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Chemical Identity of a Rotting Animal-Like Odor Emitted from the Inflorescence of the Titan Arum (Amorphophallus titanum)

DOI:10.1271/bbb.100692
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Mika Shirasu
Mika Shirasu
Mika Shirasu
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Kouki Fujioka at The Jikei University School of Medicine
Kouki Fujioka
Satoshi Kakishima at Showa University
Satoshi Kakishima
Shunji Nagai
Shunji Nagai
Shunji Nagai
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Abstract and Figures

The titan arum, Amorphophallus titanum, is a flowering plant with the largest inflorescence in the world. The flower emits a unique rotting animal-like odor that attracts insects for pollination. To determine the chemical identity of this characteristic odor, we performed gas chromatography-mass spectrometry-olfactometry analysis of volatiles derived from the inflorescence. The main odorant causing the smell during the flower-opening phase was identified as dimethyl trisulfide, a compound with a sulfury odor that has been found to be emitted from some vegetables, microorganisms, and cancerous wounds.
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Chemical Identity of a Rotting Animal-Like Odor Emitted
from the Inflorescence of the Titan Arum (Amorphophallus titanum)
Mika SHIRASU,1Kouki FUJIOKA,2Satoshi KAKISHIMA,3Shunji NAGAI,4Yasuko TOMIZAWA,5
Hirokazu TSUKAYA,6Jin MURATA,3Yoshinobu MANOME,2and Kazushige TOUHARA1;y
1Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences,
The University of Tokyo, Tokyo 113-8657, Japan
2Department of Molecular Cell Biology, Institute of DNA Medicine, Jikei University School of Medicine,
Tokyo 105-8461, Japan
3Botanical Gardens, Graduate School of Science, The University of Tokyo, Tokyo 112-0001, Japan
4National Cancer Center, Hospital East, Chiba 277-8577, Japan
5Department of Cardiovascular Surgery, Tokyo Women’s Medical University, Tokyo 162-8666, Japan
6Department of Biological Science, Graduate School of Science, The University of Tokyo, Tokyo 113-0033, Japan
Received September 28, 2010; Accepted November 3, 2010; Online Publication, December 7, 2010
[doi:10.1271/bbb.100692]
The titan arum, Amorphophallus titanum, is a flower-
ing plant with the largest inflorescence in the world. The
flower emits a unique rotting animal-like odor that
attracts insects for pollination. To determine the chemi-
cal identity of this characteristic odor, we performed gas
chromatography-mass spectrometry-olfactometry anal-
ysis of volatiles derived from the inflorescence. The
main odorant causing the smell during the flower-
opening phase was identified as dimethyl trisulfide, a
compound with a sulfury odor that has been found to be
emitted from some vegetables, microorganisms, and
cancerous wounds.
Key words: Amorphophallus titanum; odor; gas chroma-
tography-mass spectrometry; olfactometry;
dimethyl trisulfide
The genus Amorphophallus is well known for the
characteristic odor of its inflorescence.
1)
Among the
species of the genus Amorphophallus,Amorphophallus
titanum (Becc.) Becc. ex Arcangeli is famous for the
large size of the inflorescence (Fig. 1A) and for emitting
a rotting animal-like odor.
2,3)
This odor probably attracts
pollinators such as carrion beetles and flies.
1)
Previous
studies using gas chromatography-mass spectrometry
(GC-MS) have identified several odorants, including
dimethyl oligosulfides, that are emitted from A. tita-
num,
1)
but it is not certain whether these odorants reflect
the odor of the flower as humans experienced it. In
addition, due to the rarity of flowering events, detailed
study of this species was limited until recently. In the
Botanical Gardens of The University of Tokyo, on July
22, 2010, we had an opportunity to analyze the smell of
the inflorescence of an A. titanum plant. The GC-MS-
olfactometry (GC-MS-O) technique allowed us to
analyze emitted odorous compounds that contribute to
the rotting animal-like smell during the flowering
period.
First we evaluated the intensity and quality of the
odors emitted from the inflorescence of A. titanum
during flowering by human nose (Fig. 2A). At the
beginning of flowering, a faint rotten fruit-like odor was
detected occasionally. Then the odor emitted from the
flower gradually intensified. During full opening of the
spathe, a strong rotting animal-like odor was emitted
constantly. In addition, infrared radiation from the
surface of the inflorescence was measured with a
thermograph (Neothermo TVS-600; Avionics Japan,
Tokyo), as described elsewhere.
4,5)
The odor became
stronger with heat production from the spadix, as
previously reported (Fig. 2B and C).
3,6)
After the peak
of the spadix temperature, the inflorescence began to
secrete a fluid from the spadix in which a rotten fish-like
odor was sensed.
Next we collected volatile compounds emitted from
the A. titanum. The volatiles derived from the inflor-
escence were absorbed directly to Carboxen/PDMS
(Carboxen/Polydimethylsiloxane) SPME (solid phase
micro extraction) fibers (SUPELCO, Bellefonte, PA)
that had been placed inside of the inflorescence from
21:00 to 23:00 on July 22 (Figs. 1B(a) and 2A). The
compounds on the SPME fibers were then analyzed by
GC-MS-O which enabled us to examine the mass spectra
and odor qualities of individual GC-separated odorants
simultaneously. Shimadzu GCMS-QP2010 (Shimadzu,
Kyoto) (a stabilwax column of 60 m 0.32 mm i.d.
with a film thickness of 0.5 mm) was combined with a
sniffing port equipped with a Sniffer9000 system
(Brechbuhler, Houston, TX) in splitless mode (MS and
sniffing port at ratio of 1:4.7). The column temperature
was programmed to rise at 5 C/min from 50 C (2-min
hold) to 230 C (30-min hold) (total run time, 68 min).
