Journal of Integrative Plant Biology 2011, 53 (1): 7–13

Invited Expert Review

Regulation of Thermogenesis in Plants: TheInteraction of Alternative Oxidase and PlantUncoupling Mitochondrial ProteinYan Zhu1, Jianfei Lu1, Jing Wang2, Fu Chen3, Feifan Leng1 and Hongyu Li1

∗

1MOE Key Laboratory of Arid and Grassland Ecology, School of Life Sciences, Lanzhou University, Lanzhou 730000, China2College of Food Science and Engineering, Gansu Agriculture University, Lanzhou 730070, China3Institute of Potato, Gansu Academy of Agricultural Sciences, Lanzhou 730070, China∗Corresponding author

Tel: +86 931 891 0560; Fax: +86 931 891 2561; E-mail: lihy@lzu.edu.cnAvailable online on 10 November 2010 at www.jipb.net and www.wileyonlinelibrary.com/journal/jipbdoi: 10.1111/j.1744-7909.2010.01004.x

Hongyu Li

(Corresponding author)

Abstract

Thermogenesis is a process of heat production in living organisms. Itis rare in plants, but it does occur in some species of angiosperm.The heat is generated via plant mitochondrial respiration. As possibleinvolvement in thermogenesis of mitochondrial factors, alternative ox-idases (AOXs) and plant uncoupling mitochondrial proteins (PUMPs)have been well studied. AOXs and PUMPs are ubiquitously present inthe inner membrane of plant mitochondria. They serve as two majorenergy dissipation systems that balance mitochondrial respiration anduncoupled phosphorylation by dissipating the H+ redox energy andproton electrochemical gradient (�μH+) as heat, respectively. AOXs andPUMPs exert similar physiological functions during homeothermic heatproduction in thermogenic plants. AOXs have five isoforms, while PUMPshave six. Both AOXs and PUMPs are encoded by small nuclear multigenefamilies. Multiple isoforms are expressed in different tissues or organs.

Extensive studies have been done in the area of thermogenesis in higher plants. In this review, we focuson the involvement and regulation of AOXs and PUMPs in thermogenesis.

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 uncouplingmitochondrial protein. J. Integr. Plant Biol. 53(1), 7–13.

Introduction

Many plants have the ability to generate heat to raise theirtemperature above air temperature. Such a phenomenon iscalled thermogenesis. To date, thermogenesis has been re-ported in flowers, inflorescences or cones in several families ofplants including Araceae (Seymour et al. 2003; Seymour, 2004;Wagner et al. 2008; Kamata et al. 2009), Cycadaceae (Tang1987; Seymour et al. 2004), Nelumbonaceae (Seymour andSchultze-Motel 1998; Watling et al. 2006), and Nymphaeaceae(Skubatz et al. 1990a). It is well accepted that thermoge-

nesis in thermogenic plants is usually related to attractingpollinators by volatilizing scents, and to allowing a speciesto grow in a cold climate (Seymour 2001; Seymour et al.2003; Seymour and Gibernau 2008), but in some cases itwas proposed to provide the optimal temperature for pollengermination and pollen tube growth (Onda et al. 2008; Seymouret al. 2009). Thermogenic plants, such as skunk cabbage(Symplocarpus renifolius), can keep the temperature in thetissue/organ around 20 ◦C, even if air temperature falls to−15 ◦C (Ito et al. 2004; Onda et al. 2008; Seymour et al.2009). The inflorescence of Philodendron sellom maintains a

C© 2011 Institute of Botany, Chinese Academy of Sciences

8 Journal of Integrative Plant Biology Vol. 53 No. 1 2011

core temperature of 38 ◦C to 46 ◦C, despite air temperaturesranging from 4 ◦C to 39 ◦C (Nagy et al. 1972; Seymouret al. 1983). The sacred lotus (Nelumbo nucifera) can maintaintemperatures of the receptacle between 30 ◦C and 36 ◦C forseveral days, despite changes in environmental temperaturesbetween 10 ◦C and 45 ◦C (Seymour et al. 1998; Watling et al.2006). These plants have the ability of thermoregulations: theycan alter their thermogenic properties to maintain a surprisinglyconstant temperature even under fluctuating environmentaltemperatures.

