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Eur. J. Hortic. Sci. 80(6), 316–321 | ISSN 1611-4426 print, 1611-4434 online | http://dx.doi.org/10.17660/eJHS.2015/80.6.7 | © ISHS 2015
Review article
German Society for
Horticultural Science
The physiology of Curcuma alismatifolia Gagnep. as a basis for
the improvement of ornamental production
S. Ruamrungsri1,2
1
2
Department of Plant and Soil Science, Faculty of Agriculture, Chiang Mai University, Chiang Mai, Thailand
H.M. The King’s Initiative Centre for Flower and Fruit Propagation, Chiang Mai, Thailand
Summary
Significance of this study
This review addresses the research on the physiology of Curcuma alismatifolia to improve the understanding of this plant, a tropical flower crop that has
become popular as a cut flower, a potted plant and a
garden plant. C. alismatifolia Gagnep., called the Siam
Tulip or Patumma, is widely cultivated as an ornamental Curcuma for cut flowers and potted plants because
of the attractive inflorescence with pink coma bracts
and long vase life. Thailand exports more than 3 million rhizomes to the world market. The review considers its distribution (widely in Thailand and Cambodia), growth cycle, flowering physiology, diurnal
photosynthesis, nitrogen metabolism (including with
N-sources, utilization, transports and N2 fixation) and
carbohydrate metabolism, which may be beneficial
for the improvement of crop production.
What is already known on this subject?
• C. alismatifolia is called ‘Siam Tulip’ which is known as
an ornamental pot plant and cut flower in the world
market. Rhizomes are exported from Thailand to
markets in temperate zone in December to January
and then they were forced to flower in May to late
summer. In general, temperature, light intensity,
fertilizer application and sunshine duration are
important factors for plant growth and development.
What are the new findings?
• Most of the environmental factors affecting growth
and development of this plant are summarized and
reviewed, including distribution and morphology,
growth cycle, flowering physiology and development,
diurnal photosynthesis, nitrogen metabolism,
carbohydrate metabolism, plant growth regulators
and post-harvest physiology.
Keywords
carbohydrate metabolism, flowering, nitrogen
metabolism, photosynthesis, rhizome quality
What is the expected impact on horticulture?
• These findings will be beneficial for C. alismatifolia
forcing and also for improvement of flower and
rhizome qualities by growers.
Distribution and morphology
Curcuma is one of the largest genera in the Zingiberaceae
family. This genus is in the tribe Zingibereae, which is widely
distributed in tropical Asia from India to South China, Southeast Asia, Papua New Guinea and Northern Australia. Thailand seems to be one of the areas richest in this genus (Larsen and Larsen, 2006; Sirirugsa et al., 2007). Approximately
38 species of Curcuma are now found in Thailand, separated
into 5 groups, i.e., 1) the “Alismatifolia” group of eight species, C. alismatifolia, C. gracillima, C. harmandii, C. parviflora,
C. rhabdota, C. sparganiifolia and two new species, found in
the northeastern and eastern region; 2) the “Cochinchinensis” group of two species, C. cochinchinensis and C. pierreana,
distributed in the north, southwest and eastern regions; 3)
the “Ecomata” group of seven species, C. bicolor, C. ecomata,
C. flaviflora, C. glans, C. singularis, C. stenochila and one new
species, distributed in the northern, northeastern, eastern
and southeastern regions; 4) the “Longa” group of thirteen
species, C. aeruginosa, C. amada, C. angustifolia, C. aromatic,
C. comosa, C. latifolia, C. leucorrhiza, C. longa, C. mangga, C.
rubescens, C. viridiflora, C. zanthorrhiza and C. zedoaria, found
widely in the north; and 5) the “Petiolata” group of eight species, C. aurantiaca, C. petiolata, C. roscoeana, C. rubrobracteata and four new species, found from the north to the peninsula along the western ranges (Sirirugsa et al., 2007).
