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1. Introduction
Floral thermogenesis occurs in several plant taxa in-
cluding gymnosperms (Cycadaceae), as well as eudicots
(Nymphaeaceae) and monocots (Araceae). Thermogen-
esis begins when these plants bloom, and heat production
terminates when pollen is released from the anthers. One
thermoregulatory plant, the Eastern Asian skunk cabbage
(Symplocarpus renifolius), can keep the spadix tempera-
ture between 22-26°C for several days even when the am-
bient temperature falls below freezing (Fig. 1A) (Knutson,
1974; Uemura et al., 1993; Seymour, 2004). Other ther-
moregulatory plants studied to date include Phillodendron
sellom (Nagy et al., 1972; Seymour et al., 1983) and Ne-
lumbo nucifera (Seymour and Schultze-Motel, 1998; Sey-
mour et al., 1998). Many species, which are thermogenic
but not thermoregulatory, are generally able to produce
heat for only 24 h at best. The robust thermoregulation ob-
served in S. renifolius and other species makes these plants
great models for unraveling the mechanism underlying
floral thermogenesis. In several species of Araceae, floral
thermogenesis has been proposed to serve the physiologi-
cal role of spreading odor to attract pollinators (Meeuse
and Raskin, 1988), whereas thermoregulation in S. renifo-
lius is not closely associated with cross-pollination (Sey-
mour and Blaylock, 1999). S. renifolius produces only a
faint aroma in early spring when few insects are active.
Thus, heating may promote early flowering or protect the
S. renifolius inflorescence from damage by freezing.
In S. renifolius, thermogenesis is closely associated with
three stages of inflorescence development: female, bisexual,
and male (Fig. 1B). At the female stage, which lasts until
the stamens emerge from the surface of the spadix, the spa-
dix can produce massive amounts of heat. At the bisexual
stage, the stamens begin to release pollen and thermogen-
esis fluctuates. Finally, at the male stage, pollen is released
from nearly all stamens and thermogenesis is undetectable.
Microscopic analysis revealed that structural changes in the
stamen are significant, and extensive anther development
occurs during inflorescence development (Ito-Inaba et al.,
2009 a). In addition to the structural changes in stamens, the
ultrastructure of petals and pistils also significantly change.
These tissues accumulate a larger number of mitochondria
during the female stage than during the male stage. Also,
large cytoplasmic vacuoles develop during the male stage.
In our recent gene expression analysis, expression of genes
involved in cellular respiration and mitochondrial function
was significantly enhanced during the thermogenic female
stage, whereas genes involved in stress responses and pro-
tein degradation were significantly up-regulated during
the non-thermogenic male stage (Ito-Inaba et al., 2012 a).
Therefore, changes in the intracellular structure observed in
Thermogenesis in skunk cabbage (Symplocarpus
renifolius): New insights from the ultrastructure and
gene expression profiles
Y. Ito-Inaba
Organization for Promotion of Tenure Track, University of Miyazaki, 1-1 Gakuenkibanadai-nishi, Mi-
yazaki 889-2192, Japan.
Key words: floral thermogenesis, inflorescence, low temperature, mitochondria, respiration, transcriptome.
Abstract: Floral thermogenesis has been found in several plant species. The spadix of one thermoregulatory plant, the
Eastern Asian skunk cabbage (Symplocarpus renifolius), can maintain its temperature at approximately 22-26°C for
several days, even when the ambient temperature falls below freezing. There are two major stages in skunk cabbage in-
orescence development: the thermogenic female stage and the non-thermogenic male stage; in the former the spadix can
produce massive amounts of heat, whereas in the latter, thermogenesis is undetectable. Based on previous studies, there
is a positive correlation between heat production and the abundance of mitochondria in plant tissues and cells, and genes
involved in cellular respiration and mitochondrial function are signicantly enhanced at the female stage. Taken together,
these ndings suggest that the increased respiration or mitochondrial abundance observed in thermogenic tissues may
be attributable to the high expression of specic genes. This review summarizes new insights into the changes in intracel-
lular structures and gene expression proles of skunk cabbage spadices during the female-male transition and proposes
possible processes that are essential for each stage during oral development.