The heat is generated via plant mitochondrial respiratorychain, which consists of the oxidative phosphorylation pathway(containing complex I, III, and IV) and two non-phosphorylatingpathways, cyanide-resistant respiratory pathway (Zhao et al.2007) and plant uncoupling mitochondrial proteins (PUMPs)(Plaxton and Podesta 2006) (Figure 1). Cyanide-resistant respi-ration is mediated by the nuclear-encoded, alternative oxidase(AOX) that functions as a homodimer in the mitochondrial innermembrane of plants. AOX is found in all plants examined todate. Electron transport to the AOX diverges from the phos-phorylating pathway at ubiquinone pool and electron flow to theAOX dramatically reduces the energy yield of respiration (Akenet al. 2009). It has long been known that thermogenesis is linkedto a burst of cyanide-resistant respiration. Increased AOXactivity was detected during blossoming of Aroide (Meesue1975) and sacred lotus (Watling et al. 2006; Grant et al. 2008).Thermogenic plants stimulated much of the initial interest in

Figure 1. Diagrammatic representation of the plant mitochondrial electron transport chain and energy dissipation systems.

I (complex I); nicotinamide adenine dinucleotide reduced (NADH) dehydrogenase; II (complex II), succinate dehydrogenase; III (complex III),

oxidoreductase ubiquonol-cytochrome c; IV (complex IV), cytochrome c oxidase; AOX, alternative oxidase; c, cytochrome c; UQ, ubiquinone;

V, (complex V) adenosine tri-phosphate (ATP) synthase; PUMP, plant uncoupling mitochondrial protein; �μH+, proton electrochemical

gradient built by the cytochrome pathway; NDex, external NAD(P)H dehydrogenases; NDin internal NAD(P)H dehydrogenases; IMS,

intermembrane space; IMM, inner mitochondrial membrane. The cytochrome electron transport chain are shown in white. The energy

dissipation systems are shown in black.

the alternative pathway, but there was surprisingly little workwith thermogenic species until PUMPs were found in plants(Vercesi et al. 1995; Laloi et al. 1997). PUMPs are present in theinner membrane of plant mitochondria and allow a transmem-brane H+ flux, which uncouples respiration from adenosinetriphosphate (ATP) synthesis and dissipates chemical energyinto metabolic heat (Jezek et al. 1996; Vercesi et al. 2006).They were shown in a variety of organs and tissues of higherplants, including thermogenic spadices of skunk cabbage (Ito1999) and thermogenic receptacles of the sacred lotus (citedby Watling et al. 2006). PUMPs are homologs of mammalianmitochondrial uncoupling proteins (UCPs) and have up tosix isoforms in plants (Borecky et al. 2001). In plants, bothAOXs and PUMPs are involved in uncoupling respiration andoxidative phosphorylation, which leads to direct dissipationof the �μH+ as heat. The function of AOXs and PUMPs isclosely coordinated suggesting a possible involvement of bothproteins in thermogenesis. Since co-expression of AOXs andPUMPs in plant tissues was found, both AOXs and PUMPswere proposed to be the putative thermogenic factor in plants(Sluse et al. 1998; Considine et al. 2001; Ito and Seymour 2005;Ito-Inaba et al. 2008a, 2008b). But what are their individualroles in thermogenesis? The mechanisms of those two energydissipations in thermogenesis have been an area of intenseinvestigation. AOXs and PUMPs as the possible mitochondrialfactors involved in thermogenesis are discussed in this mini-review.

Energy Dissipation Systems in Thermogenesis of Plants 9

Mechanism of Thermoregulation in theNelumbonaceae (Lotus)

As homoeothermic plants, sacred lotus (Nelumbo nucifera)belongs to the Nelumbonaceae. To our knowledge, sacredlotus is the only thermoregulating dicot so far described.Extensive work has been done in the area of mechanism ofthermoregulation in sacred lotus (Watling et al. 2006; Grantet al. 2008, 2009).