Unlike C. longa (tumeric), C. zedoaria, C. aromatic, etc.,
which are species generally used as medicinal plants (Sabu
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and Skornickova, 2003), C. alismatifolia Gagnep. is widely
cultivated as an ornamental Curcuma for cut flowers and
potted plants because the attractive inflorescence has a pink
coma bract, called Siam Tulip or Patumma, with a long vase
life (Figure 1). This flower clone was first selected by Dr.
Pisit Woraurai from Chiang Mai University, and the famous
selected clone called ‘Chiangmai Pink’ was introduced as
an ornamental plant in early 1980, and nowadays is wellknown in the world market (Woraurai, 1991; Department
of Agricultural Extension, 1995; Wannakrairot, 1997). The
aboveground organs consisted of leaves and inflorescences.
There are two types of leaves, sheath leaves are former
sprouting with short and thick leaf blade and followed by
foliage leaves with elliptic shape, deep green and reddish
median vein. Stomata is mostly tetracyctic type, however,
pentacytic and hexacytic types were found in both upper and
lower surfaces. Guard cells are kidney shape and the cell size
in the adaxial is longer than the abaxial site. Stomatal density in the abaxial site was about 1,000–1,200 stomata mm-2
which was higher than in adaxial site (400–500 stomata
mm-2). The cuticle layer of upper leaf surface is about 10–12
µm thick and thicker than the lower leaf surface (13–15 µm
thick) (Anuwong et al., 2014b). Underground organs consist of two parts, i.e., the underground stem called a stubbed
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Ruamrungsri | The physiology of Curcuma alismatifolia Gagnep.
Figure 2. Stubby rhizome and storage
roots of Curcuma alismatifolia Gagnep.
Figure 2. Stubby rhizome and storage roots of Curcuma
opening occurs at about 11–13 WAP, usually in the middle
of the rainy season around July–August and during this period new rhizome formations start at underground part by
swelling of new rhizome and storage roots at the base of
pseudo-stem. The total nonstructural carbohydrate maximum accumulated in a new rhizome with 69.25 mg g-1 DW
and 286.52 mg g-1 DW in the storage roots. The new rhizome
reaches maturity at 23 WAP (Chidburee, 2008).
After the rhizome harvest, Thai growers generally stored
Figure 1. Inflorescence of Curcuma alismatifolia Gagnep. with
rhizome plants at room temperature (25 ± 2°C, 60% RH)
pink coma bracts and true flowers are presented in axil of
with good ventilation (Chidburee, 2008). Storage temperagreen bracts.
ture and duration have affected sucrose, fructose and glucose
Figure
Inflorescence
of Curcumaalismatifolia
Gagnep.
pink coma bracts
and concentration
true flowers are
presented
instorSucrose
decreased
when
rhizome1.with
2-3 buds that
will produce next season
leaves,withconcentrations.
axil
of green bracts.
age duration increased (Paz, 2003).
inflorescence
and roots (Apavatjrut et al., 1999). There are
three type of roots, i.e., 1) storage roots or tuberous roots
(T-roots) which were modified from contractile roots. The
Flowering physiology and development
terminal part of contractile roots are swollen and become
C. alismatifolia is classified as a quantitative long day
egg shape; 2) contractile roots which are long and thick
plant (Hagiladi et al., 1997), where a long day length advances
develop from the base of a new shoot; and 3) fibrous roots
or enhances flowering but the plants will eventually flowor capillary roots which are short and thin shaped, develop
er anyway (Hart, 1988). Changjeraja (2009) reported that
from storage roots when rhizome starts sprouting (Hagiladi
flower initiation of ‘Chiangmai Pink’ could be seen when the
et al., 1997; Honpakdee, 2010). Thailand exports approxishoot height was approximately 6–10 cm. The inflorescence
mately 2–3 million rhizomes to the world market, including
apex is shallowly domed and produces bracts on the dome
Japan, USA and The Netherlands. The standard size of a rhi(Figure 3A). When the shoot was 11–15 cm in height (about 8
zome for export to European countries and the USA is up to
WAP), the differentiation of inflorescence began (Figure 3B).
