty. Ltd. and Suntory Ltd.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Genetically modified ornamentals; pipeline and products
  5. Hurdles to commercialisation
  6. The regulatory environment
  7. Looking ahead
  8. Acknowledgements
  9. References
  • Aida, R., Komano, M., Saito, M., Nakase, K. and Murai, K. (2008) Chrysanthemum flower shape modification by suppression of Chrysanthemum-AGAMOUS gene. Plant Biotechnol. 25, 5559.
  • Alston, J.M., Bradford, K.J. and Kalaitzandonakes, N. (2006) The economics of horticultural biotechnology. J. Crop Improvement 18, 413431.
  • Anderson, N.O. (2007) Prevention of invasiveness in floricultural crops. In Flower Breeding and Genetics (Anderson, N.O., ed), pp. 177214. Dordrecht: Springer.
  • Areal, F., Riesgo, L. and Rodriguez-Cerezo, E. (2011) Attitudes of European farmers towards GM crop adoption. Plant Biotechnol. J. 9, 945957.
  • Auer, C. (2008) Ecological risk assessment and regulation for genetically-modified ornamental plants. Crit. Rev. Plant Sci. 27, 255271.
  • Azadi, P., Otang, N.V., Chin, D.P., Nakamura, I., Fujisawa, M., Harada, H., Misawa, N. and Mii, M. (2010) Metabolic engineering of Lilium × formolongi using multiple genes of the carotenoid biosynthesis pathway. Plant Biotechnol. Rep. 4, 269280.
  • Batista, R., Saibo, N., Lourenco, T. and Oliveira, M.M. (2008) Microarray analyses reveal that plant mutagenesis may induce more transcriptomic changes than transgene insertion. Proc. Natl Acad. Sci. USA, 105, 36403645.
  • Bayer, J.C., Norton, G.W. and Falck-Zepeda, J.B. (2010) Cost of compliance with biotechnology regulation in the Philippines: implications for developing countries. AgBioForum 13, 5362.
  • Benschop, M., Kamenetsky, R., Nard, M.L., Okubo, H. and De Hertogh, A. (2010) The Global flower bulb industry: production, utilisation, research. Hortic Rev. 36, 1115.
  • Biotechnology Australia (2007) Community attitudes to biotechnology; report on overall perceptions of Biotechnology and general applications. Eureka Strategic Research Eureka Project 4001.
  • Boase, M.R., Lewis, D.H., Davies, K.M., Marshall, G.B., Patel, D., Schwinn, K.E. and Deroles, S.C. (2010) Isolation and antisense suppression of flavonoid 3′, 5′-hydroxylase modifies flower pigments and colour in cyclamen. BMC Plant Biol. 10, 107.
  • Brand, H. (2006) Ornamental plant transformation. J. Crop Improvement, 17, 2750.
  • Cazzonelli, C.I. and Pogson, B.J. (2010) Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci. 15, 266274.
  • Century, K., Eeuber, T.L. and Ratcliffe, O.J. (2008) Regulating the regulators: the future prospects for transcription-factor-based agricultural biotechnology products. Plant Physiol. 147, 2029.
  • Chandler, S. (2007) Practical lessons in the commercialisation of genetically modified plants – long vase life carnation. Acta Hortic. 764, 7182.
  • Chandler, S. and Brugliera, F. (2011) Biotechnology in floriculture. Biotechnol Lett. 33, 207214.
  • Chang, C., Chen, Y.-C., Hsu, Y.-H., Wu, J.-T., Hu, C.-C., Chang, W.-C. and Lin, N.-S. (2005) Transgenic resistance to Cymbidium mosaic virus in Dendrobium expressing the viral capsid protein gene. Transgenic Res. 14, 4146.
  • Chen, W.-H., Hsu, C.-Y., Cheng, H.-Y., Chang, H., Chen, H.-H. and Ger, M.-J. (2011) Down regulation of putative UDP-glucose: flavonoid 3-O-glucosyltransferase gene alters flower coloring in Phalaenopsis. Plant Cell Rep. 30, 10071017.
  • Christensen, B., Sriskandarajah, S., Serek, M. and Muller, R. (2008) Transformation of Kalanchoe blossfeldiana with rol-genes is useful in molecular breeding towards compact growth. Plant Cell Rep. 27, 14851495.