Adv. Hort. Sci., 2014 28(2): 73-78
Received for publication 31 March 2014
Accepted for publication 18 June 2014
74
petals or pistils during the female-male transition are well
supported by changes in the transcriptome during inflores-
cence development.
Two processes may be important for thermoregulation
in skunk cabbage (Ito-Inaba et al., 2012 a). First, short-
term mechanisms that depend on increased cellular respi-
ration with the help of energy dissipating proteins, such as
alternative oxidase (AOX) or uncoupling protein (UCP),
may play an essential role in which AOX may have a more
major function than UCP. Secondly, long-term effects of
mitochondrial biogenesis on the number and structure
of mitochondria probably are also involved. Following
much effort to characterize the activity or expression of
AOX during floral development, the pivotal role of this
enzyme in floral thermogenesis was revealed (Watling et
al., 2006; Grant et al., 2008; Wagner et al., 2008; Ito-Inaba
et al., 2009 b; Miller et al., 2011). However, the presence
of additional genes that are co-expressed with AOX and
that may function directly or indirectly in thermogenesis
remains to be clarified. In addition, although it has been
hypothesized that heat-producing floral tissues contain
many mitochondria, quantitative and comparative stud-
ies on mitochondrial content are lacking. In this review,
we summarize our recent progress in describing changes
in the ultrastructure and gene expression profiles during
skunk cabbage floral development.
2. Thermogenesis and mitochondrial abundance
In mammalian cells, the positive correlation between
metabolic activity and the number and size of mitochon-
dria within a tissue is well established (Ghadially, 1988).
Mammalian brown adipose tissue (BAT), which is the main
site for non-shivering thermogenesis, contains consider-
able numbers of large mitochondria with abundant cristae.
In contrast, these relationships are not well characterized in
plants, and there are very few published papers that have
examined the intracellular structure of thermogenic tissues
by electron microscopy. In a well-known thermogenic plant,
Sauromatum guttatum (voodoo lily), ultrastructural changes
in the inflorescence during the transition from the pre- to
post-thermogenic stages were extensively studied, and clear
details of mitochondrial morphology were obtained (Sku-
batz et al., 1993). In addition, during the thermogenic stage
of S. guttatum floral development, mitochondria accumu-
lated osmophilic material between the inner and outer mem-
branes (Skubatz and Kunkel, 2000). In another thermogenic
plant, Philodendron selloum, large lipid bodies present in
sterile florets before heating were progressively depleted
during heat generation, and the mitochondria often con-
tained enlarged cristae during maximum heating (Walker et
al., 1983). However, there are no conclusive data indicating
a relationship between heating in plant tissues and mito-
chondrial features, such as content or morphology.
We first analyzed the detailed changes in mitochondrial
content and morphology during floral development of ther-
mogenic skunk cabbage, S. renifolius (Ito-Inaba et al., 2009
a). As shown in figure 2A, petal cells at the female stage
contained a large number of mitochondria. By contrast,
petal cells at the male stage contained only a small number
of mitochondria but had large central vacuoles. In the pistil
cells, likewise, a large number of mitochondria were pres-
ent at the female stage but few mitochondria persisted to the
male stage. Furthermore, stamens at the female stage, espe-
cially in the microspore and plasmodium, had high densities
of mitochondria. The sizes and morphologies of mitochon-
dria observed in all tissues varied. To evaluate the mitochon-
drial content quantitatively between the female and male
stages in each floral tissue, the average mitochondrial den-
sity (mitochondrial numbers µm-2 cytosol) in thin sections
of cells were analyzed in five to 10 cells. These data also
revealed that both petals and pistils at the female stage con-
tained larger numbers of mitochondria compared with the
male stage. Details of the ultrastructure and the quantitative
Fig. 1 - Thermoregulation in skunk cabbage (S. renifolius). (A) Skunk
cabbages were photographed using a camera in the visible (left
panel) and infrared spectra (right panel). The thermal image
was taken with Thermotracer SC620 (FLIR). Heat production
was observed in the spadix during the female stage of floral
development. (B) The sequential changes in spadix (red) and air
(blue) temperatures during floral development from the female
to the male stage. Spadices at the female stage can maintain in-
ternal temperature at approximately 22-26°C, whereas spadices
at the male stage cannot produce heat. Spadices at the bisexual
stage between the female and male stages show unstable ther-
mogenesis. Photographs of a female- and a male-stage spadix,
are shown in the upper right and lower right panels, respec-
tively. (B) was partially extracted from figure 1 in our previous
paper (Ito-Inaba et al., 2009 a).