2 cm in diameter with 4 storage roots attached (Figure 2).
Pubuopiend (1992) revealed that the flower initiation and
development of ‘Chiangmai Pink’ consisted of nine stages,
i.e., 1) the vegetative stage; 2) the transition stage; 3) the
Growth cycle
initiation of the floral bract (Br); 4) the initiation of the first
For the regular growing season in Thailand, growers will
floral primordium (Pr); 5) the division of the floral primordiplant Curcuma in the early stage of the rainy season (April
um; 6) the initiation of petals (P); 7) the initiation of sepals
to May) when dormancy of rhizome naturally releases and
(Sp); 8) the initiation of androecium (A); and 9) the initiabud emerges. After planting, shoots will sprout within 2–3
tion of gynoecium (G). However, flower initiation with dome
weeks after planting (WAP), depending on rhizome size and
formation of ‘Shaarome Pink’ and ‘Kimono Pink’ has also
environmental condition. The days to shoot emergence debeen observed at a shoot height of 11–15 cm when plants
creased when the storage temperature increased, or longer
were grown in a greenhouse under minimum temperature of
storage duration (Criley, 2013). In ‘Chiangmai Pink’, plant
15°C. The developmental stages and flowering process from
grows rapidly and reaches a maximum of vegetative growth
floral bud initiation, organogenesis until anthesis were also
at 10–11 WAP (Chidburee et al., 2009). However, the first
investigated by Fukai and Udomdee (2005).
sign of flower initiation, with dome formation at shoot apex,
Growing seasons of C. alismatifolia in Thailand can be
was found when the shoot length is approximately 6–10 cm
divided into three periods, i.e., 1) early-season planting;
(approximately at 5–6 WAP) (Changjeraja, 2009). Floret
8 the
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Ruamrungsri | The physiology of Curcuma alismatifolia Gagnep.
Figure 3. (A) Flower development of C. alismatifolia ‘ChiangFigure 3. (A) Flower development of C.alismatifolia ‘Chiangmai Pink’, floral bud primordia initiation with dome
shape
at 5 weeks floral
after planting.
(B) Floral
bud differentiation atinitiation
6 weeks after planting
(Changjeraja,
2009). shape
mai
Pink’,
bud
primordia
with
dome
at 5 weeks after planting. (B) Floral bud differentiation at 6
weeks after planting (Changjeraja, 2009).
rhizome must be soaked in water to stimulate shoot emergence
(pre-germinated) before planting in hot weather (March). It will
flower in May and rhizomes will be harvested in the mild winter
of Thailand (December). (2) regular season planting (April or
May); flowering occurs in rainy season (July or August) about
2–3 months after planting depending on rhizome size under
the average temperature of 27°C, 90% RH and 13 h of sunshine
duration and rhizomes are harvested around December and
January. (3) off-season planting; rhizome must be carefully kept
in cool temperature (15°C) and 65–70% RH to retard bud emer10
gence. The year round climate condition of Thailand was shown
in Figure 4. Rhizome of ‘Chiangmai Pink’ can be kept under this
condition for 10–12 months. It cannot survive when stored at
9°C (Criley, 2013). Later planting can be done in August to October, flowering occurs in November to January under average
of 40% RH, 22°C and 11 h of sunshine duration (Hongpakdee
et al., 2010). However, shoot growth and inflorescence quality
of C. alismatifolia ‘Chiangmai Pink’ was retarded when planting
in off-season caused by many factors such as low temperature,
lower photosynthesis rate, short day length and low relative humidity as reported by Hongpakdee (2010).
