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MINI REVIEW
The flowers or inflorescences of certain primitive seed plants are able to regulate their
temperature during blooming by modulating the rate of heat production to remain much
warmer than the surroundings. A large drop in ambient temperature causes a smaller drop
in flower temperature which causes an increase in the rate of heat production by futile
involvement of the cytochrome and alternative oxidase respiratory pathways. The result is
that the rate of heat production is inversely related to ambient temperature and flower
temperature remains high and relatively independent of ambient temperature. While the
biophysics of thermal balance in the whole flowers is better understood, the regulation of
the biochemical heat-generating pathways is not known.
INTRODUCTION
For over 200 years, botanists have known that the flowers of some plants become
warm during the sequence of blooming. Some species, such as Philodendron selloum
(Nagy et al., 1972) and Symplocarpus foetidus (Knutson, 1974), are so intensely
thermogenic that their flowers can heat up to 35°C above their surroundings. Sig-
nificant self-heating occurs in the flowers, inflorescences or cones of some species in
several families of primitive seed-plants, namely the aroids, or arum lilies (Araceae)
(Meeuse and Raskin, 1988), lotus (Nelumbonaceae) (Miyake, 1898; Schneider and
Buchanan 1980) water lilies (Nymphaeaceae) (Prance and Arias, 1975), Dutchman’s
pipes (Aristolochiaceae) (Raskin et al., 1987), palms (Arecaceae and Cyclanthaceae)
(Schroeder, 1978; Gottsberger, 1990; Listabarth, 1996) custard apples (Annonaceae)
(Gottsberger, 1990), magnolias (Magnoliales) (Thien et al., 1999; Schultze-Motel,
unpubl.) and cycads (Cycadaceae) (Skubatz et al., 1993). Explanations for heat pro-
duction include enhancement of scent production (Meeuse and Raskin, 1988), pro-
tection from freezing (Knutson, 1979), and a thermal reward to insect pollen vectors
(Seymour and Schultze-Motel, 1997).
Many thermogenic flowers produce heat at variable and apparently uncon-
trolled rates, and their temperatures vary widely during the flowering sequence. A
1
Department of Environmental Biology, University of Adelaide, Adelaide, SA 5005, Australia; E-mail:
roger.seymour@adelaide.edu.au
223
0144-8463兾01兾0400-0223$19.50兾0 2001 Plenum Publishing Corporation
224 Seymour
few species, however, adjust the rate of heating in relation to ambient temperature
such that the flower temperature remains somewhat independent of ambient tem-
perature. This phenomenon is known as physiological temperature regulation.
Temperature regulation was first discovered in the arum lily P. selloum (Nagy et al.,
1972) and subsequently in eastern skunk cabbage S. foetidus (Knutson, 1974), the
sacred lotus Nelumbo nucifera (Seymour and Schultze-Motel, 1996) and the dragon
lily Dracunculus ûulgaris (Seymour and Schultze-Motel, 1999). It may also occur in
the arum lilies Sauromatum guttatum and Xanthosoma robustum (Meeuse and Ras-
kin, 1988). Similar patterns of flower temperature and rate of heat production in
response to ambient temperature occurs in all of these species; as ambient tempera-
ture decreases, the difference between flower and ambient temperature increases and
the rate of oxygen consumption increases (Fig. 1).
Temperature regulation is usually attributed to endothermic animals, such as
mammals and birds, although it does occur in many flying insects. In the animals,
regulation is mediated by a complex interaction between thermal receptors in the
body, integrative and regulative centers in the brain, and effector organs that alter
the animal’s insulation, augment heat production or invoke evaporative heat loss. It
is fascinating that temperature regulation can be as effective in some flowers that
lack these mechanisms. Regulation in flowers occurs mainly by modulating the rate
of heat production, and the control apparently occurs at the cellular level. This
review explores the phenomenon in thermoregulating flowers, presents a biophysical
model for heat balance, compares the precision of regulation, and proposes potential
biochemical temperature control mechanisms.
Fig. 1. Effect of ambient temperature on mean rates of oxygen consumption and flower tempera-
ture in the sacred lotus Nelumbo nucifera during the 2–4 day thermoregulatory period in an out-
door pond (Seymour and Schultze-Motel, 1998). Note that the rate of oxygen consumption,
indicative of the rate of heat production, increases linearly as ambient temperature decreases.
Meanwhile flower temperature remains between about 30 and 36°C. Evaporative cooling is suf-
ficient to depress flower temperature several degrees below at high ambient temperatures in the
sun. The dashed line is isothermal.
returned to 39°C. Significantly, the responses to temperature change are not immedi-
ate; recovery time is 20 min after exposure to 44°C, and longer at higher tempera-
tures. The measurements from P. selloum suffer from the facts that cut spadices or
florets are triggered into a single, intense episode of thermogenesis that lasts only 1–
2 hr and the rate of heat production never stabilizes. Therefore it is not possible to
examine the effects of floret temperature on heat production throughout a broad
range of temperature or over longer periods of time.
