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

Exogenous induction of thermogenesis in Arum concinnatum by salicylic acid

Danae Laina A , Ioanna Oikonomou A , Konstantina Koutroumpa A B , Michael Bariotakis A , Kiriakos Kotzabasis A , Kikukatsu Ito D , Roger S. Seymour E and Stergios A. Pirintsos orcid.org/0000-0002-6287-0795 A C F
+ Author Affiliations
- Author Affiliations

A Department of Biology, University of Crete, PO Box 2208, 71409, Heraklion, Greece.

B Department of Systematic and Evolutionary Botany, University of Zürich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland.

C Botanical Garden, University of Crete, Gallos Campus, Rethymnon 74100, Greece.

D Agri-Innovation Research Center, Iwate University, 3-18-8 Ueda, Morioka, Iwate 020-8550, Japan.

E School of Biological Sciences, University of Adelaide, Adelaide, SA 5005, Australia.

F Corresponding author. Email: pirintsos@biology.uoc.gr

Functional Plant Biology 45(12) 1195-1204 https://doi.org/10.1071/FP17247
Submitted: 29 August 2017  Accepted: 14 June 2018   Published: 9 August 2018

Abstract

Arum concinnatum Schott is a highly thermogenic species, with the temperature of the appendix exceeding ~10.9°C above the ambient temperature during thermogenesis, whereas the rates of respiration of the male florets in intact inflorescences peak at 0.92 μmol s–1 g–1, which is the highest rate so far measured among the plants. Here, we attempt the ex situ exogenous induction of thermogenesis in whole inflorescences and in separate appendices of the spadix, and explore the thermogenic patterns under controlled laboratory conditions of light and temperature. Mature but unopened inflorescences and appendices showed thermogenic responses when treated with salicylic acid (SA), but not when treated with distilled water (control). With regard to light conditions, the responses revealed only one significant difference for inflorescences, which concerns the higher maximum temperature in the continuous light treatment compared with continuous dark. Along the ambient temperature gradient, at the lowest temperature edge individuals remained stable close to ambient temperature and to control. These findings suggest that, in general, ex situ exogenous induction of thermogenesis can be achieved in whole inflorescences and in separate appendices of spadix of A. concinnatum using SA. This study also indicates that SA acts independently of light conditions, while exogenous induction of thermogenesis takes place within an ambient temperature range.

Additional keywords: appendix, biophysics, light/dark photoperiod, switching temperature, tolerance range, whole inflorescence.


References

Albre J, Quilichini A, Gibernau M (2003) Pollination ecology of Arum italicum (Araceae). Botanical Journal of the Linnean Society 141, 205–214.
Pollination ecology of Arum italicum (Araceae).Crossref | GoogleScholarGoogle Scholar |

Chartier M, Gibernau M, Renner SS (2014) The evolution of pollinator–plant interaction types in the Araceae. Evolution 68, 1533–1543.
The evolution of pollinator–plant interaction types in the Araceae.Crossref | GoogleScholarGoogle Scholar |

Chen J, Meeuse BJD (1975) Purification and partial characterization of two biologically active compounds from the inflorescence of Sauromatum guttatum Schott (Araceae). Plant & Cell Physiology 16, 1–11.
Purification and partial characterization of two biologically active compounds from the inflorescence of Sauromatum guttatum Schott (Araceae).Crossref | GoogleScholarGoogle Scholar |

Diaz A, Kite GC (2006) Why be a rewarding trap? The evolution of floral rewards in Arum (Araceae), a genus characterized by saprophilous pollination systems. Biological Journal of the Linnean Society. Linnean Society of London 88, 257–268.
Why be a rewarding trap? The evolution of floral rewards in Arum (Araceae), a genus characterized by saprophilous pollination systems.Crossref | GoogleScholarGoogle Scholar |

