Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Distribution of thermogenic activity in floral tissues of Nelumbo nucifera

Nicole M. Grant A B , Rebecca A. Miller A B C , Jennifer R. Watling B and Sharon A. Robinson A D
+ Author Affiliations
- Author Affiliations

A Institute for Conservation Biology, University of Wollongong, Wollongong, NSW 2522, Australia.

B School of Earth and Environmental Sciences, University of Adelaide, Adelaide, SA 5005, Australia.

C Present address: School of Biological Sciences, Monash University, Clayton, Vic. 3800, Australia.

D Corresponding author. Email: sharonr@uow.edu.au

Functional Plant Biology 37(11) 1085-1095 https://doi.org/10.1071/FP10024
Submitted: 5 February 2010  Accepted: 9 August 2010   Published: 22 October 2010

Abstract

Thermogenesis in Nelumbo nucifera (Gaertn.) has been known to scientists for many years; however, the extent of heating by different floral parts remains unclear. We present evidence that the receptacle, stamens and petals produce heat independently, and that the source of heating in these tissues is most likely the alternative oxidase (AOX). The temperatures of the receptacle, petals and stamens were significantly higher than non-thermogenic leaf tissue. After removal from the pedicel, the receptacle retained the most heat (8.1 ± 1.9°C above non-thermogenic tissue temperature) and the petals the least (2.8 ± 4.2°C), with the stamens intermediate. High AOX protein levels and flux through the AOX pathway (in all tissues) during the thermogenic period are consistent with AOX being the mechanism used for thermogenesis. Lipids and carbohydrates were investigated as possible substrates for thermogenesis. There was little change in total lipids during floral development; however, soluble carbohydrate levels decreased by 70% with the onset of thermogenesis. These sugars may fuel thermogenesis in the stamens. The localisation of AOX protein in the various floral parts and the evolutionary significance of its heating role are discussed.

Additional keywords: alternative oxidase, alternative pathway respiration, lipid, plant thermogenesis, sacred lotus, starch.


Acknowledgements

We thank the Adelaide Botanical Gardens for the use of their lotus pond. We also thank Professor Kikukatsu Ito and Dr Yoshi Onda for advice and useful suggestions, David Bruce for technical advice, and Andrew Netherwood and David Hollingworth for photography and image production assistance. Antibodies were kindly donated by Professor James Whelan (University of Western Australia, Perth, Australia), Professor Murray Badger (Australian National University, Canberra, Australia) and Professor Kikukatsu Ito (Iwate University, Morioka, Japan). This work was supported by the Australian Research Council (grant no. DP0451617) and NMG received an APA studentship. The thermal imaging camera was purchased using funding from the University of Wollongong Research Infrastructure Block Grant. We would also like to thank two anonymous reviewers for helpful comments.


References


ap Rees T, Wright BW, Fuller WA (1977) Measurements of starch breakdown as estimates of glycolysis during thermogenesis by the spadix of Arum maculatum L. Planta 134, 53–56.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Breidenbach RW, Saxton MJ, Hansen LD, Criddle RS (1997) Heat generation and dissipation in plants: can the alternative oxidative phosphorylation pathway serve a thermoregulatory role in plant tissues other than specialized organs? Plant Physiology 114, 1137–1140.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Clement C, Burrus M, Audran JC (1996) Floral organ growth and carbohydrate content during pollen development in Lilium. American Journal of Botany 83, 459–469.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Considine MJ, Daley DO, Whelan J (2001) The expression of alternate oxidase and uncoupling protein during fruit ripening in mango. Plant Physiology 126, 1619–1629.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Crombie WM (1958) Fatty acids in chloroplasts and leaves. Journal of Experimental Botany 9, 254–261.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Dickinson DB (1965) Germination of lily pollen: respiration and tube growth. Science 150, 1818–1819.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Dieringer G, Cabrera LR, Lara M, Loya L, Reyes-Castillo P (1999) Beetle pollination and floral thermogenicity in Magnolia tamaulipana (Magnoliaceae). International Journal of Plant Sciences 160, 64–71.
Crossref | GoogleScholarGoogle Scholar | open url image1

