Heat production by sacred lotus flowers depends on ambient temperature, not light cycle

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1 Jounal of Expeimental Botany, Vol. 49, No. 324, pp , July 1998 Heat poduction by saced lotus flowes depends on ambient tempeatue, not ligt cycle Roge S. Seymou1,3, Paul Scultze-Motel1 and I. Lampect2 1 Depatment of Zoology, Univesity of Adelaide, Adelaide, SA 5005, Austalia 2 Institute fo Biopysics, Fee Univesity of Belin, Tielallee 63, D Belin, Gemany Received 3 Febuay 1998; Accepted 20 Febuay 1998 Abstact Scultze-Motel, 1998), and a quantitative analysis of eat poduction and eat loss as been made, using diect Flowes of te saced lotus, Nelumbo nucifea, mainand indiect caloimety (Lampect et al., 1998). tain eceptacle tempeatue (T ) between about 30 C Temoegulation begins in te bud, wen te petals ae and 36 C duing tei 2 4 d sequence of antesis by tigtly closed, continues toug a day wen te petals inceasing te ate of eat poduction, measued as open sligtly to eveal te stigmas, and ends as te flowe oxygen consumption (V ), at low ambient tempeatue opens widely to expose te stamens. Te patten of (T ) at nigt and educing it at ig T duing te day. a a antesis is potogynous, and te peiod of temoegul- Te effects of T and potopeiod on V wee sepaation ougly coesponds to eceptivity of te capels to a ated by manipulating T aound outdoo flowes unde a pollination. Tee is evidence tat temoegulation natual potopeiod o constant dakness. Tee was migt be a ewad to insect pollinatos tat would benefit no effect of time of day on eite T o V, but bot fom a ig body tempeatue wile emaining in te depended on T. Rising T esulted in an incease in a a flowe (Seymou and Scultze-Motel, 1997). T, a bief upwad spike in V, followed by a long-tem Ealie wok on te lotus in tis laboatoy involved decease in V. Deceasing T ad te opposite a simultaneous measuements of tempeatues and oxygen effects: a decease in T and a bief depession, consumption ates of flowes in an outdoo pond wee followed by a slow ise, in V. Te two-pase espon- ambient conditions wee uncontolled (Seymou and ses to sudden T cange indicate a apid, mass- a Scultze-Motel, 1996, 1998). Temoegulation was demaction effect and a slowe, egulatoy adjustment. onstated by stability of flowe tempeatues duing natu- Tempeatue egulation continued in constant dak- ally occuing cycles of ambient tempeatue. In addition, ness fo ove 3 d. tee was a ecipocal elationsip between ambient tempeatue and oxygen consumption, wic demonstated Key wods: Temoegulation, lotus, potopeiod, tem- tat te ate of eat poduction inceased wit inceased peatue, eat poduction, oxygen consumption, diffeence between ambient and flowe tempeatue. Nelumbonaceae. Altoug tee seemed to be no elationsip between ate of eat poduction and ambient ligt levels, tee Intoduction was a possibility tat eat poduction was patly co-odinated wit te ligt cycle, geneally ising at nigt Flowes of te saced lotus, Nelumbo nucifea Gaetn., and deceasing duing te day. It is well known tat ae stongly temogenic (Miyake, 1898) and temoegu- floweing in some temogenic plants is stongly dependlatoy (Seymou and Scultze-Motel, 1996). Tempea- ent upon ligt cycle. Fo example, te aum lilies, tues inside te flowes geneally emain between C Sauomatum and Aum, do not bloom o poduce eat duing a 2 4 d peiod, despite canges in envionmental in constant ligt o constant dak, but equie cycling of tempeatues between about C. Te elationsips bot to initiate antesis (Meeuse and Raskin, 1988). between ambient tempeatue, flowe tempeatue, and Temogenesis in te aum lily, Pilodendon selloum, espiation ate ave been studied in detail (Seymou and also depends on ligt cycle, usually eacing its peak in 3 To wom coespondence sould be addessed. Fax: seymou@zoology.adelaide.edu.au Oxfod Univesity Pess 1998 Downloaded fom ttps://academic.oup.com/jxb/aticle-abstact/49/324/1213/481115