Espíndola A, Buerki S, Bedalov M, Küpfer P, Alvarez N (2010) New insights into the phylogenetics and biogeography of Arum (Araceae): unravelling its evolutionary history. Botanical Journal of the Linnean Society 163, 14–32.
New insights into the phylogenetics and biogeography of Arum (Araceae): unravelling its evolutionary history.Crossref | GoogleScholarGoogle Scholar |

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

Kite GC, Hetterscheid WLA, Lewis JM, Boyce PC, Ollerton J, Cocklin E, Diaz A, Simmonds MSJ (1998) Inflorescence odours and pollinators of Arum and Amorphophallus (Araceae) In ‘Reproductive biology’. (Eds JS Owens, JP Rudall) pp. 295–315. (Royal Botanic Gardens: Kew, UK)

Krasavina MS (2007) Effect of SA on solute transport in plants. In ‘Salicylic acid: a plant hormone’. (Eds S Hayat, B Ali, A Ahmad) pp. 25–68. (Springer: Dordrecht, The Netherlands)

Maxwell DP, Nickels R, McIntosh L (2002) Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence. The Plant Journal 29, 269–279.
Evidence of mitochondrial involvement in the transduction of signals required for the induction of genes associated with pathogen attack and senescence.Crossref | GoogleScholarGoogle Scholar |

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

Méndez M (1999) Effects of sexual reproduction on growth and vegetative propagation in the perennial geophyte Arum italicum (Araceae). Plant Biology 1, 115–120.
Effects of sexual reproduction on growth and vegetative propagation in the perennial geophyte Arum italicum (Araceae).Crossref | GoogleScholarGoogle Scholar |

Millar AH, Whelan J, Soole KL, Day DA (2011) Organization and regulation of mitochondrial respiration in plants. Annual Review of Plant Biology 62, 79–104.
Organization and regulation of mitochondrial respiration in plants.Crossref | GoogleScholarGoogle Scholar |

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.
The regulation and nature of the cyanide-resistant alternative oxidase of plant mitochondria.Crossref | GoogleScholarGoogle Scholar |

Moore AL, Shiba T, Young L, Harada S, Kita K, Ito K (2013) Unraveling the heater: new insights into the structure of the alternative oxidase. Annual Review of Plant Biology 64, 637–663.
Unraveling the heater: new insights into the structure of the alternative oxidase.Crossref | GoogleScholarGoogle Scholar |

Norman C, Howell KA, Millar AH, Whelan JM, Day DA (2004) Salicylic acid is an uncoupler and inhibitor of mitochondrial electron transport 1. Plant Physiology 134, 492–501.
Salicylic acid is an uncoupler and inhibitor of mitochondrial electron transport 1.Crossref | GoogleScholarGoogle Scholar |

Ohashi Y, Murakami T, Mitsuhara I, Seo S (2004) Rapid down and upward translocation of salicylic acid in tobacco plants. Plant Biotechnology 21, 95–101.

Onda Y, Mochida K, Yoshida T, Sakurai T, Seymour RS, Umekawa Y, Pirintsos SA, Shinozaki K, Ito K (2015) Transcriptome analysis of thermogenic Arum concinnatum reveals the molecular components of floral scent production. Scientific Reports 5, 8753
Transcriptome analysis of thermogenic Arum concinnatum reveals the molecular components of floral scent production.Crossref | GoogleScholarGoogle Scholar |

Raskin I, Ehmann A, Melander WR, Meeuse BJD (1987) Salicylic acid: a natural inducer of heat production in arum lilies. Science 237, 1601–1602.
Salicylic acid: a natural inducer of heat production in arum lilies.Crossref | GoogleScholarGoogle Scholar |

Raskin I, Turner IM, Melander WR (1989) Regulation of heat production in the inflorescences of an Arum lily by endogenous salicylic acid. Proceedings of the National Academy of Sciences of the United States of America 86, 2214–2218.
Regulation of heat production in the inflorescences of an Arum lily by endogenous salicylic acid.Crossref | GoogleScholarGoogle Scholar |