In order to force good quality of inflorescence in the
off- season planting, in Thailand, a night break treatment by
supplementing with 100 Watt incandescent light bulbs for
2 h from 8:00–10:00 pm, could be performed (Ruamrungsri
et al., 2007). The photosynthetic rate (Pn) of control plant
(not given supplemental lighting) at night was approximately 0.81 µmol CO2 m-2 s-1 and it was significantly lower than
that of night break treatment with 1.59 µmol CO2 m-2 s-1 (Siritrakulsak et al., 2010). Although the night break treatment
could promote inflorescence qualities in off-season cropping, it decreased the formation of storage roots. Off-season
cropping in Thailand under short day length (11 h) without
the supplemental light reduced the plant growth and inflorescence qualities but significantly stimulated the formation
of rhizome and storage roots compared to regular season
production. The abscisic acid (ABA) in the leaves, rhizome
and storage roots was higher during off-season cropping,
while the level of trans-zeatin riboside was slightly higher
in the off-season plants than in the regular season plants
(Hongpakdee et al., 2010; Siritrakulsak et al., 2010). Kuehny
(2003) reported that an 8 h day length promoted dormancy
of C. petiolata, C. thorelii, C. cordata and C. alismatifolia but
increased the number of storage roots; however, the effects
of day length on vegetative shoot growth and development of
storage organs (rhizome and storage roots) is not the same
for all Curcuma species.
Diurnal photosynthesis
Siritrakulsak et al. (2010) measured the photosynthetic
rate of C. alismatifolia ‘Chiangmai Pink’ at the 1st – 4th fully
expanded leaf (L1–L4 stages) using portable automatic leaf
photosynthesis measurement when plants were grown under average temperatures 33/28°C (day/night), relative humidity (RH) 61% and 13 h of day length every two hours from
6:00 am. to 9:00 pm. At all growth stages (L1–L4), the photosynthesis was greatest at 10:00 am with 6.99 µmol m-2 s-1
(at L1), 6.13 µmol m-2 s-1 (at L2), 6.58 µmol m-2 s-1 (at L3) and
5.71 µmol m-2 s-1 (at L4); then continuously decreased in the
afternoon, caused by the increase of photosynthetically active radiation (PAR) between 12:00 am – 2:00 pm. Although
photosynthetic rate at each stage did not differ too much, dry
weight accumulation increased continuously. Total leaf dry
weights were increased continuously from 0.51 g (at L1) to
2.97 g (at L4). The chlorophyll fluorescence was also measured using an Exciting Chlorophyll Fluorescence Meter. It
Figure 4. Temperature, humidity and sunshine duration in Thailand (Chidburee,
2008).
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Figure 4. Temperature, humidity and sunshine duration in Thailand (Chidburee, 2008).
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Ruamrungsri | The physiology of Curcuma alismatifolia Gagnep.
was found that the chlorophyll fluorescence of the 3rd leaf
(L3) was nearly constant in the range of 0.77–0.78 Fv/Fm.
The stomatal resistance continuously decreased when the
light intensity increased from 200 to 500 µmol m-2 s-1 PPFD,
then remained constant between 500–800 µmol m-2 s-1 PPFD
and slightly increased thereafter (Siritrakulsak, 2010).
Nitrogen metabolism
The whole plant dry matter consists of 2–4% N. In C. alismatifolia, the rhizome is a major organ for N storage, which
accumulated approximately 2–4% of N, while the storage
roots stored only 1–2% N and were the major organ for carbohydrate storage. Arginine is the predominant free amino acid in the rhizome, and glutamic acid is the major free
amino acid in the storage roots (Ruamrungsri et al., 2001).
During the growing period, nitrogen uptake [from Na15NO3
and (15NH4)2SO4 sources] was approximately 4–5 mg g-1 DW
during root emergence until the two leaves were expanded,
then 9–10 mg g-1 DW with the two expanded leaves until
the first floret opening. The absorption decreased to 7–8
mg g-1 DW from the first floret opening until rhizome harvest
(Ruamrungsri et al., 2006). However, the daily gain of N was
constant throughout the growing period. The absorbed-N at
10 weeks after planting translocated to accumulate in the
leaves and roots, and some was transported to the flowering organs at 13 weeks after planting. At harvest, 41% of the
absorbed-N was recovered in the new rhizome and 17% in
the new storage roots (Khuankaew et al., 2010). The high N
supply increased the growth and development of this plant,
including the number of inflorescences and the new rhizome formation. The protein and total free amino acids also
increased in both the rhizome and the storage roots, which
indicated the assimilation of N into protein and free amino acids. The protein profile in the Curcuma rhizomes was
separated by SDS-PAGE, and low molecular weight peptides
of 12.0 kDa and 10.6 kDa were detected, with minor bands
at 29.1, 23.8 and 16.8 kDa. The 12.0 kDa and 10.6 kDa are
two major soluble proteins in rhizome and they were different from protein in storage roots (Anuwong et al., 2014a).