The interface temperature was maintained at 200 C and
the ion source temperature at 230 C. Mass spectra were
obtained in full scan mode (range 20–400) by electron
impact using the NIST library database.
yTo whom correspondence should be addressed. Fax: +81-3-5841-8024; E-mail: ktouhara@mail.ecc.u-tokyo.ac.jp
Abbreviations: GC-MS, gas chromatography-mass spectrometry; GC-MS-O, GC-MS-olfactometry; TIC, total ion chromatogram; RT, retention
time; DMTS, dimethyl trisulfide; DMDS, dimethyl disulfide
Biosci. Biotechnol. Biochem.,74 (12), 2550–2554, 2010
Communication
Figure 3A shows total ion chromatograms (TIC) of a
SPME-absorbed sample collected by the method shown
in Fig. 1B(a). The odor characters sensed at the sniffing
port are described under the chart. GC-MS-O analysis
and evaluation of odors were performed by three
persons. The sensory characters of the odor-positive
peaks and the identified odorants are summarized in
Fig. 3D. The characteristic rotting animal-like surfury
odor, which was identical to the odor we sensed in the
inflorescence during the opening of the spathe, came
out at a retention time (RT) of 18.79 min. The mass
spectrum of the peak predicted the structure of dimethyl
trisulfide (DMTS) (Fig. 3C). The mass spectrum and the
retention time of authentic DMTS (Wako, Tokyo) were
identical to those of the peak compound, confirming
that the sulfury odor at RT ¼18:79 min was DMTS
(Fig. 3C).
In addition, the gaseous odor (RT ¼9:06 min) was
identified as methyl thiolacetate, and the cheesy, foot-
like valerian odor (RT ¼25:93 min) was identified as
isovaleric acid (Fig. 3A). The green odor at RT ¼16:19
could not be identified due to low concentration or to
overlapping peaks in the TIC. Dimethyl disulfide
(DMDS), which has been reported to be a major odorant
emitted from A. titanum, was also detected abundantly
at RT ¼9:80 min, but we could not sense the odor by
GC-MS-O analysis due to a high threshold,
7,8)
suggest-
ing that the contribution of DMDS to human olfactory
perception is not significant. The presence of a large
amount of DMDS, however, is plausible, because
DMDS is thought to be a precursor of DMTS which is
biosynthesized from methionine or S-methyl-L-cysteine
sulfoxide via methanethiol, which was also detected by
GC-MS (Fig. 3A).
9,10)
Considering that GC-MS-O anal-
ysis directly identifies crucial volatiles that contribute to
the quality of the smell that humans sense, these results
suggest that the main odorous component of A. titanum
is DMTS. GC-MS-O analysis of another flowering
A. titanum cultivated in a greenhouse at Flower Park
Kagoshima gave the same results (flower opening on
August 2, 2010) (data not shown).
At the end of the flower-opening phase, the odor
quality of the inflorescence changed gradually following
secretion of the odorous fluid from the spadix. The fluid
secreted from the spadix was collected from 1:00 to 3:00
on July 23, and head-space volatile compounds from a
10 ml sample enclosed in a 40 ml glass vial were absorbed
to SPME fibers for 7 h (Fig. 1B(b)). GC-MS-O analysis
of the SPME sample showed a strong rotten fish-like
odor similar to the odor we sensed at the end of the
flower-opening phase at RT ¼3:33 min, and this was
identified as trimethylamine (Fig. 3B, inset). Green,
burnt odor (RT ¼6:13 min) was identified as 3-methyl
butanal, and a vinegary odor (RT ¼20:47 min) as acetic
acid (Fig. 3B).
Time Event Odor quality
14:00 Opening of the spathe Slight rotten fruit-like odor
16:00
18:00
Yellow pickled radish
Spathe full opened Rotting animal-like odor
20:00
22:00 Spadix warming phase
0:00
Fluid exuded from the spadix
2:00
Rotten fish, Rotten egg
4:00
6:00
8:00 Closing of the spathe
Strong rotting animal-like odor
Rotten egg
daytime
nighttime
daytime
28oC35oC
19:47
0:47
ABC
18:00
22:00
2:00
6:00
-2
0
2
4
6
28
30
32
34
36
Spadix temperature (oC)
16:00
20:00
0:00
4:00
8:00
Spadix temp - ambient temp (oC)
July 22
July 23
Fig. 2. Scheme of the Flowering Behavior, Odor Quality and Thermogenesis of A. titanum.
(A) Flowering events and characteristic odors of A. titanum. The darkness of the gray indicates the intensity of the rotting animal-like odor.
(B) Time course record of spadix temperature (black line). Difference between the spadix and the ambient temperature (red line).
(C) Representative thermographic images (top, taken at 19:47 on July 22, 2010; bottom, taken at 0:47 on July 23, 2010). Scale bar, 20 cm.
Spadix
Spathe
AB
Fluid
Gas
SPME
SPME
(a)
(b)
Spadix
Spathe
Fig. 1. Odor Sampling from a Flower of Amorphophallus titanum.
(A) Full opening of the spathe of an A. titanum with a height of
1.6 m in the Koishikawa Botanical Gardens in July 2010. Scale bar,
20 cm. (B) Methods of collecting volatiles emitted from A. titanum.
(a) Volatile compounds from the inflorescence were directly
absorbed to SPME fibers placed between the spadix and the spathe.
(b) A fluid secreted onto the spadix was collected, and the head-
space volatiles from the fluid were absorbed to SPME fibers. Scale
bar, 20 cm.
Odor from a Flower of the Titan Arum 2551
Finally, we attempted to evaluate flower odor objec-
tively by using an electronic nose, FF-2A (Shimadzu,
Kyoto).