2 1214 Seymou et al. te ealy evening in Bazil (Gottsbege and Amaal, sealed wit clea plastic cling wap. Altoug tis ood 1984), but in Califonia tee ae two pattens of waming pemitted enty of ligt, a glass-domed solaimete sowed tat total intensity was educed to 45% of outside insolation. of onamental cultivas, bot dependent on time of day Flowe buds wee cosen on te day befoe anticipated (Seymou et al., 1983). Seveal species of Sout Ameican opening and measuements wee made continuously duing te Annona (Gottsbege, 1989) and te Amazon wate lily, temogenic peiod. Expeimental flowes wee exposed to a Victoia amazonica (Pance and Aias, 1975), always evese tempeatue egime. Te wate bat was set at 15 C at appea to wam duing te evening ous wen te about and to 30 C at about Wen possible, ecods fom expeimental flowes in jacketed oods wee pollinating insects become active. compaed to contol flowes in tanslucent oods witout Tis study on Nelumbo was designed to sepaate ligt jackets tat wee measued simultaneously unde te natual and tempeatue as envionmental factos tat possibly tempeatue and ligt egime. affect temogenesis. Because of te limited life of cut flowes in te laboatoy, intact flowes wee studied Results outdoos unde tee conditions: ( 1) natual tempeatue and ligt cycles, (2) evesed tempeatue and constant Duing te nomal floweing sequence in tanslucent dakness, ( 3) evesed tempeatue and natual ligt cycle. oods witout te wate jacket, ood tempeatue (T ) Tempeatues of te flowes and suounding ai wee deceased at nigt and inceased duing te day ( Fig. 1). measued to evaluate temal stability, and ates of Duing te fist two nigts of temoegulation, eceptacle oxygen consumption wee used as indiect measues of tempeatue (T ) tended to emain between C, eat poduction. except tat tee was often a dip in te ealy evening. Te T inceased duing te day, and T tended to be sligtly above it. Oxygen consumption ates (V ) Mateials and metods inceased duing te nigt and deceased duing te day, Nelumbo nucifea was studied in a lage outdoo pond at te Adelaide Botanic Gadens, duing Januay and Febuay, Te saced lotus, Nelumbo nucifea nucifea, and te Ameican lotus, N. n. lutea, ae consideed subspecies by Bosc and Batlott (1996). Te plants and conditions wee te same as peviously descibed (Seymou and Scultze-Motel, 1996, 1998). Measuements of oxygen consumption wee made wit a 4-cannel flow-toug system tat opeated continuously. Biefly, a constant-flow pump dew atmospeic ai toug a ood coveing te flowe, and sent it toug a mass flowmete tat was vented to te atmospee. Subsamples of te flows toug tee oods and one efeence cannel of atmospeic ai wee dawn into a paamagnetic oxygen analyse. Tempeatues, flow ates and oxygen levels wee ecoded at 2 min intevals wit a Gant Squiel data logge, but te complete cycle of fou cannels equied 24 min, because te oxygen analyse dwelt on eac cannel fo 6 min to ensue a stable eading. Computations of oxygen consumption wee standad fo flow-toug espiomety and wee appopiate to te system ( Wites, 1977). Fo te pesent expeiments, te ood ove te flowe was equipped wit a tempeatue-contolled wate jacket, constucted fom a clea, styene, double-walled bucket designed to keep a wine bottle cool (10 cm i.d., 20 cm deep; Deco, Austalia). Te space between te walls was sealed and fitted wit inlet and outlet pots tat povided an even patten of ciculation. Wate was povided by a efigeated wate bat (Julabo model F20-HC; 2550 W ), toug two, 6 m, 1 cm i.d. oses, insulated wit 1 cm tick foam ubbe sleeves. Te ood was inveted ove te flowe and suppoted by wooden stakes diven into te bottom of te pond. Te opening was sealed aound te petiole except fo a small ole tat allowed enty of ai. Temocouples povided tempeatues of te ood inteio Fig. 1. Nomal