Hot Topic for Early Spring: Thermogenesis of Eastern Skunk Cabbage

Co-Authored by Dean J. Campbell* and Kristi McQuade* *Bradley University, Peoria, Illinois

Some of the very first flowers to appear in portions of the eastern United States are those of the eastern skunk cabbage (Symplocarpus foetidus).¹ They resemble small reddish cones rising several centimeters out of swampy soil. For example, the skunk cabbage blossoms shown in Figure 1 were observed in central Illinois in late February. While the blossoms are not generally considered to be visually spectacular, they harbor fascinating biochemistry that can be used in the classroom to illustrate thermochemical principles.

Eastern skunk cabbage belongs the Araceae family of plants, many of which are thermogenic (heat-producing) and many of which emit a foul odor. The heat is believed to help volatilize the odorous compounds in order to attract pollinating insects to the flowers. For eastern skunk cabbage at least, the rotten odor is not limited to the flowers; all parts of the plant produce an unpleasant smell when damaged.² The flowers also might provide shelter and beneficial warmth for the pollinating insects. The heat can help to melt snow and thaw frozen ground, enabling the blossoms to emerge in late winter/early spring. The increased temperatures of skunk cabbage are temporary, only lasting for a couple of weeks.¹

So where does the heat come from? To answer that question one must first review a little biochemistry. While plants are best known for their ability to use photosynthesis to convert CO₂ to carbohydrates, they can also break down those carbohydrates to produce energy. In the typical cellular respiration of carbohydrates, an electron transport chain, mediated by several proteins embedded within the inner mitochondrial membrane, ends with the reduction of oxygen to water. The same proteins use the energy produced from these favorable electron transfer reactions to pump hydrogen ions (protons) across the inner mitochondrial membrane, creating an electrochemical gradient. This is analogous to pumping water into a reservoir behind a dam. In the final “payoff” step of the process, the enzyme ATP synthase uses the potential energy stored in the proton gradient (the “proton motive force”) to pay for the thermodynamically unfavorable conversion of adenosine diphosphate and inorganic phosphate to adenosine triphosphate (ATP), the main energy currency of life.³ This is analogous to using the spontaneous flow of water from the reservoir to spin the turbines in a hydroelectric power plant.

These conversions of energy from one form to another, referred to as “energy transduction,” do not typically produce much heat. However, thermogenic plants, including the eastern skunk cabbage, hijack that process and produce heat by “uncoupling” carbohydrate oxidation from ATP synthesis. One of the ways they do this involves a modified electron transport pathway in which the enzyme alternative oxidase (AOX) substitutes for the final protein in the electron transport chain.^3,4 AOX catalyzes the transfer of electrons to oxygen, forming water, but its inability to pump protons means that the energy produced by the reaction is dissipated as heat rather than being used to produce ATP. In addition to the modified electron transport pathway, thermogenic plants also use a second approach to produce heat. This one involves uncoupling proteins (UCPs),^3,5 which are inner mitochondrial membrane proteins that function as proton channels. The membrane becomes “leaky,” with hydrogen ions flowing through the UCPs in a manner not unlike water flowing through holes in a dam. Passive flow of protons through the channels dissipates the proton gradient, bypassing ATP synthase and releasing the potential energy stored in the proton gradient in the form of heat. UCPs are also a key component of non-shivering (brown-fat) thermogenesis in mammals, including humans.

Figure 1: Two eastern skunk cabbage blossoms viewed with visible light (LEFT) and with an FLIR camera (MIDDLE AND RIGHT). The middle thermogram reads a temperature of 0.9°C away from the blossom and the right thermogram reads a temperature of 22.3°C coming from within the blossom.

