Petal Growth Physiology of Cut Rose Flowers: Progress and Future Prospects

Abstract

Roses are the most important crop in the floriculture industry and attract both pollinators and human admirers. Until now, a lot of research focusing on postharvest physiology including flower senescence has been conducted, leading to improvement in vase life. However, few studies have focused on the physiology of petal growth, the perception of light by petals, and the relationship between petal growth and environmental conditions. Regarding roses, whose ornamental value lies in the process of blooming from buds, it is also important to understand their flowering mechanisms and establish methods to control such mechanisms, as well as focus on slowing the aging process, in order to achieve high quality of postharvest cut roses. Elucidation of the mechanisms of rose flower opening would contribute to enhanced quality and commercial production of floricultural crops as well as greatly advance basic scientific knowledge regarding plant biology. In this review, we describe the progress and future prospects in the study of petal growth physiology of cut roses.

Full text

Journal of Horticultural Research 2017, vol. 25(1): 5–18
DOI: 10.1515/johr-2017-0001
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*Corresponding author:
e-mail: t-horibe@isc.chubu.ac.jp, Tel.: +81-092-642-2913
PETAL GROWTH PHYSIOLOGY OF CUT ROSE FLOWERS:
PROGRESS AND FUTURE PROSPECTS
Takanori HORIBE*, Kunio YAMADA
College of Bioscience and Biotechnology, Chubu University
Kasugai 487-8501, Japan
Received: January 2017; Accepted: April 2017
ABSTRACT
Roses are the most important crop in the floriculture industry and attract both pollinators and human
admirers. Until now, a lot of research focusing on postharvest physiology including flower senescence has
been conducted, leading to improvement in vase life. However, few studies have focused on the physiology
of petal growth, the perception of light by petals, and the relationship between petal growth and environ-
mental conditions. Regarding roses, whose ornamental value lies in the process of blooming from buds, it
is also important to understand their flowering mechanisms and establish methods to control such mecha-
nisms, as well as focus on slowing the aging process, in order to achieve high quality of postharvest cut
roses. Elucidation of the mechanisms of rose flower opening would contribute to enhanced quality and
commercial production of floricultural crops as well as greatly advance basic scientific knowledge regard-
ing plant biology. In this review, we describe the progress and future prospects in the study of petal growth
physiology of cut roses.
Key words: Petal morphology, sugar metabolism, Rosa, circadian rhythm, postharvest
INTRODUCTION
The rose (genus Rosa) holds an important po-
sition in the ornamental flower industry. Roses can
usually be found as cut flowers in vases or growing in
gardens. Humans are said to have been cultivating
roses since before the Common Era, making it one
of the most familiar and cherished flowers known
to mankind in recorded history. Initially used as
a fragrance and medicinal purposes, the rose even-
tually came to be appreciated as an ornamental
flower. In the Northern Hemisphere alone, there are
approximately 150 species of roses growing in the
wild. While there may be tens of thousands of cul-
tivars grown to date, only 8–20 of these are in-
volved in the breeding of the four main genealogi-
cal lines presently being cultivated (Bendahmane et
al. 2013). Nowadays, cut flower cultivars are be-
coming more diverse, ranging from the more tradi-
tional varieties with tall, pointy petals to those with
rounded, cup-shaped petals; old-rose-like quarter-
bloom petals; or single-petal flowers.
The quality of a cut flower is contingent upon
the external characteristics of the plant such as color,
length, volume, freshness, and fragrance as well as its
perishability, which is determined by the duration of
these aforementioned conditions. In particular, vase
life is a critical factor in determining the market value
of cut flowers. However, because it takes a few days
before cut flowers produced by farmers reach con-
sumers via retailers, aging progresses in the mean-
time. As a result, most cut flowers will no longer be
suitable for ornamental purposes within a week or so,
making it difficult to enjoy them for a long time. Fac-
tors implicated in shortening the life expectancy of cut
flowers include aging, detachment and withering of
tissues by ethylene generation, obstruction of vessels
because of bacterial propagation (and thus poor water
absorption), and deficiency in saccharides that act as
osmoregulators and respiratory substrates (Durkin
1979; Burdett 1970; De Stigter 1980; Macnish et al.