11,12)
The device contains electronic sensors with
various sensitivities and selectivities for volatile com-
pounds, and is standardized with nine gases (hydrogen
sulfide, methylmercaptan, ammonia, trimethylamine,
propionic acid, butylaldehyde, butylacetate, toluene,
and heptane), the odor quality of which can be
categorized into nine groups (hydrogen sulfide, sulfur,
ammonia, amine, organic acid, aldehyde, ester, aromatic
group and carbon hydrate). The flower smell was
collected directly into a 2 L tedlar bag (SUPELCO,
Bellefonte, PA) with a sampling pump (GL Sciences) at
21:00 on July 23. The collected air was diluted 5-fold
with odorless nitrogen gas and injected into the FF-2A.
Various concentrations of DMTS and DMDS were also
applied to the device. The virtual odor index in terms of
the nine aromatic categories is plotted in Fig. 4. For the
sample of A. titanum, the sulfur category was identified
as the highest odor index, and organic acid, aldehyde,
amine, and ester categories constituted lower index
categories (Fig. 4A). In a series of diluted DMTS, the
chart pattern of 0.01 ppm DMTS was similar to that of
the A. titanum sample (Fig. 4), which was fairly
consistent with the approximate concentration of DMTS
emitted as calculated at the basis of the GC-MS analysis
(data not shown). The chart pattern of DMDS was also
similar to that of the A. titanum sample, but the overall
odor intensity was weaker than that of DMTS (see
Fig. 4B and E). These results again confirm that DMTS
is the major contributor to the flower smell for human
olfactory sensation.
In conclusion, simultaneous evaluation of odor qual-
ity and the molecular masses of volatiles by GC-MS-O
enabled us to identify DMTS as the main odorant that
causes the rotting animal-like odor of A. titanum during
CD
126
15 32
45
64
79
111
100
80
60
40
20
0
20 40 60 80 100 120
m/z
Intensity (%)
126
32
45
64
79
111
100
80
60
40
20
0
20 40 60 80 100 120
m/z
Intensity (%)
2 4 6 8 10 12 14 16 18 20 22 24 26 28 30
0.0×10 -00
1.0×10 07
2.0×10 07
Time (min)
Intensity
Green
Sulfury
Valerian
Gaseous
A
S O SSS
O
OH
Gas-SPME
RT=18.8 min
Authentic DMTS
B
2 4 6 8 10 12 14 16 18 20 22 24 26 28 30
0.0×10 -00
1.0×10 07
2.0×10 07
Time (min)
Intensity
Rotten fish
Acidity
Sulfury
Green, burnt
O
OH
O
N
Fluid-SPME
Gas Fluid
3.33 Rotten fish Trimethylamine - ++
6.13 Green, burnt 3-Methyl-butanal - +
9.06 Gaseous Methyl thiolacetate + -
16.19 Green + -
18.79 Surfury Dimethyl trisulfide ++ +
20.47 Acidity Acetic acid - +
25.93 Valerian, cheese, feet Isovaleric acid + -
RT Odor character Odorant Odor intensity
2 3 4 5
0
5.0×10 06
1.0×10 07
1.5×10 07
TIC
2 3 4
0
5.0×10 06
1.0×10 07
1.5×10 07
5
TIC
m/z
EI
C
EI
C
SCH3H
SS
Fig. 3. GC-MS-O Analysis of SPME-Absorbed Head-Space Volatiles Emitted from A. titanum.
(A) Total ion chromatogram of volatile compounds absorbed to SPME fibers by the method described in Fig. 1B(a). Characteristics of odors
sensed at the sniffing port of GC-MS-O are described at the bottom of the chart. (B) Total ion chromatogram of head-space volatiles emitted from
the fluid of spadix, as described in Fig. 1B(b). Inset in (A) and (B) is the close-up TIC from 2 min to 5 min. The light gray and dark gray lines
indicate extracted ion chromatograms of the molecular ion peaks of trimethylamine (m=z59) and methanethiol respectively (m=z48)
respectively. (C) Mass spectrum of the peak at 18.8 min of TIC in Fig. 3A (top). Mass spectrum of authentic DMTS (bottom). (D) Retention
times (RTs), odor characters, and chemical identities of odor-positive peaks by GC-MS-O analysis. The intensities of the odors at the odor-
positive peaks in Fig. 3A (odor intensity, Gas) and 3B (odor intensity, Fluid) are categorized into three groups: not detected (), slight (þ),
strong (þþ).
2552 M. SHIRASU et al.
the opening of the spathe. Trimethylamine was found to
be the odorant that caused the rotten-fish odor at the end
of flowering. We also identified several other com-
pounds contributing to the odor of the inflorescence,
including methyl thiolacetate, 3-methyl butanal, acetic
acid, and isovaleric acid.
DMTS has been reported to be present in volatiles
emitted from vegetables such as cooked onion and
cabbage, decayed meats, and fermented food and drink,
which usually cause fly attraction.
13,14)
Indeed, oligo-
sulphides emitted from the flower of dead-horse arum
(Helicodiceros muscivorus) have been reported to be
attractants for flies,
15)
suggesting that A. titanum also
fools flies into pollinating it by mimicking the odors of
fermented products and rotting animal bodies. On the
other hand, an interesting coincidence is that DMTS is
known to be the main source of the malodor of fungating
cancer wounds in human.
16)
Indeed, the odor index
pattern of the head-space volatiles of a gauze pad placed
on a breast cancer wound was very similar to that of
A. titanum on electronic nose FF-2A (Fig. 4G). It is an
intriguing question how mechanisms of producing
DMTS have been acquired in various organisms as a
signal for various purposes during the process of
evolution.
Acknowledgment
We are grateful to Tadashi Yamaguchi (Botanical
Gardens, Graduate School of Science, the University of
Tokyo) for the photograph of A. titanum in Fig. 1A.
This research was approved by the Research Ethics
Committee of the University of Tokyo. It was supported
in part by grants from the Ministry of Education,
Culture, Sports, Science, and Technology (MEXT) of
Japan.