Elthon TE, Nickels RL, McIntosh L (1989) Monoclonal antibodies to the alternative oxidase of higher plant mitochondria. Plant Physiology 89, 1311–1317.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Florez-Sarasa ID, Ostaszewska M, Galle A, Flexas J, Rychter AM, Ribas-Carbo M (2009) Changes of alternative oxidase activity, capacity and protein content in leaves of Cucumis sativus wild-type and MSC16 mutant grown under different light intensities. Physiologia Plantarum 137, 419–426.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Folch J, Lees M, Sloane-Stanley G (1957) A simple method for the isolation and purification of total lipids from animal tissue. The Journal of Biological Chemistry 226, 497–509.
CAS | PubMed |
open url image1

Galen C, Stanton ML (2003) Sunny-side up: flower heliotropism as a source of parental environmental effects on pollen quality and performance in the snow buttercup, Ranunculus adoneus (Ranunculaceae). American Journal of Botany 90, 724–729.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gonzàlez-Meler MA, Blanc-Betes E, Flower CE, Ward JK, Gomez-Casanovas N (2009) Plastic and adaptive responses of plant respiration to changes in atmospheric CO2 concentration. Physiologia Plantarum 137, 473–484.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Grant NM (2010) ‘Thermogenesis in plants: the mode of heating and regulation in hot flowers.’ PhD Thesis, School of Biological Sciences, University of Wollongong.

Grant NM, Miller RE, Watling JR, Robinson SA (2008) Synchronicity of the thermogenic activity, alternative pathway respiratory flux, AOX protein content, and carbohydrates in receptacle tissues of sacred lotus during floral development. Journal of Experimental Botany 59, 705–714.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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 Physiology 150, 987–995.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Ito K (1999) Isolation of two distinct cold-inducible cDNAs encoding plant uncoupling proteins from the spadix of skunk cabbage (Symplocarpus foetidus). Plant Science 149, 167–173.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Jezek P, Costa ADT, Vercesi AE (1996) Evidence for anion-translocating plant uncoupling mitochondrial protein in potato mitochondria. The Journal of Biological Chemistry 271, 32 743–32 748.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Knutson RM (1974) Heat production and temperature regulation in eastern skunk cabbage. Science 186, 746–747.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Lepage G, Roy CC (1986) Direct transesterification of all classes of lipids in a one-step reaction. Journal of Lipid Research 27, 114–120.
CAS | PubMed |
open url image1

Li JK, Huang SQ (2009) Flower thermoregulation facilitates fertilization in Asian sacred lotus. Annals of Botany 103, 1159–1163.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

McDonald AE (2008) Alternative oxidase: an inter-kingdom perspective on the function and regulation of this broadly distributed ‘cyanide-resistant’ terminal oxidase. Functional Plant Biology 35, 535–552.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Meeuse BJD, Raskin I (1988) Sexual reproduction in the arum lily family, with emphasis on thermogenicity. Sexual Plant Reproduction 1, 3–15.
Crossref | GoogleScholarGoogle Scholar | open url image1

Miller RE, Watling JR, Robinson SA (2009) Functional transition in the floral receptacle of the sacred lotus (Nelumbo nucifera): from thermogenesis to photosynthesis. Functional Plant Biology 36, 471–480.
Crossref | GoogleScholarGoogle Scholar | open url image1

Miyake K (1898) Some physiological observations on Nelumbo nucifera, G. Botanical Magazine Tokyo 12, 112–117. open url image1

Moore AL, Siedow JN (1991) The regulation and nature of the cyanide-resistant alternative oxidase of plant mitochondria. Biochimica et Biophysica Acta 1059, 121–140.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Nagy KA, Odell DK, Seymour RS (1972) Temperature regulation by the inflorescence of Philodendron. Science 178, 1195–1197.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Onda Y, Kato Y, Abe Y, Ito T, Morohashi M , et al . (2008) Functional coexpression of the mitochondrial alternative oxidase and uncoupling protein underlies thermoregulation in the thermogenic florets of skunk cabbage. Plant Physiology 146, 636–645.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Rasmusson AG, Fernie AR, van Dongen JT (2009) Alternative oxidase: a defence against metabolic fluctuations? Physiologia Plantarum 137, 371–382.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Ribas-Carbo M, Berry JA, Yakir D, Giles L, Robinson SA, Lennon AM, Siedow JN (1995) Electron partitioning between the cytochrome and alternative pathways in plant mitochondria. Plant Physiology 109, 829–837.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Ribas-Carbo M , Robinson SA , Giles L (2005) The application of the oxygen-isotope techniques to assess respiratory pathway partitioning. In ‘Plant respiration: from cell to ecosystem. Advances in photosynthesis and respiration’. (Eds H Lambers, M Ribas-Carbo) pp. 31–42. (Springer: Dordrecht)