2010; Reid 1989; van Doorn 1997). Ethylene, a phy-
tohormone, is a key player involved in the aging of
many cut flowers. Consequently, numerous studies
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6 T. Horibe, K. Yamada
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have aimed to suppress or inhibit ethylene generation
during the blooming of cut flowers to slow down the ag-
ing process (Ichimura & Shimizu-Yumoto 2007). In rose
flower, it has been reported that ethylene regulate flower
opening and petal expansion as well as senescence (Ma
et al. 2006; Ma et al. 2008; Tan et al. 2006). The relation-
ship between flower opening and hormones has been
reviewed recently by van Doorn & Kamdee (2014).
As a result of continued efforts to improve the
quality of cut flowers, agents such as ethylene inhib-
itors have been developed, ensuring long-lasting
quality of harvested cut flowers. However, many of
these studies investigated decelerating the aging pro-
cess. Regarding roses, whose ornamental value lies
in the process of blooming from buds, it is also im-
portant to understand their flowering mechanisms
and establish methods to control such mechanisms,
as well as focus on slowing the aging process, in or-
der to achieve high quality of postharvest cut roses.
PETAL GROWTH AND FLOWER OPENING
The process of rose flower bud development and
subsequent flower opening is irreversible petal growth
and reflection in which existing cells expand and fresh
and dry weights (DW) increase (Reid & Evans 1986;
Evans & Reid 1988; Faragher et al. 1984). In Gaillar-
dia × grandiflora, cell division of the petals seems to
stop at a much early stage of flowering, with no in-
crease in the number of abaxial epidermal cells (Kon-
ing 1984). In carnation flowers, the amount of DNA in
the petals does not increase once petals emerge from
the calyx, suggesting that cell division also stops at an
early stage (Kenis et al. 1985). These findings indi-
cated that petal growth as it relates to flower opening
mainly depends on cell expansion. Cell division in
rose petals almost stops while petals are still covered
by the calyx (Roberts et al. 2003; Yamada et al.
2009c), suggesting that rose petal growth associated
with flower opening may indeed depend on cell ex-
pansion. During flower opening, large amounts of sol-
uble carbohydrates accumulate in petals (van Doorn et
al. 1991; Ichimura et al. 2003). Many studies have re-
ported on the application of sugars in extending the
vase life of cut flowers (Paulin 1979; Paulin & Jamain
1982; Ichimura et al. 2003). Paulin and Jamain (1982)
and Ichimura et al. (2003) demonstrated that sucrose
treatment increased the vase life of cut carnations and
roses, suggesting that soluble carbohydrates play an
important role in regulating osmotic pressure in petal
cells (Fig. 1). Sugar accumulation in petal cells re-
duces petal water potential, thereby promoting water
influx for cell expansion, which may lead to flower
opening (Ho & Nichols 1977). In tulip petals, glucose
and fructose accumulate mainly in the vacuole (Wag-
ner 1979). In addition to the vacuole, soluble carbohy-
drates accumulate in the apoplast in some sink organs,
such as tomato fruits (Damon et al. 1988) and sugar-
cane stalks (Welbaum & Meinzer 1990). Flowers are
also sink organs, and particularly, carbohydrates accu-
mulate in the apoplast of rose petal cells (Yamada et
al. 2009b). To accelerate water influx into cells, os-
motic pressure should be higher in the symplast than
in the apoplast.
In most rose species, the degradation of storage
carbohydrates, the import of sucrose, or both is asso-
ciated with flower opening (van Doorn & van
Meeteren 2003). Young petal cells of many species
contain considerable amounts of starch, which is rap-
idly converted to hexose (Hammond 1982; Ho &
Nichols 1977). Petal starch levels at harvest are high
in many rose cultivars such as ‘Sonia’, but are low in
cultivars such as ‘Madelon’ (Berkholst 1989; Gorin &
Berkholst 1982; van Doorn 1991; van Doorn & van
Meeteren 2003). Gorin and Berkholst (1982) elabo-
rated a criterion of rose maturity for harvest, which
was starch content in petals: less than 10% on DW ba-
sis would denote that flowers were picked too early.
