The Hot and the Classic

Plant Thermogenesis and thermoregulate: They can alter their pounds) are liberated during the ther- thermogenic properties to maintain a mogenic activity in voodoo lily Thermoregulation surprisingly constant temperature (Sauromatum guttatum; Skubatz et al., One of the drawbacks of our current even under fluctuating environmental 1996) Electron microscopy revealed preoccupation with model organisms temperatures. that the endoplasmic reticulum (ER) in- and our inveterate focus on crop teracts with the plasma membrane, cre- is that our natural curiosities ating novel routes of excretion of the about some of the more bizarre plants The Raison d’Eˆ tre of volatiles to the exterior of the cell. The in the world go largely unsatisfied. I Thermogenesis foul odor produced by the appendix suspect that many readers of this jour- attracts at least 30 species of insects. In nal were inspired to become Many reasons for the occurrence of the case of temperate-zone, early flow- physiologists when they first observed thermogenesis in have been ering skunk cabbage, however, there is time-lapse images of a climbing ten- put forward. Thermogenesis may en- a paucity of good insect to dril, or touched a Mimosa pudica plant, sure protection of flowers during pe- attract and, in fact, in the case of Sym- or, usually with disappointing results, riods of cold temperature. For exam- plocarpus renifolius, only 13% of the fed their first to Dionaea muscipula. ple, the spadices of eastern skunk spadices set (Uemura et al., 1993). Plant movements and plant carnivory cabbage are not frost-resistant, even In addition to attracting insect polli- are two examples of plant functions though they can emerge from snow- nators by smell, thermogenic flowers that, in a grand and anthropocentric covered ground (Knutson, 1974). may also attract insects by heat. The view of life, are in themselves not ter- Avoiding frost damage, however, can- floral temperatures of thermogenic ribly important. Their fascination to us not be the primary function of thermo- plants are in the range required by en- dothermic insects for purposes of mat- (and to the minds of children) lies in genesis: Most members of the ing and flight (Schneider and Buchanan, the fact that these seemingly animal- are tropical species that would have 1980; Seymour and Schulze-Motel, like behaviors challenge our precon- no need to escape frost in nature. 1997). ceived notions of what plants are capa- Rather, frost-avoidance by thermo- ble of doing, and make us appreciate, genesis may reflect a physiological ex- aptation of a process that originally often for the first time, that the plant evolved in response to selective pres- and animal kingdoms have more in sures other than frost. Other research- Mechanism of Plant common than they do differences. ers have suggested that thermogenesis Thermogenesis A third plant function that the un- and thermoregulation may help pro- initiated often expect is limited to the It has long been known that thermo- vide the optimum temperature for flo- animal world is thermogenesis. The genesis is linked to a burst of cyanide- ral development or pollen tube most dramatic examples of plant ther- resistant respiration involving the al- growth (Ervik and Barfod, 1999). Sey- mogenesis occur in certain types of ternative oxidase pathway (James and mour and Blaylock (1999) found that flowers, particularly, but not exclu- Beevers, 1950; Meeuse, 1975). Classical warming did advance the develop- sively, in the Araceae. Although most studies revealed that heat production ment and early flowering of eastern studies of plant thermogenesis have usually begins first in male flowers skunk cabbage but pointed out that and then spreads throughout the in- examined Araceae, it must be borne in the adaptive value of this was obscure: florescence. It was hypothesized that mind that thermogenesis has been Many plants were observed complet- this pattern was a reflection of the measured in the flowers of members ing their blooming beneath a layer of movement of a chemical signal “cal- of eight other angiosperm families as forest litter and sometimes a layer of origen.” Salicylic acid may be “calori- well as in the cones of various species snow. gen”: it triggers an increase in the al- of cycads (Thien et al., 2000). There is Other hypotheses concerning the ternate oxidase and heat evolution in some evidence that thermogenesis, al- raison d’eˆtre of thermogenicity in the voodoo lily (Raskin et al., 1987), beit at rates much less than those ob- flowers have focused on the effects it but it has it not been demonstrated served in thermogenic flowers and may have in attracting pollinators. that it moves in the same manner as cones, may be a property of most The heat produced by thermogenic “calorigen.” In fact, it may be the sen- plants. It should also be noted that flowers helps to volatilize odorous sitivity of the tissue to salicylic acid some plants, including Philodendron compounds that attract carrion , that increases daily with the approach selloum (Nagy et al., 1972), eastern beetles, and other insects, and there is of anthesis (Raskin et al., 1987). skunk cabbage ( foetidus) a strong temporal correspondence be- (Knutson, 1974), the sacred lotus tween thermogenicity and the release ( nucifera) (Seymour and of such odors (Lamprecht et al., 2002). Schulze-Motel, 1996, and Rhizanthes More than 100 compounds from at ៮ How Widespread is Plant lowiiMDNM (Patino et al., 2000) can least nine different chemical classes Thermoregulation? (monoterpenes, sesquiterpenes, fatty www.plantphysiol.org/cgi/doi/ acids, ketones, alcohols, aldehydes, in- Many but not all plants increase al- 10.1104/pp.900071. dole, and phenolic and sulfur com- ternate oxidase activity at low temper-