In sacred lotus, strong thermoregulatory activity is foundwithin the spongy tissues of the receptacle (Seymour andSchultze-Motel 1998). Three distinct physiological phases inflowers of the sacred lotus were identified: pre-thermogenic,thermogenic, and post-thermogenic (Watling et al. 2006). Arapid increase in alternative pathway flux and AOX proteinassociated with thermogenesis was observed in the thermo-genic phase and a rapid decrease in AOX protein occurredpost-thermogenesis. In contrast, cytochrome pathway flux didnot change significantly during thermogenesis (Watling et al.2006). In plants, the activity of PUMPs would result in highfluxes through the cytochrome pathway (Vercesi et al. 1995;Ito 1999; Jezek et al. 2000; Ricquier and Bouillaud 2000;Møller 2001), thus, there is no correlation between PUMPs andheating in thermogenic lotus. These findings suggest that AOXsare responsible for thermogenesis in sacred lotus; PUMPs donot play a significant role in this species (Watling et al. 2006;Grant et al. 2008).

Regulation of AOX has been extensively studied in non-thermogenic plants. Transcriptional and post-translational reg-ulation mechanisms have been identified (Umbach et al. 2002).The flowers of sacred lotus control their temperature preciselyby regulating the activity of AOXs. Although the role of AOXs inthermoregulation in sacred lotus has been confirmed (Watlinget al. 2006), the mechanisms of thermoregulation in this speciesremain unclear. It is still unknown whether the regulation occursat the transcriptional level or post-translational level. Grantet al. (2008) determined that thermogenesis via the AOXpathway in the sacred lotus receptacle was precisely regulatedthrough changes in AOX flux rather than changes in proteincontent. No clear correlation was found between AOX fluxand either heating or AOX protein content, suggesting thatregulation of thermogenesis in this species is likely to be post-translational (Grant et al. 2008). In plants, post-translationalregulation of AOX is controlled by two related mechanisms:the reduction status of a disulfide bond and the α-keto acidsregulation. It was reported that the detected AOX proteinfrom sacred lotus receptacles was present in the reducedform, suggesting it is unlikely that the AOX reduction statusis a regulatory mechanism (Grant et al. 2009). This leavesone possibility that thermoregulation of AOX in sacred lotusreceptacles is achieved via the α-keto acids regulation. Themechanism of α-keto acids (typically pyruvate) regulation is

complex and involves two conserved cysteine residues. Cys1

and Cys2 were found in AOX sequences of several thermogenicspecies (Umbach et al. 2002). However, in thermogenic sacredlotus the AOX proteins (NnAOX1a and NnAOX1b) lack theregulatory Cys1, which is replaced by Ser. Cys2 might alsobe missing (Grant et al. 2009). These observations indicatedthat the activity of AOX was not stimulated by private; in-stead, it was stimulated by succinate in thermogenic sacredlotus.

Mechanism of Thermoregulation in the Araceae

The most dramatic examples of plant thermogenesis are in theAraceae. Araceae belongs to the monocot family and containsmany thermogenic species such as eastern skunk cabbage(Symplocarpus renifolius) (Ito-Inaba et al. 2009a), dead-horsearum (Helicodiceros muscivorus) (Ito et al. 2003; Seymouret al. 2003), Arum maculatum (Bermadinger-Stabentheinerand Stabentheiner 1995), voodoo lily (Sauromatum guttatum)(Skubatz et al. 1991), Arum italicum (Skubatz et al. 1990b;Albre et al. 2003), and Philodendron selloum. Thermogenicplants in Araceae are divided into unisexual flowers and bisex-ual flowers (Cabrera et al. 2008) and the heat is generatedfrom the appendix and male florets or the spadix in theseplants. According to reports, the male florets in dragon lily(Dracunculus vulgaris) (Ito and Seymour 2005), the male andsterile male florets in Philodendron melinonii (Barabe et al.2002; Seymour and Gibernau 2008), and the spadix in skunkcabbage (Symplocarpus renifolius) (Ito et al. 2003) are allthermogenic organs in these species. So, they are importantmaterials for studying the mechanism of thermogenesis.

The dead horse arum (Helicodiceros muscivorus) showsstrong thermogenicity in the appendix and male florets. Re-markable AOX gene expression was found in their thermogenicmitochondria (Ito et al. 2003). However, the PUMP expressionis not limited to the thermogenic floral organs but rather ubiqui-tous including the non-thermogenic female florets, spathe andclub-shaped organs of the spadix (Ito et al. 2003). The equalexpression of PUMP in both thermogenic and nonthermogenictissues indicated that PUMP might not necessarily regulatethe thermogenesis in this species. Similarly, high levels ofthe alternative pathway capacity were found to coincide withspadix maturation of voodoo lily (Sauromatum guttatum), andthe expression of AOX changed in this period (Elthon et al.1989; Rhoads and McIntosh 1992). In dragon lily (Dracunculusvulgaris), expression of the AOX gene occurred in highlythermogenic male florets, but not in nonthermogenic tissuesof the same plant. The content of AOX protein increased withincreasing thermogenic activity and declined immediately afterheat production (Ito and Seymour 2005). These results indicatethat the AOX protein has important roles in thermogenic plants,

10 Journal of Integrative Plant Biology Vol. 53 No. 1 2011

whereas the involvement of PUMPs in thermogenesis in theseplants is doubtful.

