Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Functional transition in the floral receptacle of the sacred lotus (Nelumbo nucifera): from thermogenesis to photosynthesis

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

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

B Institute for Conservation Biology, Department of Biological Sciences, University of Wollongong, Wollongong, NSW 2522, Australia.

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

D Corresponding author. Email: rebecca.miller@sci.monash.edu.au

Functional Plant Biology 36(5) 471-480 https://doi.org/10.1071/FP08326
Submitted: 22 December 2008  Accepted: 10 March 2009   Published: 6 May 2009

Abstract

The receptacle of the sacred lotus is the main source of heat during the thermogenic stage of floral development. Following anthesis, it enlarges, greens and becomes a fully functional photosynthetic organ. We investigated development of photosynthetic traits during this unusual functional transition. There were two distinct phases of pigment accumulation in receptacles. Lutein and photoprotective xanthophyll cycle pigments accumulated first with 64 and 95% of the maximum, respectively, present before anthesis. Lutein epoxide comprised 32% of total carotenoids in yellow receptacles, but declined with development. By contrast, more than 85% of maximum total chlorophyll, β-carotene and Rubisco were produced after anthesis, and were associated with significant increases in maximum electron transport rates (ETR) and photochemical efficiency (Fv/Fm). Leaves and mature receptacles had similar Rubisco content and ETRs (>200 μmol m−2 s−1), although total chlorophyll and total carotenoid contents of leaves were significantly higher than those of green receptacles. Receptacle δ13C before anthesis was similar to that of leaves; consistent with leaf photosynthesis being the source of C for these tissues. In contrast, mature receptacles had significantly lower δ13C than leaves, suggesting that 14–24% of C in mature receptacles is the result of refixation of respired CO2.

Additional keywords: antheraxanthin, chlorophyll, development, greening, lutein epoxide, photosynthesis, Rubisco, violaxanthin, zeaxanthin, β-carotene.


Acknowledgements

We thank Tiffany Barlow, Nicole Grant and Laura Howie for assistance in the field and with chlorophyll fluorescence analyses, Spencer Whitney (ANU) for generously providing Rubisco primary antibody, Jodie Dunn for assistance with HPLC, Shizue Matsubara for a lutein epoxide standard, and David Hollingworth for the photography and image layout in the supplementary figures.


References


Aschan G, Pfanz H (2003) Non-foliar photosynthesis – a strategy of additional carbon acquisition. Flora 198, 81–97. open url image1

Aschan G, Pfanz H, Vodnik D, Batic F (2005) Photosynthetic performance of vegetative and reproductive structures of green hellebore (Helleborus viridis L. agg.). Photosynthetica 43, 55–64.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Asokanthan PS, Johnson RW, Griffith M, Krol M (1997) The photosynthetic potential of canola embryos. Physiologia Plantarum 101, 353–360.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Bazzaz FA, Carlson RW, Harper JL (1979) Contribution to reproductive effort by photosynthesis or flowers and fruits. Nature 279, 554–555.
Crossref | GoogleScholarGoogle Scholar | open url image1

Biscoe PV, Gallagher JN, Littleton EJ, Monteith JL, Scott RK (1975) Barley and its environment: IV. Sources of assimilate for the grain. Journal of Applied Ecology 12, 295–318.
Crossref | GoogleScholarGoogle Scholar | open url image1

Blanke MM, Lenz F (1989) Fruit photosynthesis. Plant, Cell & Environment 12, 31–46.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Blanke MM, Notton BA, Hucklesby DP (1986) Physical and kinetic properties of photosynthetic phosphoenolpyruvate carboxylase in developing apple fruit. Phytochemistry 25, 601–606.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Buchmann N, Kao W-Y, Ehleringer JR (1997) Influence of stand structure on carbon-13 of vegetation, soil, and canopy air within deciduous and evergreen forests in Utah, United States. Oecologia 110, 109–119.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bungard RA, Ruban AV, Hibberd JM, Press MC, Horton P, Scholes JD (1999) Unusual carotenoid composition and a new type of xanthophyll cycle in plants. Proceedings of the National Academy of Sciences of the United States of America 96, 1135–1139.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Cipollini ML, Levey DJ (1991) Why some fruits are green when they are ripe: carbon balance in fleshy fruits. Oecologia 88, 371–377.
Crossref | GoogleScholarGoogle Scholar | open url image1

Clément C, Mischler P, Burrus M, Audran J-C (1997) Characteristics of the photosynthetic apparatus and CO2 fixation in the flower bud of Lilium. II. Anther. International Journal of Plant Sciences 158, 801–810.
Crossref | GoogleScholarGoogle Scholar | open url image1