The increased N supply led to decreased starch content in
this plant which Marchner (1986) reported that the carbohydrates are required for nitrate reduction in higher plant.
Moreover, Ohtake et al. (2006) found that a reduced N supply increased the accumulation of carbohydrate in both the
rhizome and the storage roots of C. alismatifolia. A similar
link between N deficiency and carbohydrate content was
also found in Narcissus roots and scales (Ruamrungsri et
al., 1996). N-deficient leaves were yellowish; the plant was
stunted; and the inflorescence and rhizome production was
decreased under N deficiency (Ruamrungsri et al., 2003).
Generally, higher plants take up both NO3- and NH4+
and convert them to organic N forms such as amino acids,
proteins or nucleic acids (Mengel and Kirkby, 1987). When
plants are supplied with NH4+ or NO3-, they may show different physiological responses that depend on the species, light
intensity and temperature (Edwards and Horton, 1982).
Inkham et al. (2011a) reported that NH4+-fed Curcuma plants
accumulated significantly more total free amino acids than
NO3--fed plants. The plant height and leaf area of plants supplied only with NO3- was higher than in plants supplied only
with NH4+ or with a mixed N (NO3- + NH4+) supply; however,
the chlorophyll content and total dry weight was not significantly different between the NO3--fed plants and plants fed
a mixed N supply. The experiment also revealed that a relatively low night temperature of 18°C significantly increased
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nitrate reductase (NR) activity in the fibrous roots of C.
alismatifolia compared with a night temperature of 24°C. The
relationship between NR activity and NO3- content in plants
depends on the exogenous NO3-, and the increase in NR
activity actually was affected by the lower temperature of root
environment, or medium (Aslam et al., 1976; Deane-Drummond et al., 1980).
The N requirement for C. alismatifolia could be predicted
using leaf analysis. The critical nitrogen level in field grown
plants at flowering stage was established at 1.51% in leaf N,
which corresponded to 90% of the maximum yield (Inkham
et al., 2011b). The N concentration in various plant tissues
increased with increasing N supply. The N application rates
affected the growth, dry weight, leaf N concentration and leaf
chlorophyll content.
The association between N2 fixing and IAA synthesis by
the endophytic bacterial symbiosis in C. alismatifolia ‘Chiangmai Pink’ was first discovered by Thepsukhon et al. (2013).
Seven N2 fixing endophytic bacteria were isolated from the
leaf, four isolated from the leaf base and two from the rhizome. It was found that the isolates from the leaf base could
fix N2 higher than the other isolates. This efficacy isolate for
N2 fixation was identified as Bacillus drentensis, a gram-negative bacterium with a round shape, showed the highest N2
fixation at 4.2 nmol C2H4 10-6 cells h-1, and another isolate was
identified as Sphingomonas pseudosanguinis which showed
the highest IAA synthesis at 296 µL µg-1 protein. After inoculation of these endophytic bacteria into C. alismatifolia
plantlets (derived in vitro) before planting using sterile media, it was found that the plant height, number of leaves per
plant and dry weight at 1 and 2 months after planting was
enhanced and new rhizome qualities were better than
non-inoculated plantlets (Thepsukhon et al., 2013).