Recently, possible thermogenesis of both systems was stud-ied intensively in skunk cabbage (Symplocarpus renifolius)which is capable of increasing and maintaining its inflorescencetemperatures for several days and belongs to the bisexualflower group of Araceae (Ito-Inaba et al. 2009a). The spadix ofskunk cabbage is the main thermogenic tissues. Developmentof the spadix of this species can be divided into four stages:immature, female, bisexual, and male. Only the female-stagespadix produces massive heat. Thermogenesis is weak at thebisexual stage, and virtually undetectable at immature or malestages (Ito-Inaba et al. 2009b).

To date, SrAOX and two SrPUMPs (SrPUMPa and Sr-PUMPb) have been identified in thermogenic spadix mito-chondria of skunk cabbage (S. renifolius) (Onda et al. 2007;Ito-Inaba et al. 2008b). SrPUMPa is a typical 6-transmembranePUMP whereas SrPUMPb is an atypical 5-transmembraneSrPUMP (Ito et al. 2006; Vercesi et al. 2006; Ito-Inaba et al.2008a). The Ito-Inaba group found that SrPUMPa mRNAis constitutively expressed in various tissues irrespective ofthermogenic stage. However, using quantitative immunoblotanalysis, they found that significant accumulation of SrPUMPaprotein is only observed in the thermogenic tissue or stage(Ito-Inaba et al. 2008b). On the other hand, both gene andprotein expression of SrAOX increased specifically in thethermogenic spadix, suggesting that the specific co-expressionof SrPUMPa and SrAOX protein in the thermogenic tissue mayplay a role in thermogenesis of skunk cabbage (Ito-Inaba et al.2008b). However, these data are inconsistent with an earlyreport that SrPUMPb is a novel thermogenic factor in skunkcabbage (Ito 1999). Onda et al. (2008) also suggested thattranscripts of SrPUMPb and SrAox were co-expressed in thestamens of skunk cabbage. These authors concluded that themajor PUMP in spadix mitochondria is SrPUMPb, based onits electrophoretic mobility without appropriate controls. Theirresults indicated that SrPUMPb and SrAOX were involved intissue-specific thermoregulation in skunk cabbage (Ito 1999;Onda et al. 2008). However, mass spectrometric analysisidentified that SrPUMPa, not SrPUMPb is the major PUMP inskunk cabbage (Ito-Inaba et al. 2008a). Hence, thermogenesisis less likely to result from the presence of an atypical geneproduct of SrPUMPb. SrPUMPb may be a pseudogene or asplicing variant of SrPUMPa transcript.

Skunk cabbage is divided into thermogenic and non-thermogenic skunk cabbage (Symplocarpus renifolius andLysichiton camtschatcensis) (Ito-Inaba et al. 2009b). Althougha close relationship between S. renifolius and L. camtschat-censis has been proposed from morphological analyses (Mayoet al. 1997) and by phylogenetic analysis of chloroplast DNA(Nie et al. 2006), only S. renifolius displays thermogenic andthermoregulatory features. The critical factor of thermogenesis

has been studied in depth in S. renifolius and L. camtschat-censis (Ito-Inaba et al. 2009b). AOX and PUMP mRNAs inL. camtschatcensis were constitutively expressed in spadix,spathe, stalk, and leaves (Ito-Inaba et al. 2009b). Previousstudy showed that SrAOX mRNA was expressed specificallyin the thermogenic spadix, while SrPUMPa mRNA was consti-tutively expressed in various tissues (Ito-Inaba et al. 2008b).Total protein profile of mitochondria in S. renifolius was similarto that in L. camtschatcensis. However, the levels of AOX andPUMP were drastically different between S. renifolius and L.camtschatcensis. The signal intensity of AOX was significantlyhigher in S. renifolius, while the accumulation of PUMP wasmuch lower in S. renifolius relative to L. camtschatcensis. L.camtschatcensis does not exhibit tissue-specific expression ofthe LcAOX gene. This might be associated with the lack ofthermogenesis in L. camtschatcensis (Ito-Inaba et al. 2009b).These results suggest that AOX plays an important role inthermogenesis in S. renifolius, and that the contribution ofPUMP in thermogenesis in this species might be less significant(Ito-Inaba et al. 2009b).