Kuiper et al. (1995) reported that adding sucrose to cut
‘Madelon’ rose buds induced proper flower opening,
even though cut roses of this variety frequently fail to
open completely under postharvest conditions, illus-
trating the importance of sugar accumulation in petal
growth. It has also been reported that increases in glu-
cose and fructose content during cut ‘Sonia‘ rose
opening were much greater than starch content in pet-
als at the bud stage (Yamada et al. 2009a), suggesting
that an increase in monosaccharide content cannot be
attributed to only the degradation of the starch reserve.
Thus, the increase in monosaccharide content derived
from photosynthetic products transported from leaves
seems important for proper opening in some rose cul-
tivars. In some other flowers, including the daylily
(Bieleski 1993) and Campanula rapunculoides (Ver-
gauwen et al. 2000), fructans in the petals decrease
during flower opening, which is associated with an in-
crease in monosaccharides.
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Flower opening physiology of cut roses 7
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Fig. 1. Flower opening and cell enlargement of rose petal cells. Rose flower opening is a process of irreversible petal
growth and reflection in which existing cells expand and fresh and dry weights increase (A). Sugar accumulation in the
vacuole, cell wall loosening, and subsequent water flow into the cell are thought to be important for cell enlargement (B)
In addition to glucose, fructose, and sucrose,
which are ubiquitous metabolic sugars, methyl glu-
coside, xylose, and myo-inositol are soluble carbo-
hydrate constituents in roses (Ichimura et al. 1997).
Myo-Inositol acts to increase osmotic pressure and
is a precursor of cell wall synthesis (Loewus &
Dickinson 1982), but its application inhibits flower
opening in cut roses (Ichimura et al. 1999). Myo-In-
ositol may accumulate in the apoplast and suppress
water influx to the vacuole, leading to the inhibition
of cell expansion associated with flower opening.
Although the application of methyl glucoside and xy-
lose promotes flower opening in cut roses (Ichimura
et al. 1999), these carbohydrates concentrations are
relatively low and do not increase during rose flower
opening (Yamada et al. 2009a). Thus, these carbo-
hydrates appear not to be important for flower open-
ing in the rose plant.
In the shoots and leaves of some plants, K+ is
a primary ion that contributes to osmotic pressure,
whereas Ca2+, Mg2+, NO3−, and Cl− are also major
ions (Cram 1976; Leigh & Tomos 1993). In addi-
tion, organic acids contribute to the increase in os-
motic pressure in many plants, such as sugarcane
stalk (Cram 1976; Welbaum & Meinzer 1990). In
rose petals, malic acid and citric acid are found to
be major organic acids (Biran et al. 1974; Schnabl
& Mayer 1976). Yamada et al. (2009a) determined
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8 T. Horibe, K. Yamada
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the subcellular distribution of soluble carbohydrates
and inorganic ions by combining nonaqueous frac-
tionation and infiltration–centrifugation methods
and showed that osmotic pressure increase in the
apoplast and symplast during flower opening was
mainly attributed to increases in fructose and glu-
cose concentrations.
FUNCTION OF SUGAR METABOLIZING
PROTEINS DURING FLOWER OPENING
There are two pathways of phloem unloading,
that is, apoplastic or symplastic unloading pathways
(Patrick & Offler 1996). After unloading, sugars are
transported through the apoplast and/or symplast.
The enzymes that metabolize sucrose translocated
from leaves to sink tissues are sucrose synthase and
acid invertase (β-fructofuranosidase), which are
present in the vacuole (soluble form) and cell wall
(insoluble form) in many higher-order plants. Acid
invertase located in the cell wall converts sucrose
into hexoses after sucrose is translocated from the
phloem to the apoplast (Roitsch & González 2004),
and this enables petals to uptake more sucrose from
the phloem. Acid invertase in the vacuole also plays
an important role in sucrose metabolism. It presum-
ably hydrolyzes sucrose to supply hexoses neces-
sary for cell growth and development (Tang et al.