Robinson SA, Yakir D, Ribas-Carbo M, Giles L, Osmond CB, Siedow JN, Berry JA (1992) Measurements of the engagement of cyanide-resistant respiration in the Crassulacean acid metabolism plant Kalanchoe daigremontiana with use of online oxygen isotope discrimination. Plant Physiology 100, 1087–1091.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Robinson SA, Ribas-Carbo M, Yakir D, Giles L, Reuveni Y, Berry JA (1995) Beyond SHAM and cyanide – opportunities for studying the alternative oxidase in plant respiration using oxygen-isotope discrimination. Australian Journal of Plant Physiology 22, 487–496.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Schneider EL, Buchanan JD (1980) Morphological studies of the Nymphaeaceae. XI. The floral biology of Nelumbo pentapetala. American Journal of Botany 67, 182–193.
Crossref | GoogleScholarGoogle Scholar | open url image1

Seymour RS, Schultze-Motel P (1996) Thermoregulating lotus flowers. Nature 383, 305.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Seymour RS, Schultze-Motel P (1998) Physiological temperature regulation by flowers of the sacred lotus. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 353, 935–943.
Crossref | GoogleScholarGoogle Scholar | open url image1

Seymour RS, Bartholomew GA, Barnhart MC (1983) Respiration and heat production by the inflorescence of Philodendron selloum Koch. Planta 157, 336–343.
Crossref | GoogleScholarGoogle Scholar | open url image1

Skubatz H, Haider ST (2004) Expression of the alternative oxidase in thermogenic and non-thermogenic reproductive organs. Phyton 44, 83–94. open url image1

Skubatz H, Williamson PS, Schneider EL, Meeuse BJD (1990) Cyanide-insensitive respiration in thermogenic flowers of Victoria and Nelumbo. Journal of Experimental Botany 41, 1335–1339.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Sluse FE, Almeida AM, Jarmuszkiewicz W, Vercesi AE (1998) Free fatty acids regulate the uncoupling protein and alternative oxidase activities in plant mitochondria. FEBS Letters 433, 237–240.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Smith CA, Melino VA, Sweetman C, Soole KL (2009) Manipulation of alternative oxidase can influence salt tolerance in Arabidopsis thaliana. Physiologia Plantarum 137, 459–472.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Thompson AC, Henson RD, Minyard JP, Hedin PA (1968) Fatty acid composition of polar lipids of cotton buds. Lipids 3, 373–374.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Vercesi AE, Martins IS, Silva MAP, Leite A, Cuccovia IM, Chaimovich H (1995) PUMPing plants. Nature 375, 24.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Vogel S, Hadacek F (2004) Contributions to the functional anatomy and biology of Nelumbo nucifera (Nelumbonaceae) III. An ecological reappraisal of floral organs. Plant Systematics and Evolution 249, 173–189.
Crossref | GoogleScholarGoogle Scholar | open url image1

Walker DB, Gysi J, Sternberg L, DeNiro MJ (1983) Direct respiration of lipids during heat production in the inflorescence of Philodendron selloum. Science 220, 419–421.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Watling JR, Robinson SA, Seymour RS (2006) Contribution of the alternative pathway to respiration during thermogenesis in flowers of the sacred lotus, Nelumbo nucifera. Plant Physiology 140, 1367–1373.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Watling JR, Grant NM, Miller RE, Robinson SA (2008) Mechanisms of thermoregulation in plants. Plant Signaling & Behavior 3, 595–597.
PubMed |
open url image1