The SrAOX exists as either a reduced or an oxidized dimmerin a reversible manner in vitro via the formation of disulfidebond; it exists as a non-covalently associated dimmer in thespadix of S. renifolius (Onda et al. 2007). The SrAOX proteinwas activated by pyruvate during thermoregulation in S. reni-folius (Onda et al. 2007). Conserved cysteinse residues areconsidered to play key roles in pyruvate regulatory systems ofAOX (Kakizaki et al. 2010). Several studies had suggested thatunique primary structures (Ito et al. 2006; Onda et al. 2007) oramino acid substitutions (Crichton et al. 2005; Kakizaki et al.2010) might be important for plant thermogenesis. However,according to the study conducted by Grant et al. (2009), there isno-specific AOX sequence associated with thermogenic activityin plants; rather, the amount of AOX synthesized may playkey roles in generating heat. In addition, another study byIto-Inaba et al. (2009b) suggests that mitochondrial density,respiratory activity and AOX expression, rather than the primarystructure of AOX or PUMP proteins may be more critical in plantthermogenesis.

Regulation of AOX and PUMP in Higher Plants

Although some tissues co-express PUMPs and AOXs, themechanisms underlying the regulation of these two proteinsare different. Little is known about the factors that affectedthe transcriptional regulation of AOXs and PUMPs as wellas the differential regulation of the multi-gene family mem-bers in organ/cell-type. Several reports described the post-translational regulation (Borecky and Vercesi 2005), i.e., redoxstate of ubiquinone pool, reactive oxygen species (ROS), andfree fatty acids (FFA). The redox state of ubiquinone poolregulates the redox state of AOX via the disulfide bond, which

Energy Dissipation Systems in Thermogenesis of Plants 11

modulates AOX activity (Dry et al. 1989) and represents aregulator of PUMP under phosphorylating respiration condi-tions (Navet et al. 2005). AOX activity also depends on intra-mitochondrial pyruvate and the redox state of the mitochondrialmatrix (Millar et al. 1993), while PUMP activity is inhibitedby non-mitochondrial purine nucleotides. Free fatty acid couldactivate PUMP with simultaneous inhibition of AOX. With theFFA concentration increased in flowering, PUMP and AOXwould start working at appropriate rates in plant cells. Thusthey would never work together at their maximal activities(Sluse et al. 1998; Ito and Seymour 2005). Post-translationalregulation of AOX and PUMP might be crucial in determiningtheir function in plant metabolism.

In conclusion, these findings suggest that members of theAOX and PUMP energy-dissipating system are subject todifferent tissue/organ transcriptional regulation. The capacitiesof AOX and PUMP rely on the enabled factors in mitochondrialmatrix, and AOX and PUMP have developmental stage-specificregulation in plants. Each AOX as well as PUMP may have adifferent physiological role in the process of plant metabolism.Although the two energy-dissipating systems are energeticallywasteful, they could help to maintain normal levels of metabo-lites in plants. The combined actions of multiple AOXs andPUMPs should make plant mitochondria more flexible andenable the cell to more precisely control its response to thermo-genesis. However, the precise interactions between AOX andPUMP in thermogenesis of higher plants are still unclear. Theinteractions between AOX and PUMP are indispensable to thefunction of mitochondrial function, and are ultimately beneficialfor plant survival. Thus, further studies of genetic properties andcorresponding functional interactions in various plant speciesare necessary to elucidate the true physiological roles of theisoforms of these proteins.

Acknowledgements

We would like to thank Dr Jiangqi Wen for his critical read-ing of the manuscript. This study was supported by the Na-tional Natural Science Foundation of China (31071335 and30670070).