1999). In addition, invertase activities in the petals
of attached rose flowers increased markedly during
petal growth but not in cut roses, even in cut roses
treated with sucrose (Yamada et al. 2007). On the
other hand, sucrose synthase activity is weaker than
acid invertase activities in rose petals (Kumar et al.
2008), suggesting that sugars appear to be trans-
ported at least partly through apoplastic unloading
in rose petals. Thus, high glucose and fructose con-
centrations in the apoplast may be due to the
transport of these carbohydrates through the apo-
plast (Yamada et al. 2007). In tomato (Damon et al.
1988) and apple fruits (Zhang et al. 2004), in which
sugar concentrations in the apoplast are relatively
high, sugars are partially transported through the
apoplast. Numerous reports have indicated a rela-
tionship between invertase activity and sink
strength of sink tissues (Tang et al. 1999; Balibrea
et al. 2004; Roitsch & González 2004). Invertase ac-
tivity seems to limit petal growth and is related to
flower opening. Some studies have shown that cer-
tain phytohormones affect invertase activity (Miya-
moto et al. 1993; Trouverie et al. 2004; Pan et al.
2006; González & Cejudo 2007). Activity of acid
invertases have been shown to be affected by α-
naphthylacetic acid and methyl jasmonate treat-
ments in cut roses, and interestingly, the speed of
flower opening also changed per treatment (Horibe
et al. 2013). Thus, the quality of cut rose flowers
may be enhanced via controlling invertase activity
postharvest.
FUNCTION OF CELL-WALL-LOOSENING
PROTEINS DURING FLOWER OPENING
Relaxing the strength of the cell wall for cell
enlargement is also important for petal growth
(Fig. 1). When the cell walls of petals remain rigid,
neither water influx nor cell expansion may occur.
Cell wall extensibility may be a growth-limiting
factor for petal expansion. Many proteins and en-
zymes are required for cell expansion. Cell-wall-
loosening candidate proteins include endotransgly-
cosylase/hydrolase (XTH) and expansins (Cosgrove
2001). Expansins were first identified in cell wall
protein fractions that restored acid-induced exten-
sion of heat-inactivated cell walls (McQueen-Ma-
son et al. 1992). They are believed to disrupt hydro-
gen bonding between cellulose microfibrils and ma-
trix glucans (McQueen-Mason & Cosgrove 1994).
Expansin genes belong to a multigene superfamily
that includes α-expansin, which was identified first,
and β-expansin (Cosgrove 2001), which are com-
monly identified in expanding and growing tissues.
Expansins are also expressed in non-growing tissue,
such as ripening fruits (Brummel et al. 1999;
Civello et al. 1999; Rose et al. 1997) and the abscis-
sion zone (Belfield et al. 2005; Sane et al. 2007).
While XTHs were first identified and characterized
in higher-order plants (Nishitani & Tominaga
1992). Each gene in the XTH family catalyzes either
molecular grafting or disassembly of xyloglucan
cross-links within the cellulose–xyloglucan frame-
work (Nishitani & Tominaga 1992; Okazawa et al.
1993); thus, XTHs participate in loosening and re-
arranging the cell walls in growing tissues (Rose et
al. 2002). XTHs may also participate in cell expan-
sion (Nishitani 1997; Vissenberg et al. 2000). XTHs
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Flower opening physiology of cut roses 9
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are expressed in growing tissues and ripening fruits
as stated earlier (Catalá et al. 2000; Rose & Bennett
1999) and in the developmental processes such as
aerenchyma formation (Antosiewicz et al. 1997;
Saab & Sachs 1996).
In ornamental plants, α- expansin and β-expan-
sin were identified from opening and senescing Mi-
rabilis jalapa flowers (Gookin et al. 2003). The two
expansin genes are also associated with petal
growth and development during carnation flower
opening (Harada et al. 2011). In addition, expansin
is expressed during the flower opening of tomatoes
(Brummel et al. 1999) and Petunia hybrida (Zenoni
et al. 2004), and XTH activity is associated with the
opening of Sandersonia flowers (O’Donoghue et al.