  • Clarke, J.L., Spetz, C., Haugslien, S., Xing, S., Dees, M.W., Moe, R. and Blystad, D.-R. (2008) Agrobacterium tumefaciens-mediated transformation of poinsettia, Euphorbia pulcherrima, with virus-derived hairpin RNA constructs confers resistance to Poinsettia mosaic virus. Plant Cell Rep. 27, 10271038.
  • Colquhoun, T.A., Schimmel, B.C.J., Kim, J.Y., Reinhardt, D., Cline, K. and Clark, D.G. (2010) A petunia chorismate mutase specialized for the production of floral volatiles. Plant J. 61, 145155.
  • Da Silva, J.A.T., Chin, D.P., Van, P.T. and Mii, M. (2011) Transgenic orchids. Sci. Hort. 130, 673680.
  • Davison, J. (2010) GM plants: science, politics and EC regulations. Plant Sci. 178, 9498.
  • Debener, T. and Winkelmann, T. (2010) Ornamentals. In Genetic Modification of Plants, Biotechnology in Agriculture and Forestry 64 (Kempken, F. and Jung, C., eds), pp. 369391. Heidelberg: Springer-Verlag.
  • Dehnen-Schmutz, K., Touza, J., Perrings, C. and Williamson, M. (2007) A century of the ornamental plant trade and its impact on invasion success. Divers. Distrib. 13, 527534.
  • Dobres, M.S. (2008) Barriers to genetically engineered ornamentals: an industry perspective. In Floriculture, Ornamental and Plant Biotechnology; Advances and Topical Issues, vol. 5 (da Silva, J.A.T., ed), pp. 114. Isleworth: Global Science Books.
  • Dobres, M.S. (2011) Prospects for commercialisation of transgenic ornamentals. In Transgenic Horticultural Crops; Challenges and Opportunities (Mou, B. and Scorza, R., eds), pp. 305316. Boca Raton, FL: CRC press.
  • Drobnik, J. (2008) Time to relax GMO regulation in Europe. Plant Cell Tissue Organ Cult. 94, 235238.
  • Dudareva, N. and Pichersky, E. (2008) Metabolic engineering of plant volatiles. Curr. Opin. Biotechnol. 19, 181189.
  • Dudareva, N., Negre, F., Nagegowda, D.A. and Orlova, I. (2006) Plant volatiles: recent advances and future perspectives. Crit. Rev. Plant Sci. 25, 417440.
  • Dunwell, J.M. (1999) Transgenic crops: the next generation, or an example of 2020 vision. Ann. Bot. 84, 269277.
  • Durham, T., Douchet, J. and Snyder, L.U. (2011) Risk of regulation or regulation of risk? A de minimus framework for genetically modified crops. AgBioForum, 14, 6170.
  • EFSA. (2006) Opinion of the scientific panel on genetically modified organisms on a request from the commission related to the notification (Reference C/NL/04/02) for the placing on the market of the genetically modified carnation Moonlite 123.2.38 with a modified colour, for import of cut flowers for ornamental use, under Part C of directive 2001/18/EC from Florigene. EFSA J. 362, 119.
  • EFSA. (2008) Opinion of the scientific panel on genetically modified Organisms on a request from the Commission related to the notification (Reference C/NL/06/01) for the placing on the market of the genetically modified carnation Moonaqua 123.8.12 with a modified colour, for import of cut flowers for ornamental use, under Part C of directive 2001/18/EC from Florigene. EFSA J. 662, 125.
  • EFSA. (2009) EFSA scientific panel on genetically modified organisms (GMO); scientific opinion on guidance for the risk assessment of genetically modified plants used for non-food or non-feed purposes, on request of EFSA. EFSA J. 1164, 142.
  • Franklin, K.A. and Whitelam, G.C. (2006) Improvement of horticultural and ornamental crops through transgenic manipulation of the phytochrome family of plant photoreceptors. J. Crop Improvement, 17, 263278.
  • Gatehouse, J.A. (2008) Biotechnological prospects for engineering insect-resistant plants. Plant Physiol. 146, 881887.