Received 2 Sept. 2010 Accepted 28 Oct. 2010

References

Aken OV, Giraud E, Clifton R, Whelan J (2009) Alternative oxidase: a

target and regulator of stress responses. Physiol. Plant. 137, 354–

361.

Albre J, Quikichini A, Gibernau M (2003) Pollination ecology of Arum

Italicum(Araceae). Bot. J. Linn. Soc. 141, 205–214.

Barabe D, Gibernau M, Forest F (2002) Zonal thermogenetic dynam-

ics of two species of Philodendron from two different subgenera

(Araceae). Bot. J. Linn. Soc. 139, 79–86.

Bermadinger-Stabentheiner E, Stabentheiner A (1995) Dynamics of

thermogenesis and structure of epidermal tissues in inflorescences

of Arum maculatum. New Phytol. 131, 41–50.

Borecky J, Maia IG, Arruda P (2001) Mitochondrial uncoupling pro-

teins in mammals and plants. Biosci. Rep. 21, 201–211.

Borecky J, Vercesi AE (2005) Plant uncoupling mitochondrial protein

and alternative oxidase: energy metabolism and stress. Biosci. Rep.

35, 271–286.

Cabrera LI, Salazar GA, Chase MW, Mayo SJ, Bogner J, Davila

P (2008) Phylogenetic relationships of aroids and duckweeds

(Araceae) inferred from coding and noncoding plastid DNA. Am.

J. Bot. 95, 1153–1165.

Considine MJ, Daley DO, Whelan J (2001) The expression of alterna-

tive oxidase and uncoupling protein during fruit ripening in mango.

Plant Physiol. 126, 1619–1629.

Crichton PG, Affourtit C, Albury MS, Carre JE, Moore AL (2005)

Constitutive activity of Sauromatum guttatum alternative oxidase

in Schizosaccharomyces pombe implicates residues in addition to

conserved cysteines in α-keto acid activation. FEBS Lett. 579, 331–

336.

Dry IB, Moore AL, Day DA, Wiskich JT (1989) Regulation of alter-

native pathway activity in plant mitochondria: nonlinear relationship

between electron flux and the redox poise of the quinine pool. Arch.

Biochem. Biophy. 273, 148–157.

Elthon TE, Nickels RL, Mcintosh L (1989) Mitochondrial events during

development of Thermogenesis in Sauromatum guttatum (Schott).

Planta 180, 82–89.

Grant NM, Miller RE, Watling JR, Robinson SA (2008) Synchronic-

ity of thermogenic activity, alternative pathway respiratory flux,

AOX protein content, and carbohydrates in receptacle tissues of

sacred lotus during floral development. J. Exp. Bot. 59, 705–

714.

Grant N, Onda Y, Kakizaki Y, Ito K, Watling J, Robinson S (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 K (1999) Isolation of two distinct cold-inducible cDNAs encoding

plant uncoupling proteins from the spadix of skunk cabbage (Sym-

plocarpus foetidus). Plant Sci. 149, 167–173.

Ito-Inaba Y, Hida Y, Inaba T (2009b) What is critical for plant thermo-

genesis? Differences in mitochondrial activity and protein expres-

sion between thermogenic and non-thermogenic skunk cabbages.

Planta 231, 121–130.

Ito-Inaba Y, Hida Y, Mori H, Inaba T (2008a) Molecular identity

of uncoupling proteins in thermogenic skunk cabbage. Plant Cell

Physiol. 49, 1911–1916.

Ito K, Ito T, Onda Y, Uemura M (2004) Temperature-triggered peri-

odical thermogenic oscillations in skunk cabbage (Symplocarpus

foetidus). Plant Cell Physiol. 45, 257–264.

12 Journal of Integrative Plant Biology Vol. 53 No. 1 2011

Ito K, Matsukawa K, Kato Y (2006) Functional analysis of skunk

cabbage SfUCPB, a unique uncoupling protein lacking the fifth

transmembrane domain, in yeast cells. Biochem. Biophys. Res.

Commun. 349, 383–390.

Ito-Inaba Y, Sato M, Masuko H, Hida Y, Toyooka K, Watanabe M,

Inaba T (2009a) Developmental changes and organelle biogenesis

in the reproductive organs of thermogenic skunk cabbage (Symplo-

carpus renifolius). J. Exp. Bot. 60, 3909–3922.