patten of tempeatue egulation in a saced lotus and te flowe eceptacle. One ood incopoated elements fo flowe unde te natual potopeiod and tempeatue egime. Tempeatues inside te espiomety ood (solid line) and te eceptacle diect caloimety as pat of anote study (Lampect et al., (dased line) and oxygen consumption (dots) ae given in elation to 1998). It was suounded by opaque insulation and its opening time. Nigt (dak bas) is defined as te peiod between local sunset was sealed wit 6 cm tick foam ubbe wic eliminated ligt. and sunise. Tempeatue egulation is appaent at nigt duing te Anote ood was tanslucent and insulated outside by 6 mm fist two cycles, and it disappeas afte te flowe opens widely on te tick polyetylene bubble-pack seeting, and te opening was tid day. Downloaded fom ttps://academic.oup.com/jxb/aticle-abstact/49/324/1213/481115

3 mioing te canges in T, but lagging beind it. Tee was often a peak in V at sunise, wen T and T wee ising apidly because of sola input. Tis patten was evident in tee flowes in te pesent study and 19 flowes studied peviously (Seymou and Scultze- Motel, 1998). Five flowes measued in constant dakness sowed epoducible esponses to enfoced tempeatue canges (Fig. 2). Wen T was aised, T also ose and sowed a sap ovesoot befoe stabilizing nea 34 C. Often coincidental wit te ovesoot was an immediate spike in V befoe it too deceased to a lowe level. Wen T deceased, T also deceased, always sowing a ponounced undesoot befoe ecoveing to tempeatues above 30 C. Te dept and duation of te undesoot toug inceased in olde flowes. Tee was often a small tansient decease in V duing te T undesoot, not always caugt duing te 24 min sampling cycle, but appaent on te tid day in Fig. 2. Ten tee was a gadual ise in V duing te peiod of cold exposue. Heat poduction by te flowe influenced T, as evidenced by te small peak at te onset of te wam pase and instability duing te cold pase. Receptacle tempeatues in fou wate-jacketed flowes on a evese tempeatue cycle also tended to emain between C, except wen T was canging apidly. Figue 3 sows an euistic example, containing an Lotus tempeatue egulation 1215 Fig. 3. Patten of tempeatue egulation of a lotus flowe unde manipulated ood tempeatues and natual potopeiod. Te data wee taken simultaneously wit tose in Fig. 1. Letteed peiods ae discussed in te text. Symbols as in Fig. 1. Fig. 2. Patten of tempeatue egulation of a lotus flowe unde evesed tempeatue cycles and constant dakness. Symbols as in Fig. 1. unplanned petubation. Instuments wee attaced to an unopened bud on te day befoe anticipated opening (a). V was low and falling, simila to te contol flowe tat was measued at te same time (Fig. 1). Exposed quickly to a cold tempeatue, flowe tempeatue dipped to 26 C, esulting in an immediate dip in V to 0.5 ml min 1, followed by inceasing V to 1.0 ml min 1, and ecovey of T to above 30 C. Low V duing tis peiod was associated wit tigtly closed petals tat etained te eat witin te bud. Wen te wate bat was set at 30 C at about 18.00, it poduced a ise in T, biefly ovesooting to 37 C befoe stabilizing at about 34 C tougout te nigt (b). Te ovesoot was immediately coupled wit a bief spike of V to 1.5 ml min 1, followed by stabilization at about 0.8 ml min 1. At about te wate bat was set at 15 C, causing a lage dop in T to about 22 C (c). Again, tee was a dip in V, followed by a steady ise duing te day. At about 15.00, te powe supply to te wate bat failed and T began to ise (d). Tis initially pused up T and deceased V, but in te evening te unegulated T deceased to about 17 C, followed by a decease in T to 30 C. A smoot ise in V to 2.8 ml min 1 and T to 33 C continued toug- out te nigt. In te moning wen powe was estoed Downloaded fom ttps://academic.oup.com/jxb/aticle-abstact/49/324/1213/481115