2002). In roses, RhEXPA, one of the three α-expansin
genes (RhEXPA1–RhEXPA4) and RhXTH1, one of
the four endotransglycosylase/hydrolase genes
(RhXTH1–RhXTH4), are mainly involved in petal ex-
pansion (Takahashi et al. 2007; Yamada et al. 2009b;
Dai et al. 2012). Dai et al. (2012) reported that
RhEXPA4 is involved in the regulation of dehydra-
tion tolerance during the expansion of rose petals.
FUNCTION OF AQUAPORINS DURING
FLOWER OPENING
Aquaporins are multifunctional membrane
channels proteins that facilitate membrane transport
of water molecules and low-molecular-weight com-
pounds (Katsuhara et al. 2008). On the basis of amino
acid sequence similarities, aquaporins are classified
into seven subfamilies: the plasma membrane intrin-
sic proteins (PIPs) and tonoplast intrinsic proteins
(TIPs), which are the most abundant aquaporins in
the plasma membrane and tonoplast; the nodulin-
26-like intrinsic proteins, which are located in the
peribacteroid membrane of nitrogen-fixing symbi-
otic root nodules of leguminous plants and are pre-
sent in the plasma membrane of other species; the
small basic intrinsic proteins, which are small pro-
teins mainly localized in the membrane of endoplas-
mic reticulum; the uncharacterized X intrinsic pro-
teins (XIPs), which are plasma membrane aqua-
porins that function in the transport of uncharged
substrates; and the hybrid intrinsic proteins and
glycerol-facilitator-like intrinsic proteins, which are
present exclusively in moss (Wang et al. 2016).
Among these aquaporins, PIPs and TIPs are thought
to play a key role in plant growth and cell enlarge-
ment (Katsuhara et al. 2008).
In tulips, Azad et al. (2004; 2008; 2013) sug-
gested that petal opening and closure occur concom-
itantly with water transport and are regulated by re-
versible phosphorylation of a PIP, and two TIPs
(TgTIP1;1 and TgTIP1;2) contribute to the petal
development. In the rose, it has been shown that
expression of Rh-TIP1;1 is related with ethylene
and water-deficit stress reaction and RhPIP1;1 si-
lencing significantly inhibited the expansion of pet-
als, resulting in decreased petal size and cell area,
illustrating the important role of aquaporins in the
expansion of petal cell (Chen et al. 2013). As aqua-
porins function in the transportation of water and
low-molecular-weight compounds, it is plausible
that they also play an important role in flower open-
ing. However, relatively little is known about aqua-
porin function in rose flower opening.
CELL MORPHOLOGY OF PETAL CELLS
DURING FLOWER OPENING
In relation to the cell morphology of cut roses,
adaxial and abaxial epidermal cells show marked
expansion during flower opening, and adaxial epi-
dermal cells become corn-shaped when fully
opened (Yamada et al. 2009c). Differences in the
patterns of cell expansion among cell types and lo-
cations, including adaxial and abaxial epidermal
cells, are thought to cause petal reflection during
rose flower opening. Cortical microtubules have
been proposed to regulate the orientation of cell
expansion (Shibaoka 1994). Ethylene inhibits lon-
gitudinal cell expansion and promotes lateral cell
expansion, which is associated with changes in cor-
tical microtubule orientation (Roberts et al. 1985;
Steen & Chadwick 1981). In some rose cultivars,
ethylene accelerates flower opening (Reid et al.
1989; Tan et al. 2006) and treatment with silver thi-
osulfate complex, which is inhibitor of ethylene ac-
tion, suppresses petal reflection (Doi 1995). Thus,
the lateral growth of adaxial epidermal cells might
be regulated by endogenous ethylene production by
changing cortical microtubule orientation. Although
exposure to ethylene at a high concentration induces
petal abscission of Sonia rose (Ichimura et al. 2005;
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10 T. Horibe, K. Yamada
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Reid et al. 1989), endogenous ethylene production of
this cultivar is relatively low (Ichimura et al. 2005),
which does not rule out the possible involvement of
ethylene in the lateral cell expansion of petals.