75
data on mitochondrial content are described in our previous
paper (Ito-Inaba et al., 2009 a). We next compared the mito-
chondrial protein content recovered from thermogenic and
non-thermogenic stages or tissues (Ito-Inaba et al.. 2009 a,
b). As shown in figure 2B, the mitochondrial protein content
of female-stage spadices (0.54 mg g-1) was two-fold higher
than that of males (0.29 mg g-1), a value consistent with our
electron microscopic data. In addition, mitochondrial pro-
tein content of non-thermogenic skunk cabbage, Lysichiton
camtschatcensis (0.011 mg g-1), was much lower than that
of S. renifolius. Since L. camtschatcensis has no ability to
produce heat but has a close relationship with S. renifolius
in morphology and phylogeny, this result suggests that a
lower mitochondrial content may correlate with the lack of
thermogenesis in L. camtschatcensis. Taken together, these
results reveal that there is a positive correlation between
heat production and the abundance of mitochondria in plant
tissues and cells. These are the first quantitative data indi-
cating differences in mitochondrial content between ther-
mogenic and non-thermogenic stages or tissues. Therefore,
plants might produce the massive heat from their tissues by
increasing their mitochondrial density in a manner similar
to mammalian BAT.
3. The quantitative gene expression profile in female-
and male-stage spadices of S. renifolius
To understand the molecular basis of floral thermogen-
esis, we examined the gene expression profiles of female-
and male-stage spadices of S. renifolius. Since the com-
plete genome sequence of S. renifolius is not available,
we took advantage of the super serial analysis of gene ex-
pression (SuperSAGE) methodology as this method can
provide quantitative and comprehensive gene expression
profiles (Ito-Inaba et al., 2012 a). In our study, 26 bp tags
(SuperSAGE tags) expressed from female- and male-stage
spadices were prepared and sequenced using a 454 Life
Sciences Genome Sequencer 20 System. Since the length
of 26 bp tags is sufficient to identify the origin of a tag
using cDNA databases (Matsumura et al., 2003, 2011),
each 26 bp tag was annotated based on our cDNA database
of the female-stage spadices using the BioEdit program.
The gene expression profiles obtained were subjected to
cluster analysis to identify candidate sets of co-regulated
genes directly or indirectly associated with the process of
female- and male-stage spadices, and were qualified as a
group of female- or male-stage specific genes. To further
assess the function of each gene, AGI codes of Arabidop-
sis orthologs corresponding to the identified genes were
obtained from the database of The Arabidopsis Informa-
tion Resource (http://www.arabidopsis.org/index.jsp), and
the identified genes were classified based on Gene Ontolo-
gy (GO) terms using the AGI codes. This analysis allowed
us to predict the localization and function of the orthologs
in S. renifolius. Each gene was weighted according to the
number of corresponding SuperSAGE tags that reflected
the expression level of each gene.
Based on these methods, transcripts were assigned to
specific cellular components or biological processes (Ito-
Inaba et al., 2012 a) and the major transcriptional chang-
es are shown in figure 3. It was of particular interest that
genes encoding mitochondrial proteins were actively tran-
scribed in female spadices but not in male spadices (Fig.
3A). In addition, the activity of genes related to electron
transport or energy pathways decreased significantly dur-
ing the transition from the female to the male stage (Fig.