4 1216 Seymou et al. to te wate bat, a quick dop in T was followed by tempeatue cycle ultimately inceased tei eat poduction T and V (e). Fo easons unknown, T was unstable wen ood tempeatue was loweed duing te day, bot between C duing te day, but T emained in constant dakness (Fig. 2) and in natual potopeiod between C, wile V mioed T. V duing (Fig. 3). Altoug potopeiod does not influence temo- peiod e was ige tan tat in peiod a, because te egulation, it pobably affects flowe development and te petals ad opened patially, eleasing eat fom onset of temogenesis as it does in aum lilies (Buggeln te eceptacle into te ood and equiing geate eat et al., 1971). Potopeiodic initiation of floweing can begin poduction to keep te eceptacle wam. At te as muc as 2 d befoe an aum lily infloescence opens wate bat was etuned to 30 C (f ) and te subsequent (Meeuse and Raskin, 1988). Te expeiments in tis study patten was simila to tat in peiod (b). began on te day befoe te petals opened fo te fist time, In summay, canges in T appeaed to ave two effects and te flowes wee aleady temoegulating (Seymou on T and V. Fist tee was an immediate effect, and Scultze-Motel, 1996, 1998). canges in T esulting in canges in T and V te same Inteestingly, temoegulation continued in constant diection. Ten tee was a delayed effect, inceased T dakness fo ove 3 d (Fig. 2), sowing tat exposue of esulting in deceasing V, followed by a eduction in te flowe to potopeiodic canges is not necessay to T, and vice vesa. Tee was no detectable effect of time maintain te esponses. Because only te flowes wee kept of day on eite T o V. in dakness, oweve, it is possible tat continued potopeiodic exposue of te est of te plant could ave Afte initial egulatoy tempeatue adjustments to tempeatue cange, T and T tended to stabilize in te influenced te esults. Te sequence of petal opening and wate-jacketed oods. Fo compaison of tese tee closing is stongly coelated wit ligt cycle in te Asian teatments, and to sow te epoducibility of te lotus subspecies (Miyake, 1898) and te Ameican subspecies esponses, data fo flowes duing tis peiod of stability (Some, 1977; Scneide and Bucanan, 1980), but it wee selected ( Table 1). Duing cold and wam exposue, was not possible to obseve wete te petals continued T aveaged about 18 C and 30 C, wile T aveaged to move in te dak in tis study. It is well known tat about 32 C and 34 C, and V aveaged 1.9 ml min 1 cyclic movements of petals continue wit an endogenous and 0.9 ml min 1, espectively. Tempeatue elevations ytm in ote flowes in constant dakness (Sweeney, and espiatoy ates of wate-jacketed flowes, in bot 1979). dakness and evese-cycle, wee simila to values taken Te two-pase esponses to sudden ambient tempeatue witin te anges of C and C in a lage cange indicate a apid, mass-action effect and a slowe, study of te lotus unde natual ligt cycles ( Table 1). egulatoy adjustment. Fo example, aising ood tempe- atue esulted in immediate inceases in eceptacle tempeatue Discussion and ate of oxygen consumption (Figs 2, 3). Tis esponse was appaent in contol flowes, wen moning Tese expeiments demonstate tat te temoegulatoy sunligt quickly aised ood tempeatue, esulting in a esponses of te saced lotus depend on tempeatue and spike in oxygen consumption ( Fig. 1; Seymou and ae not influenced by potopeiod. Flowes on te evesed Scultze-Motel, 1996, 1998). Te bief, inappopiate ise Table 1. Tempeatues of eceptacle and ates of oxygen consumption (V ) of lotus flowes in natual and evesed ligt cycles, and in constant dakness Data wee cosen wen ood tempeatues wee stable, i.e. duing te peiod of tempeatue egulation and seveal ous afte a ood tempeatue cange. Means, 95% confidence intevals and sample sizes ae given fo cool and wam envionments. Ligt cycle Tempeatue V Tempeatue V Hood Receptacle (ml min 1) Hood Receptacle (ml min 1) Natual Mean CI n Natuala Mean CI n Dakness Mean CI n Revese Mean CI n adata fom Seymou and Scultze-Motel (1998). Downloaded fom ttps://academic.oup.com/jxb/aticle-abstact/49/324/1213/481115