Via light and scanning electron microscopy,
the parenchyma cells of rose petals showed unique
growth, resulting in a tetrapod-like shape that re-
sembles the mesophyll cells of leaves (Yamada et
al. 2009c). Mesophyll cell morphogenesis and inter-
cellular space formation were investigated in Adian-
tum capillus-veneris leaves (Panteris et al. 1993)
and Nigella damascena leaves (Wernicke et al.
1993). The resulting observations showed that mes-
ophyll cell morphogenesis and intercellular space
formation are controlled by highly organized corti-
cal microtubule systems with the distribution of mi-
crotubule bundles between neighboring mesophyll
cells being highly coordinated (Hellmann & Wer-
nicke 1998; Schröder et al. 2001; Uehara & Hogetsu
1993). Intercellular space formation in leaves seems
to make space for gas exchange in photosynthesis.
Although petals are similar tissues to leaves, their
functions are quite different, so the role of the air
space in rose petals, in the context of flower open-
ing, is unclear.
FUNCTION OF SUGAR IN VASE WATER
SOLUTION AND ITS TRANSLOCATION
The length of life in a vase, vase life, is one of
the most important factors for prolonged quality of
cut flowers. Vase life was shown to vary among var-
ious cultivars in carnations (Wu et al. 1991), in Ger-
bera (Wernett et al. 1996), and also in roses
(Ichimura et al. 2002). The vase life of cut rose
flowers often terminates by bending the floral axis
just below the flower head, which is called bent-
neck. Parups and Voisey (1976) showed that thick-
ening of the pedicel takes place at a relatively late
stage in flower development and insufficient ligni-
fied pedicel lead to bent-neck. Insufficiently ligni-
fied pedicel remains rigid only because of the cell
turgidity and the smallest turbulences in water bal-
ance are manifested in this region of a cut rose stem,
producing bent-neck symptoms. They also reported
that spraying rose shrubs with phenolic compounds
before harvest could hasten lignification and pre-
vent the phenomenon (Parups & Voisey 1976). The
development of bent-neck is also considered to be
caused by vascular occlusion, which inhibits water
supply to the flowers (Van Doorn 1997). Vascular
occlusion is caused by the multiplication of bacteria
(Van Doorn et al. 1989; Jones & Hill 1993), air em-
boli (Durkin 1979), or unknown physiological re-
sponses (Marousky 1969). It has been reported that
resistance to bacteria and dry storage is involved in
cultivar variation in the vase life of cut roses (Van
Doorn & D’hont 1994).
Rose flowers are harvested at the bud stage,
and the vase life is one of the most important char-
acteristics. Cut roses held in water lack soluble car-
bohydrates that results in the suppression of petal
growth and incomplete flower opening (Ichimura et
al. 2003). The application of sugars to vase water
improves the quality of various cut flowers, includ-
ing roses (van Doorn et al. 1991; Ichimura et al.
2003). In addition, adding sucrose to cut flowers in-
creases the levels of glucose and fructose, but it has
little effect on the sucrose content in petals, indicat-
ing that sucrose translocated to petals from other or-
gans is metabolized to glucose and fructose and thus
accumulates in petal cells (Kaltaler & Steponkus
1976). In cut rose flowers, the leaves play an im-
portant role in maintaining rates of water uptake
through transpiration (Halevy & Mayak 1981), and
removal of these leaves reduces water uptake rates
and causes flowers to not fully open. Mayak et al.
(1974) showed that ability to close stomates in re-
sponse to water stress condition was decisive factor
in postharvest longevity. Adverse water relations
are associated with incomplete flower opening,
premature petal wilting, and bending of the pedicel
in roses (Doi et al. 1999). The leaves and stems of
cut flowers can also act as a source of soluble car-
bohydrates for the flower sink tissue. In cut chry-
santhemum flowers, soluble carbohydrates accumu-
lated in the leaves and stems were reported to affect
vase life (Ishikawa et al. 2006). In cut roses, soluble
carbohydrates accumulated in petals also affected
vase life (Ichimura et al. 2005). Chin and Sacalis
(1977) reported that 14C-sucrose, when taken up
into the xylem, moved rapidly into leaves and
flower heads of cut roses and that invertase located
in the xylem involved in the rapid hydrolysis of su-
crose. Horibe et al. (2014) showed that most of the
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Flower opening physiology of cut roses 11
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exogenously applied glucose first moved to leaves,
where it was converted to sucrose, and then synthe-
sized sucrose was translocated to petals as reported
in Eustoma (Shimizu-Yumoto & Ichimura 2007),
and rose and carnation (Paulin & Jamain 1982).
