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Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Thermogenesis and developmental progression of Macrozamia macleayi pollen cones

R. B. Roemer A D , D. Booth B , L. I. Terry C and G. H. Walter B
+ Author Affiliations
- Author Affiliations

A University of Utah, Department of Mechanical Engineering, 1495 E 100 S, Salt Lake City, UT 84112, USA.

B The University of Queensland, School of Biological Sciences, Brisbane, Qld 4072, AUS.

C University of Utah, Department of Biology, South Biology Building, 257 S 1400 E, Salt Lake City, UT 84112, USA.

D Corresponding author. Email: bob.roemer@utah.edu

Australian Journal of Botany 65(5) 421-430 https://doi.org/10.1071/BT17048
Submitted: 22 March 2017  Accepted: 18 June 2017   Published: 25 July 2017

Abstract

Macrozamia macleayi Miq. (family Zamiaceae) pollen cones generate high thermogenic temperatures that are crucial to pollination of these dioecious plants. However, cone thermal behaviour has not been characterised with respect to developmental stage, so any links with the progression and development of their pollination processes remain unclear. Here we show that after growing to full girth, cones progress through thermally active stages of slow/no growth, rapid lengthening, dehiscence and early post-dehiscence, each with a distinct thermal response. During slow/no growth cones exhibit a small late afternoon peak thermogenic temperature elevation above peak ambient, and remain elevated overnight. During rapid lengthening the late afternoon/night-time temperature elevations disappear, and mid-day thermogenesis commences. During dehiscence the midday cone temperature elevations become large, approaching 10°C near the day of maximum dehiscence rate, and then decrease daily. Pollen cones generate their large, dehiscence stage thermogenic temperature elevations synchronously with the diel ambient temperature peak, thus maximising the peak cone temperature. This likely enhances the expulsion of their pollen bearing obligate mutualist thrips pollinator, thus boosting pollination rates. Thermogenic events are fuelled by carbohydrates only, and significantly increase the pollen cone water loss – yet the percentage of water in sporophylls remains nearly constant (~63%) throughout all developmental stages. Similar coordinated pollen cone developmental stage and thermogenic responses are also present in Cycas micronesica K.D. Hill (family Cycadaceae), suggesting a conserved physiological response across cycad families.

Additional keywords: carbohydrates, cycads, evaporation, optimization, pollination, respiration, stomata, temperature.


References

Azuma H, Thien LB, Kawano S (1999) Floral scents, leaf volatiles and thermogenic flowers in Magnoliaceae. Plant Species Biology 14, 121–127.
Floral scents, leaf volatiles and thermogenic flowers in Magnoliaceae.Crossref | GoogleScholarGoogle Scholar |

Bartholomew GA, Vleck D, Vleck CM (1981) Instantaneous measurements of oxygen consumption during pre-flight warm-up and post-flight cooling in Sphingid and Saturniid moths. Journal of Experimental Biology 90, 17–32.

Bowe LM, Coat G, dePamphilis CW (2000) Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales’ closest relatives are conifers. Proceedings of the National Academy of Sciences of the United States of America 97, 4092–4097.
Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales’ closest relatives are conifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXislSgtb8%3D&md5=06bb3eba9bab9189d9ae39ee58e5b984CAS |

Chaw SM, Parkinson CL, Cheng Y, Vincent TM, Palmer JD (2000) Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales from conifers. Proceedings of the National Academy of Sciences of the United States of America 97, 4086–4091.
Seed plant phylogeny inferred from all three plant genomes: monophyly of extant gymnosperms and origin of Gnetales from conifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXislSgtb4%3D&md5=93993af6e5a5175176c49ef216420fb7CAS |

Cvetkovska M, Dahal K, Alber NA, Jin C, Cheung M, Vanlerberge GC (2014) Knockdown of mitochondrial alternative oxidase induces the ‘stress state’ of signaling molecule pools in Nicotania tabacum, with implications for stomatal function. New Phytologist 203, 449–461.
Knockdown of mitochondrial alternative oxidase induces the ‘stress state’ of signaling molecule pools in Nicotania tabacum, with implications for stomatal function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVahtLvE&md5=16ccb02632da70414a9869119527cc12CAS |

Donaldson J (2003) ‘Cycads status survey and conservation action plan.’ (International Union for Conservation of Nature: Gland, Switzerland)

Fragnière Y, Bétrisey S, Cardinaux L, Stoffel M, Kozlowski G (2015) Fighting their last stand? A global analysis of the distribution and conservation status of gymnosperms. Journal of Biogeography 42, 809–820.
Fighting their last stand? A global analysis of the distribution and conservation status of gymnosperms.Crossref | GoogleScholarGoogle Scholar |

François P, Despierre N, Siggia E (2012) Adaptive temperature compensation in circadian oscillations. PLoS Computational Biology 8, e1002585
Adaptive temperature compensation in circadian oscillations.Crossref | GoogleScholarGoogle Scholar |