  • Gubrium, E.K., Clevenger, D.J., Clark, D.G., Barrett, J.E. and Nell, T.A. (2000) Reproduction and horticultural performance of transgenic ethylene-insensitive petunias. J. Am. Soc. Hort. Sci. 125, 277281.
  • Gudin, S. (2010) Rose: genetics and breeding. Plant Breed. Rev. 17, 159189.
  • Guterman, I., Shalit, M., Menda, N., Piestun, D., Dafny-Yelin, M., Shalev, G., Bar, E., Davydov, O., Ovadis, M., Emanuel, M., Wang, J., Adam, Z., Pichersky, E., Lewinsohn, E., Zamier, D., Vainstein, A. and Weiss, D. (2002) Rose scent: genomics approach to discovering novel floral fragrance–related genes. Plant Cell, 14, 23252338.
  • Hall, C.R. and Dickson, M.W. (2011) Economic, environmental, and health/well-being benefits associated with green industry products and services: a review. J. Environ. Hort. 29, 96103.
  • Hall, C.R. and Hodges, A.W. (2011) Economic, environmental and well-being benefits of lifestyle horticulture. Chron Horticult. 51, 58.
  • Hammond, J., Hsu, H., Huang, Q., Jordan, R., Kamo, K. and Pooler, M. (2006) Transgenic approaches to disease resistance in ornamental crops. J. Crop Improvement, 17, 155210.
  • Han, Y.-J., Kim, Y.-M., Lee, J.-Y., Kim, S.J., Cho, K.-C., Chandrasekhar, T., Song, P.-S., Woo, Y.-M. and Kim, J.-I. (2009) Production of purple-colored creeping bentgrass using maize transcription factor genes Pl and Lc through Agrobacterium-mediated transformation. Plant Cell Rep. 28, 397406.
  • Harriman, R.W., Bolar, J.P. and Smith, F.D. (2006) Importance of biotechnology to the horticultural plant industry. J. Crop Improvement, 17, 126.
  • Hichri, I., Barrieu, F., Bogs, J., Kappel, C., Delrot, S. and Lauvergeat, V. (2011) Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. J. Exp. Bot. 62, 24652483.
  • Holton, T.A., Brugliera, F., Lester, D.R., Tanaka, Y., Hyland, C.D., Menting, J.G., Lu, C.Y., Farcy, E., Stevenson, T.W. and Cornish, E.C. (1993) Cloning and expression of cytochrome P450 genes controlling flower colour. Nature, 366, 276279.
  • Hsiao, Y.-Y., Pan, Z.-J., Hsu, C.-C., Yang, Y.-P., Hsu, Y.-C., Chuang, Y.-C., Shih, H.-H., Chen, W.-H., Tsai, W.-C. and Chen, H.-H. (2011) Research on orchid biology and biotechnology. Plant Cell Physiol. 52, 14671486.
  • Kalaitzandonakes, N., Alston, J.M. and Bradford, K.J. (2007) Compliance costs for regulatory approval of new biotech crops. Nat. Biotechnol. 25, 509511.
  • Kamiishi, Y., Otani, M., Takagi, H., Han, D.-S., Mori, S., Tatsuzawa, F., Okuhara, H., Kobayashi, H. and Nakano, M. (2011) Flower color alteration in the liliaceous ornamental Tricyrtis sp. by RNA interference-mediated suppression of the chalcone synthase gene. Mol Breed., DOI: 10.1007/s11032-011-9653-z.
  • Katsumoto, Y., Mizutani, M., Fukui, Y., Brugliera, F., Holton, T.A., Karan, M., Nakamura, N., Yonekura-Sakakibara, K., Togami, J., Pigeaire, A., Tao, G.-Q., Nehra, N., Lu, C.-Y., Dyson, B., Tsuda, S., Ashikari, T., Kusumi, T., Mason, J. and Tanaka, Y. (2007) Engineering of the rose flavonoid biosynthetic pathway successfully generated blue-hued flowers accumulating delphinidin. Plant Cell Physiol. 48, 15891600.
  • Khodakovskaya, M., Vankova, R., Malbeck, J., Li, A., Li, Y. and McAvoy, R. (2009) Enhancement of flowering and branching phenotype in Chrysanthemum by expression of ipt under the control of a 0.821 kb fragment of the LEACO1 gene promoter. Plant Cell Rep. 28, 13511362.