Plenty of soluble carbohydrates accumulate in leaves
after sugar treatment, but there seems to be partial
carbohydrate translocation to petals (Horibe et al.
2014). Therefore, promoting sugar translocation
from leaves to petals would improve cut flower qual-
ity and elevate the positive effects of sugar treatment.
More studies are still necessary to further understand
the functions of leaves of cut flowers in sugar metab-
olism and sucrose translocation.
DIURNAL RHYTHMIC GROWTH
OF CUT ROSES
Rhythmic flower opening is observed in many
plant species. The existence of endogenous rhyth-
mic opening is usually identified by placing flowers
in constant darkness or constant light as the circa-
dian clock continues despite these constant condi-
tions (Jones & Mansfield 1975). Some day-bloomer
species and night-bloomer species have an endoge-
nous rhythm of flower opening and closure (van
Doorn & van Meeteren 2003). However, changing
from light to darkness or vice versa is necessary for
flower opening in several species. The periods and
amplitude of circadian rhythm are known to
change without zeitgeber, such as changes of light
to darkness or vice versa (Jones & Mansfield 1975).
In the Asiatic hybrid lily, flower opening has been
shown to proceed irregularly if it was kept in con-
tinuous darkness, indicating the importance of
changing from light to darkness for appropriate tim-
ing of flower opening (Bieleski et al. 2000). In the
hybrid tea rose, Horibe et al. (2014) reported that
flower opening showed a diurnal rhythm under a 12-
h photoperiod and constant dark conditions, alt-
hough rhythmic flower opening under constant dark
was not as clear as that of cut flowers kept under 12-
h light and 12-h dark cycles. However, cut roses
maintained under constant light did not show rhyth-
mic growth and kept opening slowly until fully
opened. These results suggested that the rhythmic
opening of cut rose flowers is influenced by changes
of light to darkness or vice versa, in addition to other
circadian factors. The relationship between circa-
dian clock and hormones, light, and temperature af-
fecting rhythmic flower opening has been well re-
viewed by van Doorn and Kamdee (2014). However,
the mechanism of rhythmic flower opening has yet to
be elucidated. Some chemical reactions, which con-
nect the circadian oscillator and flower opening,
might be halted under constant light conditions. It,
therefore, seems that the opening of rose flowers
needs external stimuli, a change of light to darkness
or vice versa, to maintain its diurnal rhythm. Inter-
estingly, some volatile compounds of rose flowers
are emitted in a similar way. Emission of geranyl
acetate oscillated under 12-h light/dark conditions
but not in constant light, indicating that cyclic light
and darkness are necessary for diurnal volatile emis-
sion (Hendel-Rahmanim et al. 2007). Thus, it seems
that changes of light to darkness or vice versa play
a key role in flower opening in plants. However, Ev-
ans and Reid (1986) reported that rhythmic opening
of rose flowers was abolished upon placing flowers
in continuous light or darkness, while Doi et al.
(1999) reported that it was observed when flowers
were exposed to constant light and darkness. These
differences might result from differences between
rose cultivars in the mechanism of rhythmic flower
opening.