Franks PJ, Drake PL, Froend RH (2007) Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance. Plant, Cell & Environment 30, 19–30.
Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance.Crossref | GoogleScholarGoogle Scholar |

Gibernau M, Barabe D, Moisson M, Trombe A (2005) Physical constraints on temperature difference in some thermogenic aroid inflorescences. Annals of Botany 96, 117–125.
Physical constraints on temperature difference in some thermogenic aroid inflorescences.Crossref | GoogleScholarGoogle Scholar |

Incropera F, DeWitt D (1996) ‘Fundamentals of heat and mass transfer.’ (John Wiley: New York)

Lamprecht I, Seymour RS, Schultze-Motel P (1998) Direct and indirect calorimetry of thermogenic flowers of the sacred lotus, Nelumbo nucifera. Thermochimica Acta 309, 5–16.
Direct and indirect calorimetry of thermogenic flowers of the sacred lotus, Nelumbo nucifera.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtFyntLY%3D&md5=a58b77521cf0a5faa88372ea901461bdCAS |

Lighton J (2008) ‘Measuring metabolic rates: a manual for scientists.’ (Oxford University Press: Oxford, UK)

Marler T, Dongol N (2011) Models to describe Cycas micronsesica leaf and stroboli development. HortScience 46, 1333–1337.

McLean JA, Watts PH (1976) Analytical refinements in animal calorimetry. Journal of Applied Physiology 40, 827–831.

Niinemets U, Hauff K, Bertin N, Tenhunen JD, Steinbrecher R, Seufert G (2002) Monoterpene emissions in relation to foliar photosynthetic and structural variables in Mediterranean evergeen Quercus species. New Phytologist 153, 243–256.
Monoterpene emissions in relation to foliar photosynthetic and structural variables in Mediterranean evergeen Quercus species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitVSnt7k%3D&md5=82354405f129189beb593b49f27414b6CAS |

Nobel PS (2005) ‘Physicochemical and environmental plant physiology.’ (Elsevier Academic Press: Amsterdam)

Norstog KJ, Nicholls TJ (1997) ‘The biology of the cycads.’ (Cornell University Press: Ithaca, NY, USA)

Patino S, Aalto T, Edwards AA, Grace J (2002) Is Rafflesia an endothermic flower? New Phytologist 154, 429–437.
Is Rafflesia an endothermic flower?Crossref | GoogleScholarGoogle Scholar |

Roemer R, Terry I, Chockley C, Jacobsen J (2005) Experimental evaluation and thermo-physical analysis of thermogenesis in male and female cycad cones. Oecologia 144, 88–97.
Experimental evaluation and thermo-physical analysis of thermogenesis in male and female cycad cones.Crossref | GoogleScholarGoogle Scholar |

Roemer RB, Terry LI, Walter GH (2008) Unstable, self-limiting thermochemical temperature oscillations in Macrozamia cycads. Plant, Cell & Environment 31, 769–782.
Unstable, self-limiting thermochemical temperature oscillations in Macrozamia cycads.Crossref | GoogleScholarGoogle Scholar |

Roemer RB, Booth D, Bhavsar AA, Walter GH, Terry LI (2012) Mathematical model of cycad cones’ thermogenic temperature responses: inverse calorimetry to estimate metabolic heating rates. Journal of Theoretical Biology 315, 87–96.
Mathematical model of cycad cones’ thermogenic temperature responses: inverse calorimetry to estimate metabolic heating rates.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38boslWksA%3D%3D&md5=4854e6af7ef883da15bfdc44f24b8520CAS |

Roemer RB, Terry LI, Marler TE (2013) Cone thermogenesis and its limits in the tropical Cycas micronesica (Cycadaceae): association with cone growth, dehiscence, and post-dehiscence phases. American Journal of Botany 100, 1981–1990.
Cone thermogenesis and its limits in the tropical Cycas micronesica (Cycadaceae): association with cone growth, dehiscence, and post-dehiscence phases.Crossref | GoogleScholarGoogle Scholar |

Schmidt-Nielsen K (1997) ‘Animal physiology.’ (Cambridge University Press: Cambridge, UK)

Seymour RS (2001) Biophysics and physiology of temperature regulation in thermogenic flowers. Bioscience Reports 21, 223–236.
Biophysics and physiology of temperature regulation in thermogenic flowers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXosVyltbw%3D&md5=ad9b6770ba505b26f679d8953de81628CAS |

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.
Physiological temperature regulation by flowers of the sacred lotus.Crossref | GoogleScholarGoogle 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. 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, Terry I, Roemer RB (2004) Respiration and thermogenesis by cones of the Australian cycad Macrozamia machinii. Functional Ecology 18, 925–930.
Respiration and thermogenesis by cones of the Australian cycad Macrozamia machinii.Crossref | GoogleScholarGoogle Scholar |