3B). These results suggest that mitochondrial function
Fig. 2 - Abundant mitochondria are present in the spadix of thermogenic
skunk cabbage. (A) Female spadix cells (petal tissues) contain
many mitochondria. This photograph was adapted from Fig. 5A
in our previous paper (Ito-Inaba et al., 2009a). In this study, large
numbers of mitochondria were also observed in pistils and in
several tissues in stamens. (B) Quantitative comparison of mi-
tochondrial protein amount from thermogenic and non-thermo-
genic stages or tissues. Female-stage spadices (♀) in S. renifolius
(Sr) contain 2-fold and 50-fold higher content of mitochondria
than male spadices (♂) and or spadices from L. camtschatcensis
(Lc), respectively. Data was extracted from Table 2 and Table 1
in our previous papers (Ito-Inaba et al., 2009 a, b, respectively).
Fig. 3 - Examples of transcriptional changes of cellular components and
biological processes of female- and male-stage spadices of S.
renifolius. Genes encoding proteins localized in mitochondria
(A) or that play roles in electron transport or the energy pathway
(B) are highly expressed at the female stage, but not at the male
stage of floral development. Genes encoding stress-responsive
proteins (C) were highly expressed at the male stage, but not at
the female stage. (A) was partially extracted from figure 3a (the
cellular component data) in our previous paper (Ito-Inaba et al.,
2012 a). (B) and (C) were also partially extracted from figure
3b (the biological process data) in the same paper.
76
and/or cellular respiration play a key role in floral thermo-
genesis. This finding is consistent with our electron mi-
croscopic observation that the thermogenic female-stage
spadix accumulates a large number of mitochondria and
has an increased oxygen consumption rate. Furthermore,
genes classified as stress responsive were highly expressed
in male spadices (Fig. 3C). Of these genes, a gene encod-
ing a cysteine protease in S. renifolius, designated as Sr-
CPA, was the most abundant transcript in the spadices, and
levels increased significantly during the female-male tran-
sition (Ito-Inaba et al., 2012 b). This class of cysteine pro-
tease is involved in programmed cell death (Beyene et al.,
2006) and stress responses (Stevens et al., 1996) in other
organisms. Since our previous studies suggested that a par-
allel relationship exists between the increase in CP tran-
scripts and vacuolar development in each of the various
spadix tissues during the female-male transition, the high
level of SrCPA expression may be correlated with vacuolar
development in male-stage spadices. In addition, several
stress-responsive genes and genes encoding degradative
enzymes or ubiquitin-proteasome system components had
increased expression levels at the post-thermogenic stage.
Therefore, we hypothesize that cysteine protease and other
degradative enzymes that leak from the vacuole may de-
grade mitochondria, thereby terminating thermogenesis at
the male stage.
4. Conclusions and Perspectives
Our previous electron microscopic study revealed
that intracellular structures within the individual tissues
change significantly during the transition from the female-
to the male-stage spadix in S. renifolius. The mitochon-
drial content is reduced, especially in the petals and pistils,
whereas the vacuolar volume increases during the female-
male transition. Consistent with this cellular change, gene
expression profiles analyzed using SuperSAGE methods
indicated that the genes involved in cellular respiration and
mitochondrial function are up-regulated in female-stage
spadices, whereas the genes involved in stress responses
and protein degradation are up-regulated in male-stage
spadices. These observations suggest that the maintenance
and termination of floral thermogenesis in the female- and
the male-stage spadices, respectively, may be explained as
shown in figure 4. At the female stage, the high expression
levels of genes related to cellular respiration and mito-
chondrial function induce significant oxygen consumption
and mitochondrial biogenesis, and activate cellular metab-
olism leading to substantial heat production. In contrast, at
the male stage, the high expression levels of genes related
to protein degradation and vacuolar metabolism induce se-
nescence, programmed cell death, and vacuolar develop-
ment, leading to the termination of heat production. After
thermogenesis, the expression of several stress response
genes, such as cold-inducible genes, increase because the
spadix cannot produce any heat. With exposure to the cold
air, the spadix cells proceed to senescence.