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... Moreover, it serves as a landing or departing platform for the attracted insects (Gibernau et al., 2004). In Amorphophallus, the reported thermogenic zones are consistently both the male flower zone and the appendix Lamprecht & Seymour, 2010;Shirasu et al., 2010;Skubatz et al., 1990). ...
... To date, thermogenesis has been investigated in only 9 out of 237 Amorphophallus species Handayani et al., 2020;Kakishima et al., 2011;Lamprecht et al., 2002;Lamprecht & Seymour, 2010;Prakash & Nayar, 2000;Shirasu et al., 2010;Skubatz et al., 1990;Teijsmann & Binnendijk, 1862;van der Pijl, 1937;Wagner et al., 1998). It has been proposed that thermogenesis in the appendix serves improved scent volatilisation Handayani et al., 2020;Lamprecht & Seymour, 2010;Seymour, 2010), whereas thermogenesis in the male flower zone might also offer heat reward to pollinating insects (Handayani et al., 2020;Lamprecht et al., 2002;Seymour, 2010). ...
... Moreover, although A. krausei Engl. (Wagner et al., 1998), A. muelleri (van der Pijl, 1937, A. paeoniifolius (Handayani et al., 2020;Lamprecht et al., 2002;Lamprecht & Seymour, 2010;Prakash & Nayar, 2000) and A. titanum Lamprecht & Seymour, 2010;Shirasu et al., 2010) showed a significant temperature increase, only a moderate temperature increase could be observed in A. bulbifer (Roxb.) Blume, A. forbesii Engl. ...
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... The most common odors describe it as smelling like a rotting animal, a dead mouse, foul, and sulfur-like during flowering. Though produced simultaneously, the individual volatile molecules emitted during female flowering include: dimethyl disulfide (garlic-like odor 8 ), dimethyl trisulfide (foul odor 9 ), methyl thioacetate (sulfurous odor 10 ), and isovaleric acid (cheesy, sweaty odor 10,11 ). The diffusion of volatile molecules from the flowers is enhanced by thermogenesis. ...
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... The scents emitted by Amorphophallus species are reminiscent of carrion, various forms of excrements, fish, sewerage, nauseating gases, rancid cheese, fermenting fruit and mushrooms. [34][35][36][37][38][39][40][41] Table S1 lists all the investigated Amorphophallus species, the analyzed voucher and sampling time and the identified scent compounds in their relative amount as well as the subjective perception. ...
... Dimethyl oligosulphides are characteristic of the decomposition of various organic matters, ranging from sulfur-rich vegetables, to cancerous wounds and most importantly cadaveric decomposition and carnivore dung. 10,41,44 They are released in various plant lineages and represent well-known attractants for various copro-necrophagous beetles and flies. [45][46][47] Furthermore, two distantly related Amorphophallus clades, comprising a handful of species each, were found to be characterized by the emission of benzenoid compounds, which are considered to be strongly evolutionarily constrained. ...
... The documented variation can obviously at least partly be accounted for by different study methodologies 37,38,40 or because of different sampling times or sample overloads, etc. 38 Particularly, the sampling time seems to be a critical aspect, as the variation in scent composition may strongly vary during anthesis. 13,38,41,55 Thus, whenever possible, a consistent sampling protocol was ensured, minimizing the influence of the sampling time. 38 However, some individuals reveal a broader intraspecific variation or scent polymorphism. ...
Odor polymorphism in deceptive Amorphophallus species - a review: Odor polymorphism in Amorphophallus
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Some plant lineages, such as Araceae and Orchidaceae, have independently evolved deceptive flowers. These exploit the insect’s perception and deceive the insects into believing to have located a suitable opportunity for reproduction. The scent compounds emitted by the flowers are the key signals that dupe the insects, guiding them to the right spots that in turn ensure flower pollination. Most species of the genus Amorphophallus of the Araceae emit scent compounds that are characteristic of a deceit, suggesting a specific plant pollinator interaction and according odors. However, only a few clear evolutionary trends in regard to inflorescence odors in Amorphophallus could be traced in previous studies – an intriguing result, considered the multitude of characteristic scent compounds expressed in Amorphophallus as well as the key function of scent compounds in deceptive floral systems in general. At least two factors could account for this result. (1) The deceptive pollinator-attraction floral system, including the emitted scent compounds, is less specific than assumed. (2) An evolutionary trend cannot be discerned if the intraspecific scent variation (odor polymorphism) exceeds the interspecific odor variation. Therefore, we discuss the potential deceptive function of the emitted scent compounds, in particular those that are related to cadaveric decomposition. Moreover, we review the data about emitted scent compounds in Amorphophallus with a focus on putative odor polymorphism. Upon examination, it appears that the emitted scent compounds in Amorphophallus are highly mimetic of decomposing organic materials. We show that several species display odor polymorphism, which in turn might constitute an obstacle in the analysis of evolutionary trends. An important odor polymorphism is also indicated by subjective odor perceptions. Odor polymorphism may serve several purposes: it might represent an adaptation to local pollinators or it might assumingly prevent insects from learning to distinguish between a real decomposing substrate and an oviposition-site mimic.
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... The atmosphere sampling instrument (QC-1S) was used for odor collection (Beijing Keanlaobao New Technology Co., Ltd., Beijing, China); the odor also needed to be filtered by the drying column filled with activated carbon before it could be absorbed into the adsorption tubes, and odorless teflon tubes were used for the connection between the adsorption tubes, drying column and atmosphere sampling instrument. After connecting the instruments, titan arum volatiles were collected by referring to the method of a previous study [10]. The top of the teflon tube was inserted between the spathe and the spadix, as shown in Figure 2a. ...