Ito K, Abe Y, Johnston SD, Seymour RS (2003) Ubiquitous expres-

sion of a gene encoding for uncoupling protein isolated from the

thermogenic inflorescence of the dead horse arum Helicodiceros

muscivorus. J. Exp. Bot. 54, 1113–1114.

Ito-Inaba Y, Hida Y, Ichikawa M, Kato Y, Yamashita T (2008b) Char-

acterization of the plant uncoupling protein, SrUCPA, expressed in

spadix mitochondria of the thermogenic skunk cabbage. J. Exp. Bot.

59, 995–1005.

Ito K, Seymour RS (2005) Expression of uncoupling protein and

alternative oxidase depends on lipid or carbohydrate substrates in

thermogenic plants. Biol. Lett.1, 427–430.

Jezek P, Costa ADT, Vercesi AE (1996) Evidence for anion-

translocating plant uncoupling mitochondrial protein in potato mi-

tochondria. J. Biol. Chem. 271, 32743–32748.

Jezek P, Zackova M, Kosarova J, Rodrigues ETS, Madeira VMC,

Vicente JAF (2000) Occurrence of plant-uncoupling mitochondrial

protein (PUMP) in diverse organs and tissues of several plants.

J. Bioenerg. Biomembr. 32, 549–561.

Kakizaki Y, Seymour RS, Ito K (2010) A novel functional element

in the N-terminal region of Arum concinnatum alternative oxidase

is indispensable for catalytic activity of the enzyme in Hela cells.

Biochim. Biophys. Acta 1797, 20–28.

Kamata T, Matsukawa K, Kakizaki Y, Ito K (2009) In vivo redox state

of the ubiquinone pool in the spadices of the thermogenic skunk

cabbage, Symplocarpus renifolius. J. Plant Res. 122, 645–649.

Laloi M, Klein M, Riesmeier JW, Muller-Rober B, Fleury C, Bouil-

laud F, Ricquier D (1997) A plant cold-induced uncoupling protein.

Nature 389, 135–136.

Mayo SJ, Bogner J, Boyce PC (1997) The Genera of Araceae. The

Trustees, Royal Botanic Gardens. Kew, London.

Meesue BJD (1975) Thermogenic respiration in Aroids. Annu. Rev.

Plant Physiol. 26, 117–126.

Millar AH, Wiskich JT, Whelan J, Day DA (1993) Organic acid

activation of the alternative oxidase of plant mitochondria. FEBS

Lett. 329, 259–262.

Møller IM (2001) Plant mitochondria and oxidative stress: electron

transport, NAD(P)H turnover, and metabolism of reactive oxygen

species. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 561–591.

Nagy KA, Odell DK, Seymour RS (1972) Temperature regulation by

the inflorescence of Philodendron. Science 178, 1195–1197.

Navet R, Douette P, Puttine-Marique F, Sluse-Goffart CM, Jar-

muszkiewicz W, Sluse FE (2005) Regulation of uncoupling protein

activity in phosphorylating potato tuber mitochondria. FEBS Lett.

579, 4437–4442.

Nie ZL, Sun H, Li H, Wen J (2006) Intercontinental biogeography of

subfamily Orontioideae (Symplocarpus, Lysichiton, and Orontium)

of Araceae in Eastern Asia and North America. Mol. Phylogenet.

Evol. 40, 155–165.

Onda Y, Kato Y, Abe Y, Ito T, Morohashi M, Ito Y, Ichikawa M,

Matsukawa K, Kakizaki Y, Koiwa H, Ito K (2008) Functional coex-

pression of the mitochondrial alternative oxidase and uncoupling

protein underlies thermoregulation in the thermogenic florets of

skunk cabbage. Plant Physiol. 146, 636–645.

Onda Y, Kato Y, Abe Y, Ito T, Ito-Inaba Y, Morohashi M, Ito Y,

Ichikawa M, Matsukawa K, Ostuka M, Koiwa H, Ito K (2007)

Pyruvate-sensitive AOX exists as a non-covalently associated dim-

mer in the homeothermic spadix of skunk cabbage, Symplocarpus

renifolius. FEBS Lett. 581, 5852–5858.

Plaxton WC, Podesta FE (2006) The functional organization and

control of plant respiration. Crit. Rev. Plant Sci. 25, 159–198.

Rhoads DM, McIntosh L (1992) Salicylic acid regulation of respiration

in higher plants: alternative oxidase expression. Plant Cell 4, 1131–

1139.