  • Kikuchi, A., Watanabe, K., Tanaka, Y. and Kamada, H. (2008) Recent progress on environmental biosafety assessment of genetically modified trees and floricultural plants in Japan. Plant Biotechnol. 25, 915.
  • Kim, Y.-S., Lim, S., Kang, K.-K., Y-J., Lee., Y-H., Choi. and Y-E. And Sano, H. (2011a) Resistance against beet armyworms and cotton aphids in caffeine-producing transgenic Chrysanthemum. Plant Biotechnol. 28, 393395.
  • Kim, Y.-S., Lim, S., Yoda, H., Choi, C.-S., Choi, Y.-E. and Sano, H. (2011b) Simultaneous activation of salicylate production and fungal resistance in transgenic Chrysanthemum producing caffeine. Plant Signal. Behav. 6, 409412.
  • Klingeman, W.E. and Babbit, B. (2006) Master gardener perception of genetically modified ornamental plants provides strategies for promoting research products through outreach and marketing. HortScience, 41, 12631268.
  • Klingeman, W.E. and Hall, C.R. (2006) Risk, trust, and consumer acceptance of plant biotechnology. J. Crop Improvement, 18, 451486.
  • Li, X., Gasic, K., Cammue, B., Broekaert, W. and Korban, S.S. (2003) Transgenic rose lines harboring an antimicrobial gene, Ace-AMP1, demonstrate enhanced resistance to powdery mildew (Sphaerotheca pannosa). Planta, 218, 226232.
  • Liao, L.-J., Pan, I.-C., Chan, Y.-L., Hsu, Y.-H., Chen, W.-H. and Chan, M.-T. (2004) Transgene silencing in Phalaenopsis expressing the coat protein of Cymbidium Mosaic Virus is a manifestation of RNA-mediated resistance. Mol. Breed. 13, 229242.
  • Lutken, H., Jensen, L.S., Topp, S.H., Mibus, H., Muller, R. and Rasmussen, S.K. (2010) Production of compact plants by overexpression of AtSHI in the ornamental Kalanchoe. Plant Biotechnol. J. 8, 211222.
  • Lutken, H., Laura, M., Borghi, C., Orgaard, M., Allavena, A. and Rasmussen, S.K. (2011) Expression of KxhKN4 and KxhKN5 genes in Kalanchoe blossfeldiana‘Molly’ results in novel compact plant phenotypes: towards a cisgenesis alternative to growth retardants. Plant Cell Rep. 30, 22672279.
  • Mackenzie, R., Burhenne-Guilmin, F., La Viña, A.G.M., Werksman, J.D., Ascencio, A., Kinderlerer, J., Kummer, K. and Tapper, R. (2006) An Explanatory Guide to the Cartagena Protocol on Biosafety. Gland, Switzerland and Cambridge, UK: IUCN.
  • Meng, L.-S., Song, J.-P., Sun, S.-B. and Wang, C.-Y. (2009) The ectopic expression of PttNN1 gene causes pleiotropic alternation of morphology in transgenic carnation (Dianthus caryophyllus L.). Acta Physiol. Plant. 31, 11551164.
  • Meyer, P., Heidemann, I., Forkmann, G. and Saedler, H. (1987) A new petunia flower colour generated by transformation of a mutant with a maze gene. Nature, 330, 677678.
  • Milbus, H., Sriskandarajah, S. and Serek, M. (2009) Genetically modified flowering potted plants with reduced ethylene sensitivity. Acta Hortic. 847, 7580.
  • Miller, J.K. and Bradford, K.J. (2010) The regulatory bottleneck for biotech speciality crops. Nat. Biotechnol. 10, 10121014.
  • Morandini, F., Avesani, L., Bortesi, L., Van Droogenbroeck, B., De Wilde, K., Arcalis, E., Bazzoni, F., Santi, L., Brozzetti, A., Falorni, A., Stoger, E., Depicker, A. and Pezzotti, M. (2011) Non-food/feed seeds as biofactories for the high-yield production of recombinant pharmaceuticals. Plant Biotechnol. J. 9, 911921.
  • Morris, S.H. and Spillane, C. (2008) GM directive deficiencies in the European Union. EMBO Rep. 9, 500504.
