Skip to main content
SpringerLink
Log in

Thermal clamping of temperature-regulating flowers reveals the precision and limits of the biochemical regulatory mechanism

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The flowers of several families of seed plants warm themselves when they bloom. In some species, thermogenesis is regulated, increasing the rate of respiration at lower ambient temperature (T a) to maintain a somewhat stable floral temperature (T f). The precision of this regulation is usually measured by plotting T f over T a. However, such measurements are influenced by environmental conditions, including wind speed, humidity, radiation, etc. This study eliminates environmental effects by experimentally ‘clamping’ T f at constant, selected levels and then measuring stabilized respiration rate. Regulating flowers show decreasing respiration with rising T f (Q 10 < 1). Q 10 therefore becomes a measure of the biochemical ‘precision’ of temperature regulation: lower Q 10 values indicate greater sensitivity of respiration to T f and a narrower range of regulated temperatures. At the lower end of the regulated range, respiration is maximal, and further decreases in floral temperature cause heat production to diminish. Below a certain tissue temperature (‘switching temperature’), heat loss always exceeds heat production, so thermoregulation becomes impossible. This study compared three species of thermoregulatory flowers with distinct values of precision and switching temperature. Precision was highest in Nelumbo nucifera (Q 10 = 0.16) moderate in Symplocarpus renifolius (Q 10 = 0.48) and low in Dracunculus vulgaris (Q 10 = 0.74). Switching temperatures were approximately 30, 15 and 20°C, respectively. There were no relationships between precision, switching temperature or maximum respiration rate. High precision reveals a powerful inhibitory mechanism that overwhelms the tendency of temperature to increase respiration. Variability in the shape and position of the respiration–temperature curves must be accounted for in any explanation of the control of respiration in thermoregulatory flowers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

\({\dot{M}}{\textsc{co}}_{2} \) :

Rate of CO2 production

T a :

Ambient temperature

T f :

Floral temperature

T s :

Spadix temperature

T r :

Receptacle temperature

T sw :

Switching temperature (at \({\dot{M}} {\textsc{co}}_{2\max } \))

Q 10 :

Factor for rate change with 10°C temperature increase

References

  • Gelhaye E, Rouhier N, Gérard J, Jolivet Y, Gualberto J, Navrot N, Ohlsson P-I, Wingsle G, Hirasawa M, Knaff DB, Wang H, Dizengremel P, Meyer Y, Jacquot J-P (2004) A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase. Proc Natl Acad Sci USA 101:14545–14550

    Article  CAS  PubMed  Google Scholar 

  • Gibernau M, Macquart D, Przetak G (2004) Pollination in the Genus Arum: a review. Aroideana 27:148–166

    Google Scholar 

  • Grant NM, Miller RE, Watling JR, Robinson SA (2008) Synchronicity 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ito K (2003) Thermoregulation in the spadix of skunk cabbage (Symplocarpus foetidus). Plant Cell Physiol 44(Suppl.):S2

    Google Scholar 

  • Ito T, Ito K (2005) Nonlinear dynamics of homeothermic temperature control in skunk cabbage, Symplocarpus foetidus. Phys Rev E 72:051909

    Article  Google Scholar 

  • Ito K, Ito T, Onda Y, Uemura M (2004) Temperature-triggered periodical thermogenic oscillations in skunk cabbage (Symplocarpus foetidus). Plant Cell Physiol 45:257–264

    Article  CAS  PubMed  Google Scholar 

  • Knutson RM (1974) Heat production and temperature regulation in eastern skunk cabbage. Science 186:746–747

    Article  CAS  PubMed  Google Scholar 

  • Lamprecht I, Seymour RS, Schultze-Motel P (1998) Direct and indirect calorimetry of thermogenic flowers of the sacred lotus, Nelumbo nucifera. Thermochim Acta 309:5–16

    Article  CAS  Google Scholar 

  • Meeuse BJD, Raskin I (1988) Sexual reproduction in the arum lily family, with emphasis on thermogenicity. Sex Plant Reprod 1:3–15

    Article  Google Scholar 

  • Millar AH, Wiskich JT, Whelan J, Day DA (1993) Organic-acid activation of the alternative oxidase of plant-mitochondria. FEBS Lett 329:259–262

    Article  CAS  PubMed  Google Scholar 

  • Moore AL, Siedow JN (1991) The regulation and nature of the cyanide resistant alternative oxidase of plant mitochondria. Biochim Biophys Acta 1059:121–140

    Article  CAS  PubMed  Google Scholar 

  • Nagy KA, Odell DK, Seymour RS (1972) Temperature regulation by the inflorescence of Philodendron. Science 178:1195–1197

    Article  PubMed  Google Scholar 

  • Nie Z-L, 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 Phylogenetics Evol 40:155–165

    Article  CAS  Google Scholar 

  • Onda Y, Kato Y, Abe Y, Ito T, Morohashi M, Ito Y, Ichikawa M, Matsukawa K, Kakizaki Y, Koiwa H, Ito K (2008) Functional coexpression of the mitochondrial alternative oxidase and uncoupling protein underlies thermoregulation in the thermogenic florets of skunk cabbage. Plant Physiol 146:636–645