Ricquier D, Bouillaud F (2000) The uncoupling protein homologues:

UCP1, UCP2, UCP3, StUCP and AtUCP. Biochem. J. 345, 161–

179.

Seymour RS (2001) Biophysics and physiology of temperature regula-

tion in thermogenic flowers. Biosci. Rep. 21, 223–236.

Seymour RS (2004) Dynamics and precision of thermoregulatory

responses of eastern skunk cabbage Symplocarpus foetidus. Plant

Cell Environ. 27, 1014–1022.

Seymour RS, Bartholomew GA, Barnhart MC (1983) Respiration and

heat production by the inflorescence of Philodendron selloum Koch.

Planta 157, 336–343.

Seymour RS, Gibernau M, Ito K (2003) Thermogenesis and res-

piration of inflorescences of the dead horse arum, Helicodiceros

muscivorous, a pseudo-thermoregulatory aroid associated with fly

pollination. Funct. Ecol. 17, 886–894.

Seymour RS, Gibernau M (2008) Respiration of thermogenic inflores-

cences of Philodendron melinonii: natural pattern and responses to

experimental temperatures. J. Exp. Bot. 59, 1353–1362.

Seymour RS, Ito Y, Onda Y, Ito K (2009) Effects of floral thermo-

genesis on pollen function in Asian skunk cabbage Symplocarpus

renifolius. Biol. Lett. 5, 568–570.

Seymour RS, Schultze-Motel P (1998) Physiological temperature

regulation by flowers of the sacred lotus. Philos. Trans. R. Soc.

Lond. B. Biol. Sci. 353, 935–943.

Seymour RS, 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.

Seymour RS, Terry I, Roemer RB (2004) Respiration and thermogen-

esis by cones of the Australian cycad Macrozamia machinii. Funct.

Ecol. 18, 925–930.

Skubatz H, Nelson TA, Meeuse BJ, Bendich AJ (1991) Heat pro-

duction in the voodoo lily (Sauromatum guttatum) as monitored by

infrared thermography. Plant Physiol. 95, 1084–1088.

Energy Dissipation Systems in Thermogenesis of Plants 13

Skubatz H, Nelson TA, Dong AM, Meeuse BJD, Bendich AJ (1990b)

Infrared thermography of Arum lily inflorescences. Planta 182, 432–

436.

Skubatz H, Williamson PS, Schneider EL, Meeuse BJD (1990a)

Cyanide-insensitive respiration in thermogenic flowers of Victoria

and Nelumbo. J. Exp. Bot. 41, 1335–1339.

Sluse FE, Almeida AM, Jarmuszkiewicz W, Vercesi AE (1998)

Free fatty acids regulate the uncoupling protein and alternative

oxidase activities in plant mitochondria. FEBS Lett. 433, 237–

240.

Tang W (1987) Heat production in cycad cones. Bot. Gaz. 148, 165–

174.

Umbach AL, Gonzalez-Meler MA, Sweet CR, Siedow JN (2002)

Activation of the plant alternative oxidase: insights from site-directed

mutagensis. Biochim. Biophys. Acta 1554, 118–128.

Vercesi AE, Borecky J, Maia I de G, Arruda P, Cuccovia IM,

Chaimovich H (2006) Plant uncoupling mitochondrial proteins.

Annu. Rev. Plant Biol. 57, 383–404.

Vercesi AE, Martins IS, Silva MAP, Leite HMF, Cuccovia IM,

Chaimovich H (1995) PUMPing plants. Nature 375, 24.

Wagner AM, Krab K, Wagner MJ, Moore AL (2008) Regulation of

thermogenesis in flowering Araceae: the role of the alternative

oxidase. Biochim. Biophys. Acta 1777, 993–1000.

Watling JR, Robinson SA, Seymour S (2006) Contribution of the

alternative pathway to respiration during thermogenesis in flowers

of the sacred lotus. Plant Physiol. 140, 1367–1373.

Zhao MG, Liu YG, Zhang LX, Zheng L, Bi YR (2007) Effects of en-

hanced UV-B radiation on the activity and expression of alternative

oxidase in red kidney bean leaves. J. Integr. Plant Biol. 49, 1320–

1326.

(Co-Editor: Lixin Zhang)