  • Nakamura, N., Fukuchi-Mizutani, M., Fukui, Y., Ishiguro, K., Suzuki, K. and Tanaka, Y. (2010) Generation of red flower varieties from blue Torenia hybrida by redirection of the flavonoid pathway from delphinidin to pelargonidin. Plant Biotechnol. 27, 375383.
  • Nakamura, N., Fukuchi-Mizutani, M., Katsumoto, Y., Togami, J., Senior, M., Matsuda, Y., Furuichi, K., Yoshimoto, M., Matsunaga, A., Ishiguro, K., Aida, M., Tasaka, M., Fukui, H., Tsuda, S., Chandler, S. and Tanaka, Y. (2011a) Environmental risk assessment and field performance of rose (Rosa × hybrida) genetically modified for delphinidin production. Plant Biotechnol. 28, 251261.
  • Nakamura, N., Tems, U., Fukuchi-Mizutani, M., Chandler, S., Matsuda, Y., Takeuchi, S., Matsumoto, S. and Tanaka, Y. (2011b) Molecular based evidence for a lack of gene-flow between Rosa × hybrida and wild Rosa species in Japan. Plant Biotechnol. 28, 245250.
  • Nakatsuka, T., Mishiba, K., Kubota, A., Abe, Y., Yamamura, S., Nakamura, N., Tanaka, Y. and Nishihara, M. (2010) Genetic engineering of novel flower colour by suppression of anthocyanin modification genes in gentian. J. Plant Physiol. 167, 231237.
  • Nakatsuka, T., Saito, M., Yamada, E. and Nishihara, M. (2011) Production of picotee type flowers in Japanese gentian by CRES-T. Plant Biotechnol. 28, 173180.
  • Narumi, T., Aida, R., Niki, T., Nishijima, T., Mitsuda, N., Hiratsu, K., Ohme-Takagi, M. and Ohtsubo, N. (2008) Chimeric AGAMOUS repressor induces serrated petal phenotype in Torenia fournieri similar to that induced by cytokinin application. Plant Biotechnol. 25, 4553.
  • Nishihara, M. and Nakatsuka, T. (2010) Genetic engineering of novel flower colors in floricultural plants: recent advances via transgenic approaches. Methods Mol. Biol. 589, 325347.
  • Nishihara, M. and Nakatsuka, T. (2011) Genetic engineering of flavonoid pigments to modify flower color in floricultural plants. Biotechnol. Lett. 33, 433441.
  • Ohtsubo, N. (2011) Beyond the blue rose: modification of floral architecture with plant-specific chimeric repressors. Plant Biotechnol. 28, 113121.
  • Oltmanns, H., Frame, B., Lee, L.-Y., Johnson, S., Li, B., Wang, K. and Gelvin, S.B. (2010) Generation of backbone-free, low transgene copy plants by launching T-DNA from the Agrobacterium chromosome. Plant Physiol. 152, 11581166.
  • Ono, E., Fukuchi-Mizutani, M., Nakamura, N., Fukui, Y., Yonekura-Sakakibara, K., Yamaguchi, M., Nakayama, T., Tanaka, T., Kusumi, T. and Tanaka, Y. (2006) Yellow flowers generated by expression of the aurone biosynthetic pathway. Proc. Natl Acad. Sci. USA, 103, 1107511080.
  • Potera, C. (2007) Blooming biotech. Nat. Biotechnol. 25, 963965.
  • Raffeiner, B., Serek, M. and Winkelmann, T. (2009) Agrobacterium tumefaciens mediated transformation of Oncidium and Odontoglossum orchid species with the ethylene receptor mutant gene etr1-1. Plant Cell Tissue Organ Cult. 98, 125134.
  • Ramessar, K., Capell, T., Twyman, R.M., Quemada, H. and Christou, P. (2009) Calling the tunes on transgenic crops: the case for regulatory harmony. Mol. Breed. 23, 99112.
  • Ricroch, A.E., Berge, J.B. and Kuntz, M. (2011) Evaluation of genetically engineered crops using transcriptomic, proteomic, and metabolomic profiling techniques. Plant Physiol. 155, 17521761.
  • Rommens, C.M. (2010) Barriers and paths to market for genetically engineered crops. Plant Biotechnol. J. 8, 101111.