226 Seymour
resume higher levels of heat production, switching to the regulated state above 16°C.
The result is that the inflorescence switches between the warm and cool states if the
ambient temperature varies above and below approximately 3°C. The rate of heat
production is maximal at a spadix temperature of 16°C, and it decreases quickly at
lower temperatures; therefore this temperature is known as the ‘‘switching tempera-
ture.’’ The distribution of data for the relationship between respiratory rate and
spadix temperature of S. foetidus (Fig. 3) shows the switching temperature and
reveals that the inflorescence tends to be either warmer than 16°C or colder than
6°C, with few intermediate points. This bimodal distribution is also seen in randomly
sampled spot measurements of spadix temperature in the field. In one survey when
ambient temperatures were close to freezing, one group of plants averaged 3.8°C
while the other group averaged 17.0°C (Seymour and Blaylock, 1999).
switching temperatures of the spadices remained near 16°C, but higher rates of heat
production in the larger spadices permitted them to remain above this temperature
at lower ambient temperatures. Most large spadices (>100 g) of P. selloum can warm
to about 40°C at air temperatures near freezing, but smaller spadices fail to warm
at 4°C (Nagy et al., 1972). In this case, switching temperature of the spadix is about
37°C.
PRECISION OF THERMOREGULATION
The temperatures achieved by thermoregulating flowers depend somewhat on
ambient temperatures. With increasing ambient temperature, flower temperature
rises. The slope of this linear relationship is a measure of the precision (sometimes
called ‘‘gain’’) of temperature regulation. Perfect independence of flower tempera-
ture from ambient temperature would produce a slope of zero, and complete depen-
dence yields a slope of 1.0. Perfect independence is not possible, because the changes
in rate of heat production ultimately depend on flower temperature which must drop
in order to cause an increase in heating rate. Comparison of the four species of
thermoregulating plants reveals significant differences in precision of regulated tem-
perature (Fig. 5). The most precise thermoregulating species are the lotus N. nucifera,
with a slope of 0.17 (Seymour and Schultze-Motel, 1998) and P. selloum with a slope
of 0.18 during the peak heating phase (Nagy et al., 1972). In another study of
P. selloum, regulation was precise (0.19) in the peak phase of warming on the first
evening of flowering, but was less precise (0.52) in the plateau phase that occurs
during the next 12 hr (Seymour, 1999). Less precise regulation occurs in S. foetidus
with slopes of 0.29 in large inflorescences (Knutson, 1974) and 0.51 in small ones
(Seymour and Blaylock 1999). Similarly, the slope is 0.59 in D. ûulgaris (Seymour
and Schultze-Motel, 1999). Interestingly, it is apparent from the available data that
flowers that regulate at higher temperatures are more precise (Fig. 5). While it might
be thought that greater precision is possible in flowers that are better insulated or
of larger size, the inflorescences of P. selloum show greater precision during the first
episode of peak heat than in the longer plateau stage (Fig. 5). The precision of
thermoregulation should reflect the slope of the relationship between rate of respir-
ation and flower temperature above the switching temperature. The steeper the inhi-
bition of respiration at high temperatures, the greater the precision of
thermoregulation.
second night, the floral chamber is regulated at about 18°C and the heat production
rate of the florets is inversely related to ambient temperature (Fig. 6). It is clear that
temperature regulation is not associated with scent production, but rather with insect
entrapment. D. ûulgaris therefore demonstrates that thermoregulation is specific to
certain parts of the plant and is not always associated with all thermogenic tissues.
The species also shows that measurements of floral temperatures are poor indi-
cations of the rate of heat production. In this case, most of the heat generated by
the inflorescence comes from the appendix and relatively little from the spadix.
Almost all of the heat from the appendix is lost by evaporation, so appendix tem-
perature does not rise (Fig. 6).
morning (Fig. 7). When water-jacketed Nelumbo are artificially exposed to sudden
ambient temperature changes, they show a two-phase reponse (Seymour et al., 1998).