Skubatz H, Tang W, Mueese B (1993) Oscillatory heat-production in the male cones of cycads. Journal of Experimental Botany 44, 489–492.
Oscillatory heat-production in the male cones of cycads.Crossref | GoogleScholarGoogle Scholar |

Suinyuy TN, Donaldson JS, Johnson SD (2013) Patterns of odour emission, thermogenesis and pollinator activity in cones of an African cycad: what mechanisms apply? Annals of Botany 112, 891–902.
Patterns of odour emission, thermogenesis and pollinator activity in cones of an African cycad: what mechanisms apply?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlGms7jK&md5=99764af7e1c65cd67835e353aaf2e3baCAS |

Takacs S, Bottomley H, Andreller I, Zaradnik T, Schwarz J, Bennett R, Strong W, Gries G (2009) Infrared radiation from hot cones on cool conifers attracts seed-feeding insects. Proceedings of Royal Society B Biological Science 276, 649–655.
Infrared radiation from hot cones on cool conifers attracts seed-feeding insects.Crossref | GoogleScholarGoogle Scholar |

Tang W (1987) Heat production in cycad cones. Botanical Gazette 148, 165–174.
Heat production in cycad cones.Crossref | GoogleScholarGoogle Scholar |

Tang W, Sternberg L, Price D (1987) Metabolic aspects of thermogenesis in male cones of five cycad species. American Journal of Botany 74, 1555–1559.
Metabolic aspects of thermogenesis in male cones of five cycad species.Crossref | GoogleScholarGoogle Scholar |

Terry I (2001) Thrips and weevils as dual, specialist pollinators of the Australian cycad Macrozamia communis (Zamiaceae). International Journal of Plant Sciences 162, 1293–1305.
Thrips and weevils as dual, specialist pollinators of the Australian cycad Macrozamia communis (Zamiaceae).Crossref | GoogleScholarGoogle Scholar |

Terry I, Moore CJ, Walter GH, Forster PI, Roemer RB, Donaldson JD, Machin PJ (2004) Association of cone thermogenesis and volatiles with pollinator specificity in Macrozamia cycads. Plant Systematics and Evolution 243, 233–247.
Association of cone thermogenesis and volatiles with pollinator specificity in Macrozamia cycads.Crossref | GoogleScholarGoogle Scholar |

Terry LI, Walter GH, Donaldson JS, Snow E, Forster PI, Machin PJ (2005) Pollination of Australian Macrozamia cycads (Zamiaceae): effectiveness and behavior of specialist vectors in a dependent mutualism. American Journal of Botany 92, 931–940.
Pollination of Australian Macrozamia cycads (Zamiaceae): effectiveness and behavior of specialist vectors in a dependent mutualism.Crossref | GoogleScholarGoogle Scholar |

Terry I, Walter GH, Moore C, Roemer R, Hull C (2007) Odor-mediated push-pull pollination in cycads. Science 318, 70
Odor-mediated push-pull pollination in cycads.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFWitLfF&md5=998dafff8957d2f54efd95cf6336f18eCAS |

Terry I, Forster PI, Moore CJ, Roemer RB, Machin PJ (2008) Demographics, pollination syndrome and conservation status of Macrozamia platyrhachis (Zamiaceae), a geographically restricted Queensland cycad. Australian Journal of Botany 56, 321–332.
Demographics, pollination syndrome and conservation status of Macrozamia platyrhachis (Zamiaceae), a geographically restricted Queensland cycad.Crossref | GoogleScholarGoogle Scholar |

Terry LI, Roemer RB, Walter GH, Booth D (2014) Thrips’ responses to thermogenic associated signals in a cycad pollination system: the interplay of temperature, light, humidity and cone volatiles. Functional Ecology 28, 857–867.
Thrips’ responses to thermogenic associated signals in a cycad pollination system: the interplay of temperature, light, humidity and cone volatiles.Crossref | GoogleScholarGoogle Scholar |

Terry LI, Roemer RB, Booth DT, Moore CJ, Walter GH (2016) Thermogenic respiratory processes drive the exponential increase of volatile organic compound emissions in Macrozamia cycad cones. Plant, Cell & Environment 39, 1588–1600.
Thermogenic respiratory processes drive the exponential increase of volatile organic compound emissions in Macrozamia cycad cones.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XpsFejsrs%3D&md5=cca2343b6ccafd4a348e24c984b03e2cCAS |

Wallenius T, Peakall R, Wanjura W, Chyb S, Oberprieler R (2012) Volatile emissions, thermogenesis, and dehiscence patterns of Macrozamia communis (Zamiaceae): Implications for cycad pollination research. Memoirs of the New York Botanical Garden 106, 395–418.