... Amorphophallus has a rich morphological diversity; almost every plant organ shows remarkable variation, and plant size is probably one of the most obvious variable characteristics [14]. The titan arum is one of the most iconic members of Amorphophallus, and some studies have shown that the main volatile compounds of the titan arum flower are dimethyl disulfide and dimethyl trisulfide, and the odor similar to rotting animals comes from dimethyl trisulfide [10,15]. In addition to dimethyl disulfide and dimethyl trisulfide, extremely small amount of dimethyl tetrasulfide can also be produced in some species of Amorphophallus (including A. titanum); these sulfur compounds are also referred to as dimethyl oligosulphides and often described as having the smell of urine and rotten meat and vegetables [1,2,16]. ...
An Analysis of Volatile Compounds and Study of Release Regularity in the Flower of Amorphophallus titanum in Four Periods
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  • Apr 2023
Titan arum (Amorphophallus titanum) is a rare and endangered plant in the world. It has a huge flower and releases a repulsive odor like a corpse. On the evening of 23 July 2022 (Beijing time), a titan arum in the north garden of the China National Botanical Garden in Beijing bloomed. In order to determine the components and contents of volatile compounds released by the titan arum during its flowering, the dynamic headspace adsorption method was utilized to collect the odor of the titan arum flower on the evening of 23 July (S1), the morning of 24 July (S2), the afternoon of 24 July (S3) and the evening of 24 July (S4). The volatile compounds were analyzed by automatic thermal desorption–gas chromatography/mass spectrometry. Sixty-three volatile compounds were detected in the titan arum flower in four periods. The comparison of the total volatile compounds released in four periods was S2 > S3 > S1 > S4. The highest content of volatile compounds in the S1 period were sulfur compounds (dimethyl disulfide and dimethyl trisulfide), and the sulfur compounds were released in large amounts only in the S1 period. Dimethyl disulfide was the volatile substance with the highest content in the S1 period (20.00%). The total volatile compounds content of titan arum flower in the S2 period was the highest among the four periods. From the S2 period, the relative content of sulfur compounds decreased significantly until the S4 period. Compared with the S1 period, 1-butanol and butyl acrylate increased significantly and 1-butanol became the highest relative component of volatile compounds in the S2 period. After the S3 period, the total amount of volatile compounds began to decline and reached the lowest level in the S4 period. It is worth noting that the contents of two terpenes, α-pinene and γ-terpinene, rose from the S1 period until their height in the S3 period. From the S4 period, the contents of most volatile compounds decreased significantly. This study revealed the varieties and contents of volatile compounds in the titan arum flower at different flowering periods. The changing trend and physiological significance of dimethyl oligosulfide from the evening of flowering (S1) to the second day (S2–S4) were emphatically discussed, and this research also provides a reference for the study of the release of volatile compounds and the molecular biology of the flower fragrance of titan arum.
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... ex Arcangeli (Araceae)). Titan arum is known to emit a unique rotting animal-like odour from its inflorescence that attracts insects for pollination; the odor consists of several sulphur-containing volatile organic compounds including dimethyl trisulfide (DMTS) 40 . DMTS is part of the odour of carrion and was also found to be attractive to two species of Central European Nicrophorus (Coleoptera: Staphylinidae: Silphinae) using electroantennography 41 . ...
Integrative taxonomy and species distribution models of the genus Diamesus Hope, 1840 (Coleoptera: Staphylinidae: Silphinae)
Article
Full-text available
  • Feb 2023
Integrative taxonomy of Diamesus Hope, 1840 (Coleoptera: Silphinae) is presented. Adults of D. bimaculatus Portevin, 1914 (endemic to Taiwan) and D. osculans (Vigors, 1825) (widely distributed from northern India to Australia) are redescribed, keyed and figured, including characters of the male and female genitalia of both species. Variation in elytral maculation in D. osculans is discussed and illustrated. The absence of diagnostic differences of D. osculans var. reductus Pic, 1917 from D. osculans is discussed, and the former name is confirmed as a junior subjective synonym of D. osculans. Types of all three names available were studied; a lectotype and paralectotypes are designated for the name D. osculans var. bimaculatus Portevin, 1914. Molecular phylogenetic analysis confirms the genus Diamesus is sister group to the genus Necrodes Leach, 1815, and D. osculans and D. bimaculatus are two, well supported clades. Detailed data on the distribution of D. bimaculatus and D. osculans are presented and mapped. Species distribution models for both species were created and interpreted. Diamesus osculans is reported for the first time from India: Uttarakhand, China: Anhui, Hainan, Hunan, Jiangxi, Shaanxi and Zhejiang Provinces, and Australia: Victoria; it is also recently confirmed from Taiwan, being sympatric in distribution there with D. bimaculatus. Available data on the ecology and seasonality of both species of Diamesus are also discussed.
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... The spadix is divided into a lower pistillate zone, followed by an upper staminate zone and finally on top, a sterile appendix that serves scent volatilization (Mayo et al., 1997;Kite & Hetterscheid, 2017). Scent volatilization is known to be promoted by heat generation in the appendix, at least in some species (Skubatz et al., 1990;Barthlott et al., 2009;Lamprecht & Seymour, 2010;Shirasu et al., 2010). ...
Phylogenomic study of Amorphophallus (Alismatales; Araceae): When plastid DNA gene sequences help to resolve the backbone subgeneric delineation
Article
  • Aug 2022
Encompassing ca. 200 species distributed in paleotropical Africa and Asia, Amorphophallus is one of the largest genera of Araceae. In spite of a great economic interest for its glucomannan production, only few studies have attempted to grasp the evolutionary history of this genus. In the current state of knowledge, four main clades, mostly linked to biogeographical delineation, have been identified from phylogenies based on few genes. However, relationships among and within these clades still remain unclear, due to the rapid radiation that occurred during the early evolutionary history of the genus. Here, we generated genome skimming libraries for 43 specimens from 36 species distributed across the four clades, which allowed us to produce a phylogenetic matrix for a set of 71 plastid genes. Our phylogenies confirm the monophyly of these clades but show a new and well‐resolved arrangement among these clades. Our analyses therefore provide a new scenario and timeline for the evolution of the main Amorphophallus clades, consistent with the morphological characteristics of the clades. The inferred scenario is also in agreement with climate dynamics and the onset of long‐distance dispersal by the earliest migratory birds near the Oligocene/Miocene transition around 23 million years ago. Our study provides an up‐to‐date baseline to understand biogeographic and ecological processes that shaped the current diversity and distribution of Amorphophallus, paving the way for larger‐scale phylogenomic studies based on plastid and nuclear genomes. This article is protected by copyright. All rights reserved.