Cold air results in immediate cooling of the flower and a sharp drop in oxygen
consumption (a mass-action effect), followed by a slow regulatory rise in oxygen
consumption and rewarming; warm air produces the opposite effects. A similar lat-
ency appears in P. selloum (Seymour et al., 1983) and S. foetidus (Knutson, 1979)
following temperature change. Thermal inhibition of individual enzymes, or changes
in enzyme activity due to alterations in membrane structure and fluidity are likely
to occur immediately with temperature change (Steponkus, 1981). On the other
hand, the response latency of 2–3 hr may indicate the involvement of intermediate
metabolic regulators that act on rate-limiting enzymes, possibly the AOX, involved
in heat production. Such response latency may be associated with slow changes in
the concentrations of regulatory substances. It is known, for example, that organic
acids such as pyruvic acid activate the alternative pathway in mitochondria of sev-
eral plant species, including thermogenic arum lilies (Day et al., 1995). Cold exposure
for 8 hr is also known to activate respiration in a variety of chill-sensitive plant
species (Moynihan et al., 1995). Alternatively, it is possible that regulation occurs
by protein synthesis. Vanlerberghe and McIntosh (1992) reported an increase of
AOX activity in tobacco cells after transfer from 30°C to 18°C due to de noûo syn-
thesis of the protein.
Recent investigations on the biochemical control of thermoregulatory responses
have been carried out with the thermogenic receptacle tissue of N. nucifera (Beardall,
Seymour and Baldwin, unpubl.). The respiratory capacities of the alternative and
cytochrome pathways were compared in tissues obtained at two times of day when
234 Seymour
respiration was either high or low. In the cool morning, flower temperature was
about 30°C and thermogenesis was high; in the warm afternoon, the flower was
about 36°C and thermogenesis was low (Fig. 7). Plugs of tissue were incubated at
30°C or 36°C in the presence of either cyanide (to block the cytochrome pathway)
or propyl gallate (to block the alternative pathway) or both. Rates of oxygen con-
sumption during these treatments indicated the relative capacities of the two path-
ways, but not the actual activities in untreated tissue. Nevertheless, in the morning,
the capacity of the alternative pathway was high and it was markedly inhibited when
exposed to 36°C. In the afternoon, the alternative pathway was lower at 30°C and
less sensitive to exposure to 36°C. The capacity of the alternative pathway was very
low in non-thermogenic buds, increased threefold in thermoregulatory stages and
decreased again in older flowers that have no thermoregulatory ability. By contrast,
the capacity of the cytochrome pathway appeared to decrease during the thermoreg-
ulatory phase. These results suggest that temperature regulation involves the alterna-
tive pathway to a significant extent, but further work is required to measure activities
of both pathways under natural conditions and to determine the mechanism for
regulation of activity.
CONCLUSION
There is no doubt that the phenomenon of temperature regulation in flowers
seems bizarre and few people are carrying out research in the area. Only my labora-
tory is apparently actively seeking a biochemical explanation for it. Part of the
reason may be that so few thermoregulating plants have been discovered so far, and
they are considered to be mere curiosities. However, the phenomenon may have
been much more common during the early history of seed plants than it is today.
The simultaneous radiations of seed plants and beetles in the late Mesozoic era
suggest that thermoregulatory flowers may have commonly provided warm refuges
for endothermic, flying beetles (Seymour and Schultze-Motel, 1997). The direct
application of heat and the stability of temperature may have been an energetic
reward that may have been as important to pollination biology then as the nectar
and pollen rewards are today. Aside from the ecological and evolutionary impli-
cations of studies on thermoregulatory flowers, the phenomenon may have wider
application for plant (and even animal) respiratory control systems. For example,
inhibition of heat production at high tissue temperatures may influence respiration
of plant tissues warmed by the sun, or it may be associated with the limitation of
body temperature in humans during fever.
ACKNOWLEDGMENTS
I appreciate the invitation by Professor Leopoldo de Meis to write this review
and Drs John Beardall, John Baldwin, and Paul Schultze-Motel for unpublished
material.
Temperature Regulation in Thermogenic Flowers 235
REFERENCES
Chauveau, M., Dizengremel, P., and Lance, C. (1978) Thermolability of the alternative electron transport
pathway in higher plant mitochondria. Physiol. Plant. 42:214–220.
Day, D. A., Whelan, J., Millar, A. H., Siedow, J. N., and Wiskich, J. T. (1995) Regulation of the
alternative oxidase in plants and fungi. Aust. J. Plant Physiol. 22:497–509.
Elthon, T. E. and McIntosh, L. (1986) Characterization and solubilization of the alternative oxidase of
Sauromatum guttatum mitochondria. Plant Physiol. 82:1–6.
Elthon, T. E. and McIntosh, L. (1987) Identification of the alternative terminal oxidase of higher plant
mitochondria. Proc. Natl. Acad. Sci. USA 84:8399–8403.
Elthon, T. E., Nickels, R. L., and McIntosh, L. (1989) Mitochondrial events during the development of
thermogenesis in Sauromatum guttatum (Schott). Planta 180:82–89.
Gottsberger, G. (1990) Flowers and beetles in the South American Tropics. Bot. Acta 103:360–365.
Knutson, R. M. (1974) Heat production and temperature regulation in eastern skunk cabbage. Science
186:746–747.