So, which endogenous mechanism governs the
rhythmic opening of rose flowers? With regard to the
function of carbohydrates in the diurnal rhythm of
rose flower opening, Evans and Reid (1988) reported
that the total carbohydrate content of petals remained
constant during a light–dark cycle, indicating its im-
portance in maintaining cell size, but it was not im-
plicated in controlling rhythmic opening. Resistance
to water movement or an inadequate water potential
gradient along the transport pathway leads to limited
water uptake, and the strength of the cell wall also
limits cell enlargement. In tulips, petal opening and
closure occur concomitantly with water transport and
both are regulated by reversible phosphorylation of
aquaporins (Azad et al. 2004). In addition, it has been
shown that cell-wall-loosening proteins, XTH and
expansins, are important in petal growth (Yamada
et al. 2009b). Further explantation of the roles of
these proteins in rhythmic flower opening will be an
interesting and necessary avenue to pursue.
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12 T. Horibe, K. Yamada
_______________________________________________________________________________________________________
PETALS AS THE SITE
OF PHOTOPERCEPTION
Several studies have indicated that flowers are
the site of photoperception and perceive red or/and
blue light (Saito & Yamaki 1967; Kaihara & Takimoto
1980, 1981a, b). In Calendula arvensis, its flower
opening and closing circadian rhythm followed the
light-dark cycle in a manner dependent upon which
flower had been exposed when the leaves were sub-
jected to a different light-dark cycle from the flow-
ers (van Doorn & van Meeteren 2003). In cut roses,
rose petals can perceive red and blue light and syn-
chronize their growth to photoperiods (Horibe &
Yamada 2014a; Horibe & Yamada 2014b; Horibe et
al. 2014), but it is still unclear which photoreceptors
play a role in receiving red and blue light and what
reactions are involved between perception of light
and rhythmic flower opening. Another report showed
that a relatively slow phytochrome reaction is in-
volved in the perception of the duration of light or
darkness (Lumsden 1991). Such a reaction might also
be involved in light perception in roses; however, it
is still not clear which wavelength is effective and
which photoreceptor perceives light in rose petals.
There are many reports showing that the light
condition affects several aspects of plant physiol-
ogy, including flower opening and volatile emis-
sion (Hendel-Rahmanim et al. 2007; Kaihara &
Takimoto 1980, 1981a, b). Red and blue light seem
to be perceived in petals and affect flower opening
and closing in some species. In Oenothera lamarck-
iana, flower opening was arrested by light, and it
was only effective when the wavelength was be-
tween 400 and 510 nm, which is, respectively, the
blue and green regions of the visible spectrum (Saito
& Yamaki 1967). Furthermore, red light was shown
to promote flower opening, but its effect was re-
versed by a subsequent exposure to far-red light in
Ipomoea nil (Kaihara & Takimoto 1980, 1981a, b).
In roses, it has been reported that the speed of flower
opening was delayed in cut flowers exposed to red
and blue light compared with those exposed to white
light (Horibe & Yamada 2014b), suggesting that ex-
posing cut flowers to specific wavelengths of light
might be useful for controlling flower opening.
Thus, understanding a cut rose flower’s response to
light stimuli might lead to the development of a new
method to improve quality. In addition, there is
a possibility that light increases petal temperature
by being absorbed by pigments in the petals, result-
ing in the promotion of petal growth. Depending on
petal anatomy and pigmentation, light can indeed
increase petal temperature (McKee & Richards
1998). In Portulaca plants, a rise in temperature re-
sulted in rapid flower opening, although light also
intensified the response (Ichimura & Suto 1998).
Changes in temperature of petals might also affect
petal growth of cut rose flowers.
CONCLUSION AND FUTURE PROSPECTS
In this review, we described cell morphology,
sugar metabolism, cell-wall-loosening proteins, aq-
uaporins, the mechanism of rhythmic flower open-
ing, and the perception of light in the context and
landscape of cut rose flower opening. However, fu-
ture research is warranted in these outlined topics as
well as in-depth analysis of their interrelatedness
and impact on cut rose flower opening and quality.
Until now, most research has focused on senescence
to improve the vase life of flowers, leading to the
invention of and utility of ethylene production/ac-
tion inhibitors. However, few studies have focused
on the physiology of petal growth, the perception of
light by petals, and the relationship between petal
growth and environmental conditions. Elucidation of
the mechanisms of flower opening would contribute
to enhanced quality and commercial production of
floricultural crops as well as greatly advance basic
scientific knowledge regarding plant biology.
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