  • Rosati, C. and Simoneau, P. (2008) Metabolite engineering of flower color in ornamental plants. J. Crop Improvement, 18, 301324.
  • Sandmann, G., Romer, S. and Fraser, P.D. (2006) Understanding carotenoid metabolism as a necessity for genetic engineering of crop plants. Metab. Eng. 8, 291302.
  • Sanikhani, M., Mibus, H., Stummann, B.M. and Serek, M. (2008) Kalanchoe blossfeldiana plants expressing the Arabidopsis etr1-1 allele show reduced ethylene sensitivity. Plant Cell Rep. 27, 729737.
  • Sasaki, K., Aida, R., Niki, T., Yamaguchi, H., Narumi, T., Nishijima, T., Hayashi, Y., Ryuto, H., Fukunishsi, N., Abe, T. and Ohtsubo, N. (2008) High-efficiency improvement of transgenic torenia flowers by ion beam irradiation. Plant Biotechnol. 25, 8189.
  • Satoh, S., Watanabe, M., Chisaka, K. and Narumi, T. (2008) Suppressed leaf senescence in Chrysanthemum transformed with a mutated ethylene receptor gene mDG-ERS1(etr1-4). J. Plant Biol. 51, 424427.
  • Saxena, G., Banerjee, S., Rahman, L., Verma, P.C., Mallavarapu, G.R. and Kumar, S. (2007) Rose-scented geranium (Pelargonium sp.) generated by Agrobacterium rhizogenes mediated Ri-insertion for improved essential oil quality. Plant Cell Tissue Organ Cult. 90, 215223.
  • Sexton, S. and Zilberman, D. (2011) The economic and marketing challenges of horticultural biotechnology. In Transgenic Horticultural Crops; Challenges and Opportunities (Mou, B. and Scorza, R., eds), pp. 175192. Boca Raton, FL: CRC press.
  • Shibata, M. (2008) Importance of genetic transformation in ornamental plant breeding. Plant Biotechnol. 25, 38.
  • Shikata, M. and Ohme-Takagi, M. (2008) The utility of transcription factors for manipulation of floral traits. Plant Biotechnol. 25, 3136.
  • Shinoyama, H. and Mochizuki, A. (2006) Insect resistant Chrysanthemum [Dendranthema × grandiflorum (Ramat.) Kitamura]. Acta Hortic. 714, 177184.
  • Shinoyama, H., Mochizuki, A., Nomura, Y. and Kamada, H. (2008) Environmental risk assessment of genetically modified chrysanthemums containing a modified cry1Ab gene from Bacillus thuringiensis. Plant Biotechnol. 25, 1729.
  • Shinoyama, H., Sano, T., Saito, M., Ezura, H., Aida, R., Nomura, Y. and Kamada, H. (2012) Induction of male sterility in transgenic chrysanthemums (Chrysanthemum morifolium Ramat.) by expression of a mutated ethylene receptor gene, Cm-ETR1/H69A, and the stability of this sterility at varying growth temperatures. Mol. Breed. 29, 285295.
  • Shulga, O.A., Mitouchkina, T.Y., Shchennikova, A.V., Skryabin, K.G. and Dolgov, S.V. (2009) Early flowering transgenic Chrysanthemum plants. Acta Hortic. 836, 241246.
  • Shulga, O.A., Mitouchkina, T.Y., Shchennikova, A.V., Skryabin, K.G. and Dolgov, S.V. (2011) Overexpression of AP1-like genes from Asteraceae induces early-flowering in transgenic Chrysanthemum plants. In Vitro Cell. Dev. Biol. Plant 47, 553560.
  • Spitzer-Rimon, B., Marheva, E., Barkal, O., Marton, I., Edelbaum, O., Masci, T., Naveen-Kumar, P., Shklamann, E., Ovadis, M. and Vainstein, A. (2010) EOBII, a gene encoding a flower-specific regulator of phenylpropanoid volatiles’ biosynthesis in petunia. Plant Cell, 22, 19611976.
  • Stein, A.J. and Rodriguez-Cerezo, E. (2010) Low-level presence of new gm crops: an issue on the rise for countries where they lack approval. AgBioForum, 13, 173182.