Carbohydrate metabolism
The storage roots primarily stored carbohydrates for use
in growth in the next season. The assimilation and transport
of nitrogen (N) and carbon (C) in C. alismatifolia was studied
using 15NH4+, 15NO3- and 13CO2, the abundance of 15N and 13C
in each plant organ was determined using an elemental
analyzer coupled to an isotope-ratio mass spectrometer. The
C stored in the old storage roots was used rapidly during the
first 10 weeks after planting. The total C was approximately 0.5 g C g-1 DW at planting and 0.4, 0.5, 0.5 and 0.5 g C g-1
DW at 10 (first shoot development stage), 13 (the first floret
blooming), 21 (inflorescence senescence) and 32 (rhizome
harvest) WAP, respectively. The daily gain of C accumulation
was high, between 10–13 WAP, depending on photosynthesis (Khuankaew et al., 2010). After the rhizome harvest, the
stubbed rhizome and storage roots contained starch approximately 91 and 68 mg g-1 FW, and approximately 17 and
16 mg g-1 FW of total soluble sugar, respectively. During the
storage period from December (20/10°C day/night temperature) to March (30/25°C day/night temperature), the carbohydrate in these organs was hydrolyzed, and their contents
continuously decreased (Ruamrungsri et al., 2001). However,
when plants were grown in relatively low temperature, 18–
20°C throughout the growing period, the total non-structural
carbohydrate in the leaves increased, but the plant height decreased at 8 WAP (Changjeraja et al., 2007). Growing plants
under a short day length (7 h) decreased the total non-structural carbohydrate and starch concentration in new rhizome
and storage roots compared with growing under a 10 and
13 h day, indicating the effect of day length on carbohydrate
accumulation (Chidburee, 2008).
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Plant growth regulators
The marketable size of potted plants is generally about
1.5–2 times of pot height (Nelson, 1998). C. alismatifolia is
usually produced excessively tall, therefore, plant growth
retardant can be used for the production of marketable pot
Curcuma. Optimum concentration of paclobutrazol (over 20
mg a.i. pot-1) or 10 mg a.i. pot-1 of uniconazole can be used
for C. alismatifolia by drench to reduce plant height to obtain a marketable height for potted plant, however, number
of flowering stems, post production life and post production
stretching were not affected (Sarmiento and Kuehny, 2000;
Kuehny et al., 2005). Gibberellin application at 200–600
mg L-1 delayed shoot emergence and flowering but did not
affect the flower numbers (Sarmiento and Kuehny, 2003).
Post-harvest physiology
Vase life of C. alismatifolia was about 14–20 days, depending on harvest date. The inflorescence is chilling-sensitive. It cannot be stored dry but can be stored in water at 7°C
for about 6 days. The respiration of inflorescence was steady
level for several days, followed by a decrease during the vase
period. The water uptake rate declined from the first day of
vase life up until 9 days of vase life which was caused by the
blockage in the xylem. Lack of carbohydrate could also be a
cause of bract browning (Bunya-atichart et al., 2004).
Concluding remarks
Considerable research on Curcuma alismatifolia Gagnep.,
mostly ‘Chiangmai Pink’, has been conducted in the last ten
years to understand the physiology of this plant, including
distribution, growth cycle, flowering process, photosynthesis, nitrogen metabolism, carbohydrate metabolism and
postharvest physiology. Because the world market demand
for rhizomes and cut flowers continuously increases year
by year, and new hybrids are also requested by wholesalers,
the basic knowledge derived from these studies will provide
information on how to improve plant growth, inflorescence
quality and rhizome yield, and can be modified for use with
other Curcuma hybrids. Further studies should investigate
year-round rhizome production and molecular techniques
for vase life improvement and introducing more color for
new hybrids.
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Addresses of author:
S. Ruamrungsri1,2
1 Department of Plant and Soil Science, Faculty of Agriculture,
Chiang Mai University, Chiang Mai 50200, Thailand
2 H.M. The King’s Initiative Centre for Flower and Fruit
Propagation, Chiang Mai 50230, Thailand
E-mail: [email protected]
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treatment and fertilizer application on physiological responses of
Curcuma alismatifolia Gagnep. Ph.D. Thesis, Graduate School, Chiang
Mai University, Chiang Mai. 225 pp.
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