More than 200 years ago, pioneering studies on floral
thermogenesis were undertaken in the European Arum
(Araceae) by Lamarck (1778). Since then, heat production
by the reproductive organs of several plants has been inves-
tigated. We anticipate that the numbers of plants known to
produce heat will increase in the future as the subtle tem-
perature differences between the air and plant bodies can
be measured by technical advances in temperature probes
or thermography. To study the molecular mechanisms un-
derlying floral thermogenesis, two energy dissipating sys-
tems, an alternative oxidase (AOX) and uncoupling protein
(UCP), have been the principal subjects of investigation
(Vanlerberghe and McIntosh, 1997; Vercesi et al., 2006;
Zhu et al., 2011). Because of the correlation between heat
production and AOX concentration, as well as activity in
several thermogenic plants (Grant et al., 2008; Ito-Inaba et
al., 2009 b; Miller et al., 2011), AOX rather than UCP has
been assumed to control plant thermogenesis. Recently,
the crystal structure of a trypanosomal AOX was reported
(Shiba et al., 2013). Since the post-translational regulation
of AOX has been hypothesized to regulate the thermogenic
capacity of this protein (Grant et al., 2009), revealing the
structural features of AOX may open the door to elucidat-
ing the mechanisms underlying the post-translational reg-
ulation of AOX. Furthermore, we anticipate that recent ad-
vances in next generation sequence (NGS) technology will
uncover additional genes, besides AOX and UCP, that are
involved in floral thermogenesis. In S. renifolius, the gene
expression profile has already been studied using NGS
technology combined with the SuperSAGE method and
could provide valuable information to define the identity
of female- and male-stage spadices at the molecular level
(Ito-Inaba et al., 2012 a). As far as we know, this was the
first study in which the molecular mechanism underlying
floral thermogenesis was analyzed using NGS technology.
Quite recently, the genome of the sacred lotus (Nelumbo
nucifera), a well-known thermogenic plant, was sequenced
(Ming et al., 2013). We also expect that this advance will
accelerate study of the molecular mechanism underlying
heat production in the reproductive organ development of
Fig. 4 - A proposed model of the possible processes in female- and
male-stage spadices to maintain and terminate thermogenesis,
respectively.
77
sacred lotus. S. renifolius is a monocot thermogenic plant,
whereas N. nucifera is a eudicot thermogenic plant. Thus,
comparative studies of these plants will reveal general and
diverse aspects of floral thermogenesis.
Acknowledgements
This work was supported by The Naito Founda-
tion, Grants-in-Aid for Research Activity Start-up (no.
24880027), the Program to Disseminate Tenure Tracking
System from the Japanese Ministry of Education, Culture,
Sports, Science and Technology, and by a grant for Sci-
entific Research on Priority Areas from the University of
Miyazaki.
References
BEYENE G., FOYER C.H., KUNERT K.J., 2006 - Two new
cysteine proteinases with specific expression patterns in ma-
ture and senescent tobacco (Nicotiana tabacum L.) leaves.
- J. Exp. Bot., 57: 1431-1443.
GHADIALLY F.N., 1988 - Ultrastructural pathology of the cell
and matrix. - Butterworth-Heinemann, London, UK, 3rd
Edition, pp. 194.
GRANT N.M., MILLER R.E., WATLING J.R., ROBINSON
S.A., 2008 - Synchronicity of thermogenic activity, alterna-
tive pathway respiratory flux, AOX protein content, and car-
bohydrates in receptacle tissues of sacred lotus during floral
development. - J. Exp. Bot., 59: 705-714.
GRANT N.M., ONDA Y., KAKIZAKI Y., ITO K., WATLING
J.R., ROBINSON S.A., 2009 - Two cys or not two cys? That
is the question; alternative oxidase in the thermogenic plant
sacred Lotus. - Plant Physiol., 150: 987-995.
ITO-INABA Y., HIDA Y., INABA T., 2009 b - What is critical
for plant thermogenesis? Differences in mitochondrial ac-
tivity and protein expression between thermogenic and non-
thermogenic skunk cabbages. - Planta, 231: 121-130.