The heat produced by skunk cabbage blossoms can be detected using a forward-looking infrared (FLIR) camera. FLIR is a type of thermography which typically uses infrared energy of roughly 7,000-14,000 nm wavelength to produce an image of the temperature of objects. These heat images (thermograms) can be shown in either black and white or false color and provide a powerful non-contact method for estimating the temperature of many objects at the same time.⁶ FLIR cameras have decreased in price and have become more widely available over the years. Figure 1 shows a visible light image and FLIR images of two eastern skunk cabbage blossoms in a local marshy area. The camera used to produce the thermograms in Figure 1 and the related YouTube video was an FLIRONE Pro for iOS (FLIR Systems, Inc.), which is sufficiently small to attach to an iPhone. These images clearly show that the blossoms are warmer than their immediate surroundings. The highest reading was 22.3°C in the gap in the wall of the left blossom, and the lowest reading in the immediate vicinity was 0.9°C. Note that some of the background of the thermograms shows some yellowish color, which might be areas of warmer water or rotting vegetation.

Video 1: Video of eastern skunk cabbage blossoms, ChemDemos YouTube Channel (accessed 3/6/21)

These thermogenic blossoms make for interesting discussions in biology¹ and chemistry courses. Plants are well known for using light energy to convert carbon dioxide and water to carbohydrates and oxygen gas, but this example illustrates that plants also consume those carbohydrates to produce energy.

In the textbook model of cellular respiration, the energy of carbohydrate oxidation is used to “pay” for ATP synthesis, and while the theoretical ATP yield can be readily calculated, inefficiencies in the process mean the true yield is lower. The process of thermogenesis takes this energy inefficiency even further. With the use of the alternative oxidase and uncoupling proteins in thermogenic plants, some of the energy from carbohydrate oxidation is rerouted into heat production, rather than producing ATP. Simplistically put, the plants are burning carbohydrates to warm up. The loss of ATP is a worthwhile trade-off for these plants, providing much-needed heat that enables them to exploit environmental conditions that other plants simply cannot handle. The humble first blossoms of spring are thermochemically spectacular!

Safety The plants can contain calcium oxalate crystals, which have toxicity by ingestion. To get close to these blossoms, one will likely encounter cold, wet, and muddy conditions. In some areas, these plants might be protected species or grow in fragile wetlands.

Acknowledgements This work was supported by Bradley University and the Mund-Lagowski Department of Chemistry and Biochemistry with additional support from the Illinois Heartland Section of the American Chemical Society and the Illinois Space Grant Consortium. The FLIR camera was provided through a subcontract from a grant from the National Science Foundation Division of Undergraduate Education, awards 1813313 and 1626228.

References

1. Nicholson, B. J.; Halkin, S. L. “Temperature Relationships in Eastern Skunk Cabbage.” Bioscene, 2007, 33, 6-14.
2. Flora of North America, Symplocarpus foetidus, eFloras.org (accessed March, 2021).
3. Onda, Y.; Kato, Y.; Abe, Y.; Ito, T.; Morohashi, M.; Ito, Y.; Ichikawa, M.; Matsukawa, K.; Kakizaki, Y.; Koiwa, H.; Ito, K. “Functional Coexpression of the Mitochondrial Alternative Oxidase and Uncoupling Protein Underlies Thermoregulation in the Thermogenic Florets of Skunk Cabbage.” Plant Physiol., 2008, 146, 636–645.
4. Berthold, D. A.; Siedow, J. N. “Partial purification of the cyanide-resistant alternative oxidase of skunk cabbage (Symplocarpus foetidus) mitochondria.” Plant Physiol., 1993, 101, 113–119.
5. Ito, T.; Matsukawa, K.; Kato, Y. “Functional analysis of skunk cabbage SfUCPB, a unique uncoupling protein lacking the fifth transmembrane domain, in yeast cells.” Biochem. Biophys. Res. Commun., 2006, 349, 383-390.
6. Green, T.; Gresh, R,; Cochran, D.; Crobar, K.; Blass, P.; Ostrowski, A.; Campbell, D.; Xie, C.; Torelli, A. “Invisibility Cloaks and Hot Reactions: Applying Infrared Thermography in the Chemistry Education Laboratory.” J. Chem. Educ., 2020, 97, 710-718.