    Article  CAS  PubMed  Google Scholar 

  • Raskin I, Turner IM, Melander WR (1989) Regulation of heat production in the inflorescence of an Arum lily by endogenous salicylic acid. Proc Natl Acad Sci USA 86:2214–2218

    Article  CAS  PubMed  Google Scholar 

  • Seymour RS (1999) Pattern of respiration by intact inflorescences of the thermogenic arum lily Philodendron selloum. J Exp Bot 50:845–852

    Article  CAS  Google Scholar 

  • Seymour RS (2004) Dynamics and precision of thermoregulatory responses of eastern skunk cabbage Symplocarpus foetidus. Plant Cell Environ 27:1014–1022

    Article  CAS  Google Scholar 

  • Seymour RS, Blaylock AJ (1999) Switching off the heater: influence of ambient temperature on thermoregulation by eastern skunk cabbage Symplocarpus foetidus. J Exp Bot 50:1525–1532

    Article  CAS  Google Scholar 

  • Seymour RS, Gibernau M (2008) Respiration of thermogenic inflorescences of Philodendron melinonii: natural pattern and responses to experimental temperatures. J Exp Bot 59:1353–1362

    Article  CAS  PubMed  Google Scholar 

  • Seymour RS, Schultze-Motel P (1998) Physiological temperature regulation by flowers of the sacred lotus. Phil Trans R Soc Lond B 353:935–943

    Article  Google Scholar 

  • Seymour RS, Schultze-Motel P (1999) Respiration, temperature regulation and energetics of thermogenic inflorescences of the dragon lily Dracunculus vulgaris (Araceae). Proc R Soc Lond B Biol Sci 266:1975–1983

    Article  Google Scholar 

  • Seymour RS, Bartholomew GA, Barnhart MC (1983) Respiration and heat production by the inflorescence of Philodendron selloum Koch. Planta 157:336–343

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Seymour RS, Gibernau M, Ito K (2003) Thermogenesis and respiration of inflorescences of the dead horse arum Helicodiceros muscivorus, a pseudo-thermoregulatory aroid associated with fly pollination. Funct Ecol 17:886–894

    Article  Google Scholar 

  • Seymour RS, Gibernau M, Pirintsos SA (2009a) Thermogenesis of three species of Arum from Crete. Plant Cell Environ 32:1467–1476

    Article  PubMed  Google Scholar 

  • Seymour RS, Ito Y, Onda Y, Ito K (2009b) Effects of floral thermogenesis on pollen function in Asian skunk cabbage Symplocarpus renifolius. Biol Lett 5:568–570

    Article  PubMed  Google Scholar 

  • Thien LB, Azuma H, Kawano S (2000) New perspectives in the pollination biology of basal angiosperms. Int J Plant Sci 161:S225–S235

    Article  Google Scholar 

  • Thien LB, Bernhardt P, Devall MS, Chen ZD, Luo YB, Fan JH, Yuan LC, Williams JH (2009) Pollination biology of basal angiosperms (ANITA grade). Am J Bot 96:166–182

    Article  Google Scholar 

  • Uemura S, Ohkawara K, Kudo G, Wada N, Higashi S (1993) Heat-production and cross-pollination of the Asian skunk cabbage Symplocarpus renifolius (Araceae). Am J Bot 80:635–640

    Article  Google Scholar 

  • Umbach AL, Siedow JN (1993) Covalent and noncovalent dimers of the cyanide-resistant alternative oxidase protein in higher-plant mitochondria and their relationship to enzyme-activity. Plant Physiol 103:845–854

    CAS  PubMed  Google Scholar 

  • Vanlerberghe GC, McIntosh L (1997) Alternative oxidase: from gene to function. Annu Rev Plant Physiol Plant Mol Biol 48:703–734

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Watling JR, Robinson SA, Seymour RS (2006) Contribution of the alternative pathway to respiration during thermogenesis in flowers of the sacred lotus. Plant Physiol 140:1367–1373

    Article  CAS  PubMed  Google Scholar 

  • Yoshikane I, Koichi O (2005) Chromosome numbers of Japanese Symplocarpus (Araceae). J Phytogeogr Taxon 53:203–205

    Google Scholar 

Download references

Acknowledgments

This project was supported by the Australian Research Council (DP 0771854). We appreciate the logistical help of Morio Kato at the Fujine skunk cabbage park, Stergios Pirintsos of the University of Crete and staff at the Adelaide Botanic Garden. Doug Butler constructed the temperature control circuits. Ingolf Lamprecht, Casey Mueller and Robin Seymour assisted in the field.

Author information

Authors and Affiliations

  1. Ecology and Evolutionary Biology, University of Adelaide, Adelaide, SA, 5005, Australia

    Roger S. Seymour & Gemma Lindshau

  2. Cryobiofrontier Research Center, Faculty of Agriculture, Iwate University, Ueda, Morioka, Iwate, 020-8550, Japan

    Kikukatsu Ito

Authors
  1. Roger S. Seymour
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gemma Lindshau
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kikukatsu Ito
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Roger S. Seymour.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Seymour, R.S., Lindshau, G. & Ito, K. Thermal clamping of temperature-regulating flowers reveals the precision and limits of the biochemical regulatory mechanism. Planta 231, 1291–1300 (2010). https://doi.org/10.1007/s00425-010-1128-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-010-1128-7

Keywords

Search

Navigation