ITO-INABA Y., HIDA Y., MATSUMURA H., MASUKO H.,
YAZU F., TERAUCHI R., WATANABE M., INABA T.,
2012 a - The gene expression landscape of thermogenic
skunk cabbage suggests critical roles for mitochondrial and
vacuolar metabolic pathways in the regulation of thermo-
genesis. - Plant, cell & environment, 35: 554-566.
ITO-INABA Y., MASUKO H., WATANABE M., INABA T.,
2012 b - Isolation and gene expression analysis of a papain-
type cysteine protease in thermogenic skunk cabbage (Symp-
locarpus renifolius). - Bioscience, Biotechnology, and Bio-
chemistry, 76: 1990-1992.
ITO-INABA Y., SATO M., MASUKO H., HIDA Y., TOYOOKA
K., WATANABE M., INABA T., 2009 a - Developmental
changes and organelle biogenesis in the reproductive organs
of thermogenic skunk cabbage (Symplocarpus renifolius). -
J. Exp. Bot., 60: 3909-3922.
KNUTSON R.M., 1974 - Heat production and temperature reg-
ulation in eastern skunk cabbage. - Science, 186: 746-747.
LAMARCK J., 1778 - Flore Français. - L’Imprimerie Royale,
Paris, France, pp. 537-539.
MATSUMURA H., REICH S., ITO A., SAITOH H., KA-
MOUN S., WINTER P., GÜNTER KAHL G., REUTER M.,
KRÜGER D.H., TERAUCHI R., 2003 - Gene expression
analysis of plant host-pathogen interactions by SuperSAGE.
- Proc. Natl. Acad. Sci. U.S.A., 100: 15718-15723.
MATSUMURA H., YOSHIDA K., LUO S., KRUGER D.H.,
KAHL G., SCHROTH G.P., TERAUCHIET R., 2011 - High-
throughput SuperSAGE. - Methods Mol. Biol. 687: 135-146.
MEEUSE B.J.D., RASKIN I., 1988 - Sexual reproduction in the
arum lily family, with emphasis on thermogenicity. - Sexual
Plant Reproduction, 1: 3-15.
MILLER R.E., GRANT N.M., GILES L., RIBAS-CARBO M.,
BERRY J.A., WATLING J.R., ROBINSON S.A., 2011 - In
the heat of the night - alternative pathway respiration drives
thermogenesis in Philodendron bipinnatifidum. - The New
phytologist, 189: 1013-1026.
MING R., VANBUREN R., LIU Y., YANG M., HAN Y., LI
L.T., BOWERS J.E., TANG H., LYONS E., FERGUSON
A.A., NARZISI G., NELSON D.R., BLABY-HAAS C.E.,
GSCHWEND A.R., JIAO Y., DER J.P., ZENG F., HAN J.,
MIN X.J., HUDSON K.A., SINGH R., GRENNAN A.K.,
KARPOWICZ S.J., WATLING J.R., ITO K., ROBINSON
S.A., HUDSON M.E., YU Q., MOCKLER T.C., CAR-
ROLL A., ZHENG Y., SUNKAR R., JIA R., CHEN N.,
ARRO J., WAI C.M., WAFULA E., SPENCE A., HAN Y.,
XU L., ZHANG J., PEERY R., HAUS M.J., XIONG W.,
WALSH J.A., WU J., WANG M.L., ZHU Y.J., PAULL R.E.,
BRITT A.B., DU C., DOWNIE S.R., SCHULER M.A.,
MICHAEL T.P., LONG S.P., ORT D.R., SCHOPF J.W.,
GANG D.R., JIANG N., YANDELL M., DEPAMPHILIS
C.W., MERCHANT S.S., PATERSON A.H., BUCHANAN
B.B., LI S., SHEN-MILLER J., 2013 - Genome of the long-
living sacred lotus (Nelumbo nucifera Gaertn.). - Genome
Biol., 14: R41.
NAGY K.A., ODELL D.K., SEYMOUR R.S., 1972 - Tempera-
ture regulation by the inflorescence of Philodendron. - Sci-
ence, 178: 1195-1197.
SEYMOUR R.S., 2004 - Dynamics and precision of thermoreg-
ulatory responses of eastern skunk cabbage Symplocarpus
foetidus. - Plant Cell and Environ., 27: 1014-1022.