  • Strauss, S.H. (2011) Why are regulatory requirements a major impediment to genetic engineering of horticultural crops? In Transgenic Horticultural Crops; Challenges and Opportunities (Mou, B. and Scorza, R., eds), pp. 249262. Boca Raton, FL: CRC press.
  • Sun, S.-B., Song, J.-P. and Yang, J. (2011) Overexpressing Arabidopsis KNAT1 gene in Celosia plumosus L. causes modification of plant morphology. Acta Physiol. Plant. 33, 15971602.
  • Suzuki, S., Nishihara, M., Nakatsuka, T., Misawa, N., Ogiwara, I. and Yamamura, S. (2007) Flower color alteration in Lotus japonicus by modification of the carotenoid biosynthetic pathway. Plant Cell Rep. 26, 951959.
  • Tanaka, Y. and Ohmiya, A. (2008) Seeing is believing: engineering anthocyanin and carotenoid biosynthetic pathways. Curr. Opin. Biotechnol. 19, 190197.
  • Tanaka, Y., Brugliera, F. and Chandler, S. (2009) Recent progress of flower colour modification by biotechnology. Int. J. Mol. Sci. 10, 53505369.
  • Tanaka, Y., Brugliera, F., Kalc, G., Senior, M., Dyson, B., Nakamura, N., Katsumoto, Y. and Chandler, S. (2010) Flower color modification by engineering of the flavonoid biosynthetic pathway: practical perspectives. Biosci. Biotechnol. Biochem. 74, 17601769.
  • Terdich, K. and Chandler, S. (2009) Regulatory considerations for the approval of gentically modified carnations in Korea. Biosafety, 10, 7283.
  • Thiruvengadam, M. and Yang, C.-H. (2009) Ectopic expression of two MADS box genes from orchid (Oncidium Gower Ramsey) and lily (Lilium longiflorum) alters flower transition and formation in Eustoma grandiflorum. Plant Cell Rep. 28, 14631473.
  • Togami, J., Okhuhara, H., Nakamura, N., Ishiguro, K., Hirose, C., Ochiai, M., Fukui, Y., Yamaguchi, M. and Tanaka, Y. (2011) Isolation of cDNAs encoding tetrahydroxychalcone 2_-glucosyltransferase activity from carnation, cyclamen, and catharanthus. Plant Biotechnol. 28, 231238.
  • Underwood, B.A. and Clarke, D.G. (2011) Transgenic ornamental crops. In Transgenic Horticultural Crops; Challenges and Opportunities (Mou, B. and Scorza, R., eds), pp. 5582. Boca Raton, FL: CRC press.
  • Waltz, E. (2011) GM grass eludes outmoded USDA oversight. Nat. Biotechnol. 29, 772773.
  • Warner, R. (2011) Genetic approaches to improve cold tolerance of petunia. Floricult. Int. June, 1516.
  • Ye, X., Williams, E.J., Shen, J., Johnson, S., Lowe, B., Radke, S., Strickland, S., Esser, J.A., Petersen, M.W. and Gilbertson, L.A. (2011) Enhanced production of single copy backbone-free transgenic plants in multiple crop species using binary vectors with a pRi replication origin in Agrobacterium tumefaciens. Transgenic Res. 20, 773786.
  • Yu, F. and Utsumi, R. (2009) Diversity, regulation, and genetic manipulation of plant mono- and sequiterpenoid biosynthesis. Cell. Mol. Life Sci. 66, 30433052.
  • Zubko, M.K., Zubko, E.I., van Zuilen, K., Meyer, P. and Day, A. (2004) Stable transformation of petunia plastids. Transgenic Res. 13, 523530.
  • Zvi, M.M.B., Negre-Zakharov, F., Masci, T., Ovadis, M., Shklarman, E., Ben-Meir, H., Tzfira, T., Dudareva, N. and Vainstein, A. (2008a) Interlinking showy traits: co engineering of scent and colour biosynthesis in flowers. Plant Biotechnol. J. 6, 403415.
  • Zvi, M.M.B., Zuker, A., Ovadis, M., Shklarman, E., Ben-Meir, H., Zenvirt, S. and Vainstein, A. (2008b) Agrobacterium-mediated transformation of gypsophila (Gypsophila paniculata L.). Mol. Breed. 22, 543553.