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... Increased temperature in their flowers or cones enables them to effectively diffuse volatile odor components (VOCs) as attractants, which renders this ability to produce heat, also known as thermogenesis, an important reproductive strategy to attract pollinators (Meeuse and Raskin 1988). The principal composition of VOCs emitted from the inflorescences was revealed in several thermogenic species, such as aroids (Kite and Hetterscheid 2017;Marotz-Clausen et al. 2018;Oguri et al. 2019;Shirasu et al. 2010;Stensmyr et al. 2002) and cycads (Azuma and Kono 2006;Salzman et al. 2020;Terry et al. 2007). In dioecious cycads, such as Macrozamia lucida and Zamia furfuracea, male cones regulate the concentration of the dominant VOCs by oscillating their internal temperature. ...
Establishing an efficient protoplast transient expression system for investigation of floral thermogenesis in aroids
Article
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Key message Floral thermogenesis is an important reproductive strategy for attracting pollinators. We developed essential biological tools for studying floral thermogenesis using two species of thermogenic aroids,Symplocarpus renifolius and Alocasia odora. Abstract Aroids contain many species with intense heat-producing abilities in their inflorescences. Several genes have been proposed to be involved in thermogenesis of these species, but biological tools for gene functional analyses are lacking. In this study, we aimed to develop a protoplast-based transient expression (PTE) system for the study of thermogenic aroids. Initially, we focused on skunk cabbage (Symplocarpus renifolius) because of its ability to produce intense as well as durable heat. In this plant, leaf protoplasts were isolated from potted and shoot tip-cultured plants with high efficiency (ca. 1.0 × 10⁵/g fresh weight), and more than half of these protoplasts were successfully transfected. Using this PTE system, we determined the protein localization of three mitochondrial energy-dissipating proteins, SrAOX, SrUCPA, and SrNDA1, fused to green fluorescent protein (GFP). These three GFP-fused proteins were localized in MitoTracker-stained mitochondria in leaf protoplasts, although the green fluorescent particles in protoplasts expressing SrUCPA-GFP were significantly enlarged. Finally, to assess whether the PTE system established in the leaves of S. renifolius is applicable for floral tissues of thermogenic aroids, inflorescences of S. renifolius and another thermogenic aroid (Alocasia odora) were used. Although protoplasts were successfully isolated from several tissues of the inflorescences, PTE systems worked well only for the protoplasts isolated from the female parts (slightly thermogenic or nonthermogenic) of A. odora inflorescences. Our developed system has a potential to be widely used in inflorescences as well as leaves in thermogenic aroids and therefore may be a useful biological tool for investigating floral thermogenesis.
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... The scent compounds of nearly a hundred Amorphophallus species have been analysed Hetterscheid 1997, 2017;Kite et al. 1998;Kakishima et al. 2011;Lamprecht and Seymour 2010;Shirasu et al. 2010;Chen et al. 2015;Raman et al. 2017) and most species release scent types that include "carrion, faeces, urine, dung, fishy, sewerage, nauseating gaseous, rancid cheese, fermenting fruit and mushrooms" (Kite and Hetterscheid 2017). These odour types are effective cues for insects that search for such substrates for feeding, mating or breeding, indicating the deceptive nature of the majority of Amorphophallus species (Kite et al. 1998;Jürgens et al. 2006Jürgens et al. , 2013Vereecken and McNeil 2010;Urru et al. 2011;Johnson and Schiestl 2016;Kite and Hetterscheid 2017). ...
The many elusive pollinators in the genus Amorphophallus
Article
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The genus Amorphophallus encompasses some 230 species and is one of the largest genera of the Araceae family. Most species release scents, smelling of carrion, faeces, dung and similar nauseating odours for pollinator attraction and are therefore considered to have evolved a deceptive pollination syndrome. Some of the most iconic members of the genus, such as the A . titanum and A . gigas , are considered to be carrion mimics. Copro-necrophagous insects, beetles and flies in particular, are attracted by these scents and are therefore assumed to act as pollinators. However, many reports and observations on Amorphophallus pollinators are anecdotal in nature or do not distinguish between legitimate pollinators and non-pollinating visitors. Moreover, some published observations are not readily accessible as they are many decades old. Therefore, the available data and information about insect visitors and/or pollinators in the genus Amorphophallus is compiled, reviewed and discussed.
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... Carcasssmelling was produced by dimethyl disulfide and dimethyl trisulfide (Lamprecht et al. 2002), dimethyl oligo-sulfides (Kite andHetterscheid 1997, Punekar andKumaran 2010). Similarly, A. titanum also produced carcass-smelling emanated during female anthesis, due to contributed of some chemical compounds; dimethyl oligo-sulfides, dimethyl trisulfide (Kate and Hetterscheid 1997), trimethylamine (Fujioka et al. 2012), methyl thiol acetate, 3-methyl butanal, acetic acid, isovaleric acid, 3-Hydroxy-2butanone, 2-Ethyl hexanol, and benzyl alcohol (Shirasu et al. 2010;Raman et al. 2017). This carcass-smelling attracted olfactory pollinators and insect visitors for coming, such as blowflies (Calliphoridae), and also as a sign for female anthesis. ...