SEYMOUR R.S., BARTHOLOMEW G.A., CHRISTOPHER
BARNHART M., 1983 - Respiration and heat production
by the inflorescence of Philodendron selloum Koch. - Planta,
157: 336-343.
SEYMOUR R.S., BLAYLOCK A.J., 1999 - Switching off the
heater: influence of ambient temperature on thermoregula-
tion by eastern skunk cabbage Symplocarpus foetidus. - J.
Exp. Bot., 50: 1525-1532.
SEYMOUR R.S., SCHULTZE-MOTEL P., 1998 - Physiologi-
cal temperature regulation by flowers of the sacred lotus.
- Philosophical Transactions of the Royal Society, B 353:
935-943.
SEYMOUR R.S., SCHULTZE-MOTEL P., LAMPRECHT I.,
1998 - Heat production by sacred lotus flowers depends on
ambient temperature, not light cycle. - J. Exp. Bot., 49: 1213-
1217.
SHIBA T., KIDO Y., SAKAMOTO K., INAOKA D.K., TSUGE
C., TATSUMI R., BALOGUN E.O., NARA T., AOKI T.,
HONMA T., TANAKA A., INOUE M., MATSUOKA S.,
SAIMOTO H., MOORE A.L., HARADA S., KITA K., 2013
78
- Structure of the trypanosome cyanide-insensitive alterna-
tive oxidase. - Proc. Natl. Acad. Sci. U.S. A., 110: 4580-
4585.
SKUBATZ H., KUNKEL D.D., 2000 - Developmental changes
in the ultrastructure of the Sauromatum guttatum (Araceae)
mitochondria. - J. Electron Microsc., 49: 775-782.
SKUBATZ H., KUNKEL D.D., MEEUSE B.J.D., 1993 - Ultra-
structural changes in the appendix of the Sauromatum gutta-
tum inflorescence during anthesis. - Sexual Plant Reproduc-
tion, 6: 153-170.
STEVENS C., TITARENKO E., HARGREAVES J.A., GURR
S.J., 1996 - Defence-related gene activation during an in-
compatible interaction between Stagonospora (Septoria)
nodorum and barley (Hordeum vulgare L.) coleoptile cells.
- Plant Mol. Biol., 31: 741-749.
UEMURA S., OHKAWARA K., KUDO G., WADA N., HI-
GASHI S., 1993 - Heat-production and cross-pollination of
the asian skunk cabbage Symplocarpus renifolius. - Ameri-
can Journal of Botany, 80: 635-640.
VANLERBERGHE G.C., MCINTOSH L., 1997 - Alternative
oxidase: From gene to function. - Annu. Rev. Plant. Physiol.
Plant. Mol. Biol., 48: 703-734.
VERCESI A.E., BORECKY J., MAIA IDE G., ARRUDA P.,
CUCCOVIA I.M., CHAIMOVICH H., 2006 - Plant uncou-
pling mitochondrial proteins. - Annu. Rev. Plant Biol., 57:
383-404.
WAGNER A.M., KRAB K., WAGNER M.J., MOORE A.L.,
2008 - Regulation of thermogenesis in flowering Araceae:
the role of the alternative oxidase. - Biochim. Biophys. Acta,
1777: 993-1000.
WALKER D.B., GYSI J., STERNBERG L., DENIRO M.J.,
1983 - Direct respiration of lipids during heat production in
the inflorescence of Philodendron selloum. - Science, 220:
419-421.
WATLING J.R., ROBINSON S.A., SEYMOUR R.S., 2006 -
Contribution of the alternative pathway to respiration dur-
ing thermogenesis in flowers of the sacred lotus. - Plant
Physiol., 140: 1367-1373.
ZHU Y., LU J., WANG J., CHEN F., LENG F., LI H., 2011 -
Regulation of thermogenesis in plants: the interaction of
alternative oxidase and plant uncoupling mitochondrial pro-
tein. - Journal of Integrative Plant Biology, 53: 7-13.