Plant Physiology, MayDownloaded 2003, Vol. 132, from pp. www.plantphysiol.org 25–26, www.plantphysiol.org on February © 12, 2003 2017 American - Published Society by www.plantphysiol.org of Plant Biologists 25 Copyright © 2003 American Society of Plant Biologists. All rights reserved. atures (e.g., Ito et al., 1997; Gonzalez- Nevertheless, Breidenbach et al. (1997), Meeuse BJD (1975) Thermogenic respiration in Meier et al., 1999;). Salicylic acid also while not contesting the increase is aroids. Annu Rev Plant Physiol 26: 117–126 Moynihan MR, Ordentlich A, Raskin I (1995) increases alternate oxidase, alternative heat given off by some chilled plant Chilling-induced heat evolution in plants. respiration and heat production in species, criticized the idea that the al- Plant Physiol 108: 995–999 tobacco suspension cell cultures ternative pathway is thermoregulatory Nagy KA, Odell DK, Seymour RS (1972) Tem- (Kapulnik et al., 1992; Rhoads and and serves to protect plants from expo- perature regulation by the inflorescence of McIntosh, 1993). It has been postu- sure to cold. They argued that the dif- Philodendron. Science 178: 1195–1197 Nevo E, Ordentlich, Belies A, Raskin I (1992) lated that the alternative respiratory ferent oxidative pathways in the mito- Genetic divergence of heat production within pathway may help to maintain mito- chondria do not have large differences and between the wild progenitors of wheat chondrial electron transport at low in enthalpy, and that the observed heat and barley: evolutionary and agronomical im- temperatures that would otherwise in- rate increases are insufficient to cause plications. Theor Appl Gen 84: 958–962 Patino S, Grace J, Banziger H (2000) Endothermy hibit the main phosphorylating path- significant temperature increases of by flowers of Rhizanthes lowii (Rafflesiaceae). way and lead to the formation of toxic physiological importance in non-ther- Oecologia 124: 149–155 reactive oxygen species. This role is mogenic plants. Raskin I, Ehmann A, Melander WR, Meeuse supported by the observation that al- BJD (1987) Salicylic acid: a natural inducer of ternative oxidase protein levels and heat production in Arum lilies. Science 237: LITERATURE CITED 1602–2602 alternate oxidase activity often in- Rhoads DM, McIntosh L (1993) Cytochrome and crease when plants are subjected to Breidenbach RW, Saxton MJ, Hansen LD, alternate pathway respiration in tobacco. Ef- growth at low temperatures (e.g., Criddle RS (1997) Heat generation and dissi- fects of salcylic acid. Plant Physiol 103: 877–883 Nevo et al., 1992; Moynihan et al., pation in plants: Can the alternative oxidative Schneider EL, Buchanan J (1980) Am J Bot 67: phosphorylation pathway serve a thermoreg- 182–193 1995; Vanderstraeten et al., 1995). ulatory role in plant tissues other than special- Seymour RS, Blaylock AJ (1999) Switching off Nevo et al. (1992) proposed that ther- ized organs? Plant Physiol 114: 1137–1140 the heater: influence of ambient temperature mogenesis resulting from increased Ervik F, Barfod A (1999) Thermogenesis in palm on thermorgulation by eastern skunk cabbage engagement of the alternative oxidase inflorescences and its ecolgocial significance. Symplocarpus foetidus. J Exp Bot 50: 1525–1532 Acta Bot Venez 22: 195–212 Seymour RS, Schulze-Motel (1996) Thermoregu- pathway may be a genetic adaptation Gonzalez-Meier MA, Ribas-Carbo M, Giles L, lating lotus flowers. Nature 383: 305 to avoid cold temperatures. When Siedow JN (1999) The effect of growth and Skubatz H, Kunkel DD, Howald WN, Trenkle tissues from Triticum dicoccoides and measurement temperature on the activity of R, Mookherjee B (1996) The Sauromatum gut- Hordeum spontaneum were exposed to the alternative respiratory pathway. Plant tatum appendix as an osmophore: Excretory low temperature, metabolic heat rates Physiol 120: 765–772 pathways, composition of volatiles and attrac- Ito Y, Saisho D, Nakazono M, Tsutsumi N, Hirai tiveness to insects. New Phytol 134: 631–640 measured at 20°C increased markedly A (1997) Transcript levels of tandem-arranged Thien LB, Azuma H, Kawano S (2000) New per- as a result of cold treatment. This re- alternative oxidase genes in rice are increased spectives on the biology of basal sponse was cultivar specific, the re- by low temperature. Gene 203: 121–129 angiosperms Intl J Plant Sci 161: S225–S235 sponse being greater in accessions James WO, Beevers H (1950) The respiration of Uemura S, Ohkawara K, Kudo G, Wada N, Hi- Arum spadix. New Phytol 49: 353–374 gashi S (1993) Heat-production and cross- from colder regions. Besides prevent- Kapulnik Y, Yalpani N, Raskin I (1992) Salicylic pollination of the Asian skunk cabbage Symp- ing free radical damage, another way acid induces cyanide resistant respiration in locarpus renifolius (Araceae). Am J Bot 80: that thermogenicity might help plants tobacco cell suspension cultures. Plant Physiol 635–640 exposed to cold temperatures to sur- 100: 1921–1926 Vanderstraeten D, Chaerle L, Sharkov G, Lam- Lamprecht I, Schmolz E, Blanco L, Romero CM bers H, Van Montagu M vive is by heat itself: Sometimes a frac- (1995) Salicylic-acid (2002) ovens: thermal investigations on enhances the activity of the alternative path- tion of 1°C is all that is necessary to heat producing plants. Thermochim Acta 391: way of respiration in tobacco- and in- protect a plant from cold damage. 107–118 duces thermogenicity. Planta 196: 412–419

Peter V. Minorsky Department of Natural Sciences Mercy College Dobbs Ferry, NY 10522

26 Downloaded from www.plantphysiol.org on February 12, 2017 - Published by www.plantphysiol.orgPlant Physiol. Vol. 132, 2003 Copyright © 2003 American Society of Plant Biologists. All rights reserved.