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Respiration by Thermogenic Flowers
Roger S. Seymour Ecology and Evolutionary Biology Adelaide University, Australia and Kikukatsu Ito Cryobiofrontier Research Center Iwate University, Japan
Over 200 years ago, the French biologist, Jean-Baptiste de Lamarck, wrote that the blossom of a European arum lily warmed up during the sequence of blooming (Lamarck, 1803 -1815). Since then, botanists have recorded significant self-heating in the flowers, inflorescences or cones in several families of plants, including Araceae, Arecaceae, Aristolochiaceae, Annonaceae, Cycadaceae, Cyclanthaceae, Hydnoraceae, Illiciaceae, Magnoliaceae, Nelumbonaceae, Nymphaeaceae, Rafflesiaceae, Schisandraceae and Winteraceae. These groups are all primitive seed-plants with rather large, fleshy floral structures that are often associated with beetle, bee or fly pollinators.
Some species, such as the arum lilies, are so intensely thermogenic that the temperature of their flowers can increase up to 35°C above the surroundings. For example, in Brazil, the inflorescence of Philodendron selloum is capable of warming to over 40°C at air temperatures close to freezing (Figure 1) (Nagy et al., 1972). Skunk cabbage, Symplocarpus, in North America and Japan, can maintain temperatures above 15°C when the air temperature drops to -15°C, and it often melts the snow around it (Seymour, 2004, Onda et al., 2008). The respiratory rates of some thermogenic flowers are the highest among plants, and in fact exceed even those of warm-blooded animals. For example, the tissues of Arum maculatum and Helicodiceros muscivorus produce up to about 400 milliWatts per gram (mW g-1) (Lance, 1974, Seymour et al., 2003a), while a flying hummingbird produces only 240 mW g-1. At an air temperature of 10°C, a 125 g inflorescence of P. selloum produces about five times the amount of the heat of a 125 g rat under the same conditions. Such high rates of heat production demand a good supply of oxygen. In the florets of P. selloum, this is achieved by diffusion through a network of tiny intercellular gas spaces that permeate the tissue to the center. Oxygen demand is so high, that the oxygen partial pressure at the center of the floret drops to about one-quarter of atmospheric, but remains just above the critical level where oxygen uptake becomes diffusion-limited (Seymour, 2001).
Heat production occurs by rapid respiration in the thermogenic cells of the flowers. In most thermogenic species studied so far, the substrate for respiration is carbohydrate, often imported from other parts of the plant, but in P. selloum, the substrate is lipid that is stored in the florets prior to blooming (Seymour et al., 1984). Analysis of heat production by direct calorimetry and respirometry show that all of the energy in the substrates ends up as heat in P. selloum (Seymour et al., 1983) and in the lotus, Nelumbo nucifera (Lamprecht et al., 1998). Although there is the possibility of some energy going into synthesis of floral structures, this appears to be negligible.
Heat production in thermogenic plants has been generally thought to be associated with an increase in the activity of the cyanide-resistant electron transport pathway in mitochondria (McIntosh, 1994). This pathway is mediated by the “alternative oxidase” (AOX) that accepts electrons from the ubiquinone pool and uses them to reduce oxygen to water. The free energy by the flow of electrons from ubiquinol to AOX does not generate ATP but instead is lost as heat. The AOX pathway seems to be present in all plants at variable capacity, but it is particularly active in thermogenic species (see Web Topic 11.3). For instance, a recent study on thermogenic receptacles of sacred lotus (N. nucifera) has revealed that an increase in respiration through the AOX is responsible for the heat production (Watling et al., 2006). On the contrary, in the case of mammals, uncoupling proteins (UCPs) have been shown to play a crucial role in non-shivering heat-production (Nicholls and Locke, 1984). UCPs reside in the mitochondrial inner membrane, across which they dissipate energy from the proton gradient that is built up by the respiratory chain, and this leads to heat production. In the skunk cabbage (Symplocarpus renifolius), thermogenic cells surrounding the stamens in the florets (Figure 2) appear to possess activities for both AOX and UCP, and this functional coexpression seems to be the molecular basis of heat production (Onda et al., 2008).