Knutson, R. M. (1979) Plants in heat. Natural History 88:42–47.
Listabarth, C. (1996) Pollination of Bactris by Phyllotrox and Epurea. Implications of the palm breeding
beetles on pollination at the community level. Biotropica 28:69–81.
Meeuse, B. J. D. and Raskin, I. (1988) Sexual reproduction in the arum lily family, with emphasis on
thermogenicity. Sex. Plant Reprod. 1:3–15.
Miyake, K. (1898) Some physiological observations on Nelumbo nucifera, Gærtn. Gœrtn. Bot. Mag. Tokyo
12:112–117.
Moore, A. L. and Siedow, J. N. (1991) The regulation and nature of the cyanide resistant alternative
oxidase of plant mitochondria. Biochem. Biophys. Acta 1059:121–140.
Moynihan, M. R., Ordentlich, A., and Raskin, I. (1995) Chilling-induced heat evolution in plants. Plant
Physiol. 108:995–999.
Nagy, K. A., Odell, D. K., and Seymour, R. S. (1972) Temperature regulation by the inflorescence of
Philodendron. Science 178:1195–1197.
Nobel, P. S. (1999) Physicochemical and Enûironmental Plant Physiology. New York: Academic Press.
Prance, G. T. and Arias, J. R. (1975) A study of the floral biology of Victoria amazonica (Poepp.) Sowerby
(Nymphaeaceae). Acta Amazonica 5:109–139.
Raskin, I., Ehmann, A., Melander, W. R., and Meeuse, B. J. D. (1987) Salicylic acid: a natural inducer
of heat production in Arum lilies. Science 237:1601–1602.
Schneider, E. L. and Buchanan, J. D. (1980) Morphological studies of the Nymphaeaceae. XI. The floral
biology of Nelumbo pentapetala. Am. J. Bot. 67:182–193.
Schroeder, C. A. (1978) Temperature elevation in palm inflorescences. Principes 22:26–29.
Seymour, R. S. (1999) Pattern of respiration by intact inflorescences of the thermogenic arum lily Philo-
dendron selloum. J. Exp. Bot. 50:845–852.
Seymour, R. S., Bartholomew, G. A., and Barnhart, M. C. (1983) Respiration and heat production by
the inflorescence of Philodendron selloum Koch. Planta 157:336–343.
Seymour, R. S. and Blaylock, A. J. (1999) Switching off the heater: influence of ambient temperature on
thermoregulation by eastern skunk cabbage Symplocarpus foetidus. J. Exp. Bot. 50:1525–1532.
Seymour, R. S. and Schultze-Motel, P. (1996) Thermoregulating lotus flowers. Nature 383:305.
Seymour, R. S. and Schultze-Motel, P. (1997) Heat-producing flowers. Endeaûour 21:125–129.
Seymour, R. S. and Schultze-Motel, P. (1998) Physiological temperature regulation by flowers of the
sacred lotus. Phil. Trans. Roy. Soc. Lond. B 353:935–943.
Seymour, R. A. and Schultze-Motel, P. (1999) Respiration, temperature regulation and energetics of
thermogenic inflorescences of the dragon lily Dracunculus ûulgaris (Araceae). Proc. Roy. Soc. Lond.
Ser. B. Biol. Sci. 266:1975–1983.
Seymour, R. S., Schultze-Motel, P., and Lamprecht, I. (1998) Heat production by sacred lotus flowers
depends on ambient temperature, not light cycle. J. Exp. Bot. 49:1213–1217.
Siedow, J. N. and Berthold, D. A. (1986) The alternative oxidase: a cyanide-resistant respiratory pathway
in higher plants. Physiol. Plant. 66: 569–573.
Skubatz, H., Tang, W., and Meeuse, B. J. D. (1993) Oscillatory heat-production in the male cones of
cycads. J. Exp. Bot. 44:489–492.
236 Seymour
Skubatz, H., Williamson, P. S., Schneider, E. L., and Meeuse, B. J. D. (1990) Cyanide-insensitive respir-
ation in thermogenic flowers of Victoria and Nelumbo. J. Exp. Bot. 41:1335–1339.
Steponkus, P. L. (1981) Responses to extreme temperatures. Cellular and sub-cellular bases. In: Physio-
logical Plant Ecology I (O. L. Lange, P. S. Nobel, C. B. Osmond, and H. Ziegler, eds.), Springer-
Verlag, Berlin, pp. 371–402.
Thien, L. B., Azuma, H., and Kawano, S. (1999) New perspectives in the pollination biology of basal
angiosperms. In: XVI International Botanical Congress. St. Louis.
Vanlerberghe, G. C. and McIntosh, L. (1992) Lower growth temperature increases alternative pathway
capacity and alternative oxidase protein in tobacco. Plant Physiol. 100:115–119.