5 Lotus tempeatue egulation 1217 in eat poduction was pobably due to van t Hoff s Q Buggeln RG, Meeuse BJD, Klima JR Te contol of 10 genealization tat biocemical eactions ougly double blooming in Sauomatum guttatum (Aaceae) by dakness. Canadian Jounal of Botany 49, wit a 10 C tempeatue ise. Howeve, te full Q effect 10 Gottsbege G Beetle pollination and floweing ytm of tempeatue was obscued by te slowe development of of Annona spp. (Annonaceae) in Bazil. Plant Systematics an indiect temoegulatoy mecanism tat deceases and Evolution 167, eat poduction. Fast and slow components ae also appa- Gottsbege G, Amaal A Pollination stategies in ent afte quick deceases in ambient tempeatue. Bazilian Pilodendon species. Beicte de Deutscen Botaniscen Gesellscaft 97, Te slow egulatoy component is pobably esponsible Lampect I, Seymou RS, Scultze-Motel P Diect and fo a maked ysteesis cuve on axes elating ate of eat indiect caloimety of temogenic flowes of te saced poduction to tempeatue of lotus flowes (Seymou and lotus, Nelumbo nucifea. Temocimica Acta 309, Scultze-Motel, 1998). Heat poduction is slow to ise in Meeuse BJD, Raskin I Sexual epoduction in te aum te evening, and slow to fall in te moning, wen flowe lily family, wit empasis on temogenicity. Sexual Plant Repoduction 1, tempeatue is canging apidly. Sluggis egulation is also Miyake K Some pysiological obsevations on Nelumbo appaent in te oscillations of flowe tempeatue afte a nucifea, Gaetn. Te Botanical Magazine, Tokyo 12, quick decease in ambient tempeatue ( Fig. 2). Tese oscil- Pance GT, Aias JR A study of te floal biology of lations, often of deceasing amplitude, suggest tat te ate Victoia amazonica (Poepp.) Soweby (Nympaeaceae). Acta of eat poduction is too ig as flowe tempeatue Amazonica 5, Scneide EL, Bucanan JD Mopological studies of appoaces its temostatic equilibium-point, and an te Nympaeaceae. XI. Te floal biology of Nelumbo ovesoot esults. Te ovesoot, in tun, educes eat pentapetala. Ameican Jounal of Botany 67, poduction too muc, esulting in a smalle tempeatue Seymou RS, Batolomew GA, Banat MC Respiation undesoot. Te oscillation eventually disappeas as te and eat poduction by te infloescence of Pilodendon flowe finds its equilibium-point. It is felt tat te slugselloum Koc. Planta 157, Seymou RS, Scultze-Motel P Temoegulating lotus gisness of te esponses indicates tat tempeatue egula- flowes. Natue 383, 305. tion occus by canges in concentations of putative Seymou RS, Scultze-Motel P Heat-poducing flowes. biocemicals tat affect te ate of eat poduction, ate Endeavou 21, tan canges in te stuctue of enzyme systems. Seymou RS, Scultze-Motel P Pysiological tempeatue egulation by flowes of te saced lotus. Pilosopical Tansactions of te Royal Society, London B (in pess). Acknowledgements Some SH Aspects of te biology of Nelumbo pentapetala ( Walte) Fenald, te Ameican lotus, of te Uppe Tis study was suppoted by te Austalian Reseac Council Mississippi. Tansactions of te Wisconsin Academy of and te Deutsce Foscungsgemeinscaft. We tank te staff Sciences, Ats, and Lettes 65, of te Botanic Gadens of Adelaide fo assistance and toleance. Sweeney BM Endogenous ytms in te movements of plants. In: Haupt W, Feinleib ME, eds. Encyclopedia of plant pysiology, Vol. VII. Pysiology of movements. Belin: Refeences Spinge, Wites PC Measuement of V, V, and evapoative C Bosc T, Batlott W Classification and distibution of wate loss wit a flow-toug mask. Jounal of Applied te genus Nelumbo Adans. (Nelumbonaceae). Beitäge zu Pysiology: Respiatoy, Envionmental and Execise Biologie de Pflanzen 68, Pysiology 42, Downloaded fom ttps://academic.oup.com/jxb/aticle-abstact/49/324/1213/481115