A few species of the most powerfully thermogenic flowers also exhibit temperature regulation, which is the maintenance of a relatively constant temperature in the flower, regardless of external air temperature. Rather precise thermoregulation has been discovered in Philodendron (Nagy et al., 1972), Symplocarpus (Knutson, 1974, Ito et al., 2004) and Nelumbo (Seymour and Schultze-Motel, 1996). In these cases, the respiratory rate increases almost linearly as the ambient temperature drops below 30°C, and the mean temperature of the flower is almost constant (Figure 3). Flower temperature varies only 6°C while ambient temperature varies 35°C. At low ambient temperatures during the night, heat production by the flower rises to about 1 Watt. On hot days, flower temperature drops as much as 10°C below effective ambient temperature by evaporative cooling. Respiration clearly responds to ambient temperature, not time of day (Seymour et al., 1998). However, it is apparent that the flowers do not detect ambient temperature directly, but only respond to changes in the temperature of their own cells. Close examination of the data reveals that there is a small decrease in flower temperature that occurs with falling ambient temperature (Figure 3). Therefore is it clear that respiration in these species is negatively related to tissue temperature, opposite to the expected positive relationship between temperature and rates of biochemical reactions.
The physiological thermoregulatory control mechanism is not yet known. It is certain, however, that it is unlike the mechanism in birds and mammals that relies on a complex nervous interaction between temperature receptors, central nervous system processing and finally control of organs that affect rates of heat production and loss. In the plants, the regulation must occur at a strictly biochemical or molecular level. One clue is that the rate of AOX-mediated respiration of mitochondria isolated from Arum maculatum increases with temperature to a peak at about 32oC, above which it falls steeply (Wagner et al., 2008). Control of AOX activity has been shown to respond to changes in the disulfide bridge that binds the two halves of the AOX dimer (Umbach and Siedow, 1993) or activation by α-keto acids (Millar et al., 1993). However neither of these mechanisms seems to occur in A. maculatum, and thermoregulation has been proposed to result from an interaction between the thermal profiles of the AOX and dehydrogenases earlier in the metabolic pathway (Wagner et al., 2008).
Temperature regulation is an adaptation shared by homeothermic (warm-blooded) birds and mammals and many groups of flying insects. High and stable body temperatures permit them to be active in cold environments. Compared to thermally compliant poikilotherms (cold-blooded animals), animal homeotherms are able to find more food, better compete for territory and mates, and reproduce faster—all evolutionarily advantageous in many circumstances. So homeothermy in immobile flowers is at first difficult to explain. Temperature regulation is not a requirement to enhance the vaporization of scents; unregulated high temperatures would suffice, as they do in the appendix of Dracunculus vulgaris inflorescences (Seymour and Schultze-Motel, 1999). However, we now have evidence that thermoregulation in the flowers is a service offered as a reward to insect visitors (Seymour et al., 2003b). Thermoregulatory flowers are often pollinated by large flying insects, chiefly beetles, which remain within the flower for about 24 h. For example, large scarab beetles congregate in the evening inside the floral chamber of Philodendron solimoesense in lowlands French Guiana, and they are active throughout the night, consuming floral parts and mating avidly (Figure 4). These activities apparently require high body temperatures, because the beetles raise their temperature by a kind of “shivering” that involves heat-generating contractions of their flight muscles. However, the energy cost of this activity inside the floral chamber is some 2-4 times less than it would be outside, despite a chamber temperature only 4°C warmer than the outside air. While many non-thermoregulatory flowers offer energy in the form of nectar, starch or pollen to their insect visitors, thermoregulatory flowers can offer energy directly as heat. In return, the beetles transfer pollen each day from one flower to the next.
Temperature regulation is also important for proper floral development and pollination success. Artificially-enforced low temperatures reduce fertilization and seed set in thermoregulatory Nelumbo nucifera (Li and Huang, 2009). In vitro pollen germination rate and pollen tube growth rate in Symplocarpus renifolius are optimal at 23 oC, which is the regulated temperature, and decrease so steeply at higher and lower temperatures that pollination would be impossible at natural ambient temperature (Seymour et al., 2009). However, it is likely that the temperature sensitivities of developmental features have evolved in response to the primary thermal stability of the flowers, rather than vice versa.
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