Plant Biotechnology Journal (2012) 10, pp. 891–903
doi: 10.1111/j.1467-7652.2012.00693.x
Review article
Genetic modification; the development of transgenic
ornamental plant varieties
Stephen F. Chandler1,* and Cory Sanchez2
1
School of Applied Sciences, RMIT University, Bundoora, Vic., Australia
2
Florigene Flowers, Miramar, FL, USA
Received 6 January 2012;
revised 20 February 2012;
accepted 28 February 2012.
*Correspondence (fax +1 954 874 1679;
email [email protected])
Keywords: ornamentals, genetic
modification, transgenic, colour modification, regulation, harmonization.
Summary
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
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 nonfood 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
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Plant Biotechnology Journal ª 2012 Society for Experimental Biology, Association of Applied Biologists and Blackwell Publishing Ltd
891
892 Stephen F. Chandler and Cory Sanchez
Table 1 Major groups and genera of ornamental plants
Potted and
Bedding
Cut-flowers
Ornamental
grasses
Palms
indoor
plants
Shrubs
Rose
Festuca spp.
Fan palm
Phalaenopsis spp
Petunia
Rose
Carnation
Deer grass
Date palm
Rose
Pansy
Hydrangea
Trees
Miscellaneous
Dogwood
Bonsai
Cotoneaster
Cacti
Rhododendron
Azalea spp.
Chrysanthemum
Tufted hair
grass
Canary Island
Kalanchoe spp.
Impatiens spp.
Abelia
Maple
Succulents
Air plants
date palm
Tulip
Panicum spp.
Sabal palm
Campanula spp.
Begonia
Viburnum
Willow
Lily
Agrostis spp.
Sago palm
English Ivy
Torenia
Agapanthaus
Birch
Ferns
Gerbera
Miscanthus
Pindo palm
Anthurium spp.
Salvia spp.
Camellia spp.
Ash
Box
Babys breath
Carex spp.
Queen palm
Eucalyptus
sinensis
Dracaena spp.
Calibrachoa spp.
Fuchsias
Peruvian lily
Chrysanthemum
Lobelia
Grevillia
Liquidambar
Freesia spp.
Ficus spp.
Osteospermum
Lavender
Cedar
Cymbidium spp.
Spathiphyllum spp.
Verbena
spp.
Ficus spp.
Mulberry
Paulownia
Anthurium spp.
Cyclamen spp.
Pinks
Magnolia
Lisianthus
Lily
African violet
Grape myrtle
Polar
Prunus
Zantedeschia spp.
Geranium
Crocus
Privet
Oak
Dendrobium spp.
Poinsettia
Narcissus spp.
Ivy
Elm
Phalaenopsis spp.
Heather
Skimmia spp.
Hibiscus
Chamaecyparis spp.
Narcissus spp.
Spider plant
Hellebores
Hydrangea
Bromeliads
Skimmia spp.
Cacti
Gaultheria spp.
Heather
Bonsai
Amaryllis
Cattleya spp.
Hyacinth
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.
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).
Genetically modified ornamentals; pipeline
and products
Transformation
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
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
1
In this review we have adopted the convention of the use of
· hybrida for hybrids of uncertain botanical origin.
ª 2012 The Authors
Plant Biotechnology Journal ª 2012 Society for Experimental Biology, Association of Applied Biologists and Blackwell Publishing Ltd, Plant Biotechnology Journal, 10, 891–903
Transformation technology and new ornamental plant varieties 893
Table 2 Recent examples of flower colour modification using GM
Species
Colour change
Citation
Cyclamen persicum
Purple to red ⁄ pink
Boase et al. (2010)
Blue to white
Nakatsuka et al.
Lotus japonicus
Light yellow to
Suzuki et al. (2007)
Phalaenopsis spp.
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)
(cyclamen)
Gentiana triflora
(Japanese gentian)
(2010, 2011)
Yellow ⁄ orange
(phalaenopsis)
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).
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 colourmodified 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).
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
GM, genetic modification.
persisted in the transgenics (Azadi et al., 2010). This illustrates
the complexity of the regulation of carotenoid biosynthesis and
metabolism.
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 delphinidinderived 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.
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 Pi-
ª 2012 The Authors
Plant Biotechnology Journal ª 2012 Society for Experimental Biology, Association of Applied Biologists and Blackwell Publishing Ltd, Plant Biotechnology Journal, 10, 891–903
894 Stephen F. Chandler and Cory Sanchez
1
2
3
4
5
6
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).
chersky, 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
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Plant Biotechnology Journal ª 2012 Society for Experimental Biology, Association of Applied Biologists and Blackwell Publishing Ltd, Plant Biotechnology Journal, 10, 891–903
Transformation technology and new ornamental plant varieties 895
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
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896 Stephen F. Chandler and Cory Sanchez
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
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 longterm 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 endconsumer. 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.
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Plant Biotechnology Journal ª 2012 Society for Experimental Biology, Association of Applied Biologists and Blackwell Publishing Ltd, Plant Biotechnology Journal, 10, 891–903
Transformation technology and new ornamental plant varieties 897
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
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 crosscompatibility 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
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898 Stephen F. Chandler and Cory Sanchez
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
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Transformation technology and new ornamental plant varieties 899
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 ‘caseby-case’ provision in most legislation (EFSA, 2009) for reducing
molecular analysis.
Looking ahead
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. Dobres (2008) has identified the shrub and tree market
as a good target for the expanded application of GM in the US
given that domestic production supplies the market, and that
the products have a high value. As more traits are 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.
ª 2012 The Authors
Plant Biotechnology Journal ª 2012 Society for Experimental Biology, Association of Applied Biologists and Blackwell Publishing Ltd, Plant Biotechnology Journal, 10, 891–903
900 Stephen F. Chandler and Cory Sanchez
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.
Acknowledgements
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.
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