Inflorescence morphology and development of suweg (Amorphophallus paeoniifolius (Dennst.) Nicolson
Article
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  • Nov 2020
Hanfayani T, Yuzammi, Hadiah JT. 2020. Inflorescence morphology and development of suweg (Amorphophallus paeoniifolius (Dennst.) Nicolson. Biodiversitas 21: 5835-5844. Inflorescence of Amorphophallus paeoniifolius (Dennst.) Nicolson consists of two main parts: spathe and spadix. Detailed information on its development, however, is not yet available. This study aimed to investigate the development and morphology of suweg’s inflorescence, to reveal the anthesis of male and female flowers, and to observe its insect visitors. The study observed 46 inflorescences, ten of which were measured for detailed developments. Inflorescences were observed from bud emergence to withering during one flowering cycle. The results showed that the flowering process included six phases which altogether required 22 to 36 days, namely the developments of inflorescence bud, cataphyll, spathe and spadix, appendix, fully bloomed inflorescence, and flowers anthesis. The inflorescence height including peduncle was 48–75 cm, spathe 19–50 cm long, spathe circle 65–176 cm, appendix 13–33 cm long, and appendix circle 45–80 cm. Three appendix forms were observed: ovate (43.48%), triangular conic (41.30%), and rounded (15.22%). Female flower anthesis occurred one day prior to male flower anthesis. Insect visitors found during anthesis were Lucilia sericata (Calliphoridae), Sarcophaga sp. (Sarcophagidae), and Trigona speciosa (Apidae).
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Thermologic investigations of three species of Amorphophallus
Article
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Thermologic investigations were carried out on three species of Amorphophallus: A. konjac, A. paeoniifolius and A. titanum, all the three strongly thermogenic. Moreover, their breeding system is described as protogynous, the heat production occurs in the appendix and male florets, no warming is seen in the female florets and pollen is shed after the end of heat dissipation. All the three have large, impressive inflorescences developed from big corms and have considerable sizes. During their inflorescence, they have a strong scent like rotting meat with carrion smell. Amorphophallus konjac (K. Koch) has a large, exposed appendix that produces a disgusting scent during the day of the female phase of blooming. The appendix produces about 3 W for several hours, and the temperature elevation is about 2.9 K. The low temperature elevation is attributed to a high surface area and a high evaporative heat loss from the appendix. During the male phase of blooming, a second episode of thermogenesis occurs during the same time of day, apparently from the male florets, reaching a maximum of 1.6 W. Amorphophallus paeoniifolius (Dennst.) Nicolson has a spadix that varies considerably from that of A. konjac and A. titanum with an amorphous upper end of the appendix like a shrunken red pepper instead of cone-like appendices for the two others. It shows thermogenic temperature increases of up to +9.1 K in the male florets and +2.6 K for a short time in the appendix. Amorphophallus titanum (Becc.) Becc. ex Arcang is the largest inflorescence of the world, growing up to 300 cm high and 250 cm across. A much smaller plant was observed during its thermogenic period by means of infrared (IR) thermography, IR thermometry, and thermometric data logger. The temperature maximum showed 36.6 °C at ambient 24.0 °C, which means a temperature difference of about +12.6 K. In the morning of the next day, all temperatures are back to ambient at about 24 °C. Estimates of the heat production (about 74 W) were made from the geometric data and special assumptions with respect to the heat transfer.
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Combination of Real-Value Smell and Metaphor Expression Aids Yeast Detection
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Smell provides important information about the quality of food and drink. Most well-known for their expertise in wine tasting, sommeliers sniff out the aroma of wine and describe them using beautiful metaphors. In contrast, electronic noses, devices that mimic our olfactory recognition system, also detect smells using their sensors but describe them using electronic signals. These devices have been used to judge the freshness of food or detect the presence of pathogenic microorganisms. However, unlike information from gas chromatography, it is difficult to compare odour information collected by these devices because they are made for smelling specific smells and their data are relative intensities. Here, we demonstrate the use of an absolute-value description method using known smell metaphors, and early detection of yeast using the method. This technique may help distinguishing microbial-contamination of food products earlier, or improvement of the food-product qualities.
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On the thermogenesis of the Titan arum ( Amorphophallus titanum )
Article
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The Titan arum (Araceae) produces the largest bloom of all flowering plants. Its flowering period of two days is divided into a female flowering phase in the first night and a male flowering phase in the second night. Recently, we have documented thermogenesis in the spadix of the Titan arum during the female flowering phase. Here, we document a second thermogenic phase in which the male florets are heated during the male flowering phase. Obviously the two nocturnal thermogenic phases are linked with the two flowering periods. These observations now allow a more detailed understanding of the flowering behavior of the Titan arum.
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Inflorescence odours of Amorphophalus and Pseudodracontium (Araceae)
Article
The inflorescence odours of 18 species of Amorphophallus and two species of Pseudodracontium were analysed by headspace techniques and compared to the limited data on potential pollinators. The odours of species with ‘gaseous’ or carrion smells had a simple chemical composition, consisting mainly of dimethyl oligosulphides. The odours of other Amorphophallus species having different smells were also generally dominated by one or two compounds: e.g. trimethylamine in A. brachyphyllus, isocaproic acid in A. elatus, 4-methoxyphenethyl alcohol in A. albispathus, and isoamyl acetate with ethyl acetate in A. haematospadix. The production of odours containing dimethyl oligosulphides appears to be a common feature of sapromyophilous flowers that attract carrion insects. © 1997 Elsevier Science Ltd. All rights reserved
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Mechanisms of formation of Volatile sulphur compounds following the action of cysteine sulphoxide lyases
Article
  • Jul 1994
Mechanisms for the formation of methanethiol, dimethyl disulfide, and dimethyl trisulfide in disrupted cabbage tissues were investigated. Dimethyl disulfide was produced in both air- and nitrogen-saturated disrupted cabbage tissues without significant differences (p ≤ 0.05), which indicated that air oxidation of methanethiol is not the predominant mechanism for the formation of dimethyl disulfide. These results favored the mechanism in which the formation of dimethyl disulfide occurs from chemical disproportionation of methyl methanethiosulfinate. Methanethiol and dimethyl trisulfide were formed rapidly in model systems containing either methyl methanethiosulfinate or methyl methanethiosulfonate and hydrogen sulfide. This indicated that the reactions of the thiosulfinate and thiosulfonate compounds with hydrogen sulfide are prominent mechanisms for the formation of methanethiol and dimethyl trisulfide following the action of cysteine sulfoxide lyases. Methyl methanethiosulfinate and methyl methanethiosulfonates were found to possess characterizing sauerkraut aroma notes.