Raskin I, Skubatzt H, Tangj W, Meeuse BJD (1990) Salicylic acid levels in thermogenic and non-thermogenic plants. Annals of Botany 66, 369–373.
Salicylic acid levels in thermogenic and non-thermogenic plants.Crossref | GoogleScholarGoogle Scholar |

Rhoads DM, McIntosh L (1992) Salicylic acid regulation of respiration in higher plants: alternative oxidase expression. The Plant Cell 4, 1131–1139.
Salicylic acid regulation of respiration in higher plants: alternative oxidase expression.Crossref | GoogleScholarGoogle Scholar |

Rivas-San Vicente M, Plasencia J (2011) Salicylic acid beyond defence: its role in plant growth and development. Journal of Experimental Botany 62, 3321–3338.
Salicylic acid beyond defence: its role in plant growth and development.Crossref | GoogleScholarGoogle Scholar |

Seymour RS (2010) Scaling of heat production by thermogenic flowers: limits to floral size and maximum rate of respiration. Plant, Cell & Environment 33, 1474–1485.

Seymour RS, Blaylock AJ (1999) Switching off the heater: influence of ambient temperature on thermoregulation by eastern skunk cabbage Symplocarpus foetidus. Journal of Experimental Botany 50, 1525–1532.
Switching off the heater: influence of ambient temperature on thermoregulation by eastern skunk cabbage Symplocarpus foetidus.Crossref | GoogleScholarGoogle Scholar |

Seymour RS, Gibernau M, Ito K (2003a) Thermogenesis and respiration of inflorescences of the dead horse arum Helicodiceros muscivorus, a pseudo‐thermoregulatory aroid associated with fly pollination. Functional Ecology 17, 886–894.
Thermogenesis and respiration of inflorescences of the dead horse arum Helicodiceros muscivorus, a pseudo‐thermoregulatory aroid associated with fly pollination.Crossref | GoogleScholarGoogle Scholar |

Seymour RS, White CR, Gibernau M (2003b) Environmental biology: heat reward for insect pollinators. Nature 426, 243–244.
Environmental biology: heat reward for insect pollinators.Crossref | GoogleScholarGoogle Scholar |

Seymour RS, Gibernau M, Pirintsos SA (2009) Thermogenesis of three species of Arum from Crete. Plant, Cell & Environment 32, 1467–1476.
Thermogenesis of three species of Arum from Crete.Crossref | GoogleScholarGoogle Scholar |

Urru I, Stökl J, Linz J, Krügel T, Stensmyr MC, Hansson BS (2010) Pollination strategies in Cretan Arum lilies. Biological Journal of the Linnean Society. Linnean Society of London 101, 991–1001.
Pollination strategies in Cretan Arum lilies.Crossref | GoogleScholarGoogle Scholar |

van Herk AWH (1937) Die chemischen Vorgange im Sauromatum-Kolben. Recueil des Travaux Botaniques Néerlandais 34, 69–156.

Wagner AM, Krab K, Wagner MJ, Moore AL (2008) Regulation of thermogenesis in flowering Araceae: the role of the alternative oxidase. Biochimica et Biophysica Acta 1777, 993–1000.
Regulation of thermogenesis in flowering Araceae: the role of the alternative oxidase.Crossref | GoogleScholarGoogle Scholar |

Xie Z, Chen Z (1999) Salicylic acid induces rapid inhibition of mitochondrial electron transport and oxidative phosphorylation in tobacco cells. Plant Physiology 120, 217–225.
Salicylic acid induces rapid inhibition of mitochondrial electron transport and oxidative phosphorylation in tobacco cells.Crossref | GoogleScholarGoogle Scholar |

Yusuf M, Hayat S, Alyemeni MN (2013) Salicylic acid: physiological roles in plants In ‘Salicylic acid – plant growth and development’. (Eds S Hayat, A Ahmad, MN Alyemeni) pp. 15–30. (Springer Science and Business Media: Dordrecht, The Netherlands)