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Formation of methanethiol from methionine by leaf tissue
Article
  • Dec 1985
Leaf discs, but not detached leaves, exposed to L-methionine or S-methyl-L-cysteine emitted a volatile sulphur compound identified as methanethiol by different trapping systems and by GC. Methanethiol emission was analyzed using pumpkin (Cucurbita pepo) leaf discs. Emission was observed in darkness or light, however methanethiol emission was greately stimulated by light. Light-dependent emission started after a lag-time of 5–6 hr with an emission peak after 36–40 hr. Maximum rates obtained were in the range of 200 pmol methanethiol/min/cm2 leaf area. After a period of 42 hr about 60–80% of total methionine sulphur added was released as methanethiol. Addition of chloramphenicol did not alter the induction period nor the maximum emission rate of methanethiol in response to L-methionine. Emission was also observed in response to S-methyl-L-cysteine; however, the shorter lag-period for methanethiol formation suggests metabolism via a different enzyme system. In a cell-free system of pumpkin leaves methanethiol formation occured in response to L-methionine. Feeding experiments with L-[35S]methionine to leaf discs showed that more than 80% of methanethiol emitted was derived from the labelled methionine fed. These findings suggest that plants have the capacity to degrade L-methionine to methanethiol. Whole leaves fed L-methionine by the petiole system do not emit methanethiol, but this compound is formed and transported into the feeding solution. Thus, methanethiol is also produced by the intact leaf, but, in contrast to sulphide, is not released into the atmosphere. It is suggested that translocation of methanethiol may function as a signal for the regulation of sulphate uptake.
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Suprathreshold intensity and odour quality of sulphides and thioesters
Article
Odour intensity ratings over a range of concentrations were determined for 13 sulphur compounds, in this case, sulphides and thioesters. Odour intensities were assessed by an olfactory intra-modal intensity matching procedure in which a concentration series of isoamyl acetate was used as a reference intensity scale. The relationship between perceived intensity and concentration for each sulphur compound was approximated by power functions on an individual and panel level. Relationships between equally intense smelling concentrations of sulphur compounds and isoamyl acetate led to power function exponents that ranged from 0.83 (dimethyltrisulphide) to 1.42 (S-methyl thioisobutanoate). Derived exponents of the suprathreshold intensity functions, obtained through calibration with the parameters of the isoamyl acetate intensity function, ranged from 0.22 to 0.38. Exponents differed significantly between compounds as well as between subjects. Besides, the subjects described, with their own vocabulary, the odour quality of each compound. The odorants differed in the nature and the number of qualities used for their description.
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Dimethyl Trisulfide as a Characteristic Odor Associated with Fungating Breast Cancer Wounds.
Article
Some advanced cancer patients suffer from pungent sulfury malodor. To determine the chemical identity of the odorant, we performed gas chromatography-mass spectrometry-olfactometry analysis of volatiles from fungating cancer wounds. We identified the source of the characteristic smell as dimethyl trisulfide, a compound that is known to be emitted from some vegetables and microorganisms. Controlling the production of dimethyl trisulfide should improve quality of life of patients.
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A torch in the rain forest: thermogenesis of the Titan Arum (Amorphophallus titanum)
Article
  • Aug 2009
An outstanding flagship species in the plant kingdom is the Titan arum (Amorphophallus titanum), which produces a fountain-like bloom up to 3 m high. The unique appearance of three simultaneous inflorescences in May 2006 was a chance to analyse the flowering behaviour and thermogenesis of this giant. For the first time, the heating of the central column (spadix) could be documented using a high-performance thermographic camera. Time series analyses of the infrared image sequences revealed that the 3-m high spadix surface heats up in pulses emanating from the base of the inflorescence. The surface temperature reaches over 36 degrees C, compared to the ambient temperature of 27 degrees C. Waves of the carrion-like odour are synchronised with these heat pulses. The combination of heat pulses, the fountain-like shape plus the enormous size lead to a unique type of 'convection flower'. On the basis of our observations, we assume that Amorphophallus titanum is able to overcome thermodynamic decoupling by a self-produced convective process.
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Screening and Identification of Precursor Compounds of Dimethyl Trisulfide (DMTS) in Japanese Sake
Article
Dimethyl trisulfide (DMTS) is involved in the unpalatable aroma of stale sake, called "hineka"; however, the mechanism underlying the formation of DMTS during the storage of sake has not been elucidated. This paper investigates the precursors of DMTS in sake. An experiment using [methyl-d(3)]-methionine showed that Strecker degradation of methionine plays a minor role in the formation of DMTS. Separation of components in sake by cation exchange resin revealed that DMTS precursors are present in the acidic/neutral fraction rather than in the basic one. Purification of the DMTS precursor compounds was carried out through several chromatographic steps, measuring DMTS-producing potential as an index. High-resolution ESI-MS and 1D/2D NMR experiments enabled the identification of one of the precursor compounds as 1,2-dihydroxy-5-(methylsulfinyl)pentan-3-one.
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