Close DC, Davidson NJ, Davies NW (2006) Seasonal fluctuations in pigment chemistry of co-occurring plant hemi-parasites of distinct form and function. Environmental and Experimental Botany 58, 41–46.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Dunn JL, Turnbull JD, Robinson SA (2004) Comparison of solvent regimes for the extraction of photosynthetic pigments from the leaves of higher plants. Functional Plant Biology 31, 195–202.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Duranceau M, Ghashghaie J, Brugnoli E (2001) Carbon isotope discrimination during photosynthesis and dark respiration in intact leaves of Nicotiana sylvestris: comparisons between wild type and mitochondrial mutant plants. Australian Journal of Plant Physiology 28, 65–71.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Eastmond PJ, Rawsthorne S (1998) Comparison of the metabolic properties of plastids isolated from developing leaves or embryos of Brassica napus L. Journal of Experimental Botany 49, 1105–1111.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Edelenbos M, Christensen LP, Grevsen K (2001) HPLC determination of chlorophyll and carotenoid pigments in processed green pea cultivars (Pisum sativum L.). Journal of Agricultural and Food Chemistry 49, 4768–4774.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Esteban R, Jiménez ET, Jiménez MS, Morales D, Hormaetxe K, Becerril JM, García-Plazaola JI (2007) Dynamics of violaxanthin and lutein epoxide xanthophyll cycles in Lauraceae tree species under field conditions. Tree Physiology 27, 1407–1414.
CAS | PubMed |
open url image1

Esteban R, Jiménez MS, Morales D, Jiménez ET, Hormaetxe K, Becerril JM, Osmond CB, García-Plazaola JI (2008) Short- and long-term modulation of the lutein epoxide and violaxanthin cycles in two species of the Lauraceae: sweet bay laurel (Laurus nobilis L.) and avocado (Persea americana Mill.). Plant Biology 10, 288–297.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40, 503–537.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Flinn AM, Pate JS (1970) A quantitative study of carbon transfer from pod and subtending leaf to the ripening seeds of the field pea (Pisum arvense L.). Journal of Experimental Botany 21, 71–82.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Furbank RT, White R, Palta JA, Turner NC (2004) Internal recycling of respiratory CO2 in pods of chickpea (Cicer arietinum L.): the role of the pod wall, seed coat, and embryo. Journal of Experimental Botany 55, 1687–1696.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

García-Plazaola JI, Hernández A, Errasti E, Becerril JM (2002) Occurrence and operation of the lutein epoxide cycle in Quercus species. Functional Plant Biology 29, 1075–1080.
Crossref | GoogleScholarGoogle Scholar | open url image1

García-Plazaola JI, Hernández A, Olano JM, Becerril JM (2003) The operation of the lutein epoxide cycle correlates with energy dissipation. Functional Plant Biology 30, 319–324.
Crossref | GoogleScholarGoogle Scholar | open url image1

García-Plazaola JI, Hormaetxe K, Hernández A, Olano JM, Becerril JM (2004) The lutein epoxide cycle in vegetative buds of woody plants. Functional Plant Biology 31, 815–823.
Crossref | GoogleScholarGoogle Scholar | open url image1

García-Plazaola JI, Matsubara S, Osmond CB (2007) The lutein epoxide cycle in higher plants: its relationships to other xanthophyll cycles and possible functions. Functional Plant Biology 34, 759–773.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gebbing T, Schnyder H (2001) 13C Labelling kinetics of sucrose in glumes indicates significant refixation of respiratory CO2 in the wheat ear. Australian Journal of Plant Physiology 28, 1047–1053.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Gilmore AM, Yamamoto HY (1991) Resolution of lutein and zeaxanthin using a non-endcapped lightly carbon-loaded C18 high-performance liquid chromatographic column. Journal of Chromatography. A 543, 137–145.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Goldstein G, Sharifi MR, Kohorn LU, Lighton JRB, Shultz L, Rundel PW (1991) Photosynthesis by inflated pods of a desert shrub, Isomeris arborea. Oecologia 85, 396–402.
Crossref | GoogleScholarGoogle Scholar | open url image1

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. Journal of Experimental Botany 59, 705–714.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Griffiths H (1993) Carbon isotope discrimination. In ‘Photosynthesis and production in a changing environment: a field and laboratory manual’. (Eds DO Hall, JMO Scurlock, HR Bolhàr-Nordenkampf, RC Leegood, SP Long). pp. 181–192. (Chapman & Hall: London)

Harlow E , Lane D (1988) ‘Antibodies: a laboratory manual.’ (Cold Springs Harbour Laboratory Press: Cold Spring Harbour, NY)

Harvey DM, Hedley CL, Keely RJ (1976) Photosynthetic and respiratory studies during pod and seed development in Pisum sativum L. Annals of Botany 40, 993–1001.
CAS |
open url image1

Heaton THE, Crossley A (1995) Carbon isotope variations in a plantation of sitka spruce, and the effect of acid mist. Oecologia 103, 109–117.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kevan PG (1983) Floral colors through the insect eye: what are they and what they mean. In ‘Handbook of experimental pollination biology’. (Eds CE Jones, RJ Little) pp. 3–30. (Van Nostrand Reinhold Company: New York)

Kirichenko EB, Krendeleva T, Koukariskikh G, Nizovskaia N (1993) Photochemical activity in chloroplasts of anthers and caryopsis pericarp in cereals. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 40, 229–233. open url image1

Kondo M, Muraoka H, Uchida M, Yazaki Y, Koizumi H (2005) Refixation of respired CO2 by understory vegatation in a cool-temperate deciduous forest in Japan. Agricultural and Forest Meteorology 134, 110–121.
Crossref | GoogleScholarGoogle Scholar | open url image1

Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Lin G, Ehleringer JR (1997) Carbon isotopic fractionation does not occur during dark respiration in C3 and C4 plants. Plant Physiology 114, 391–394.
CAS | PubMed |
open url image1

Lüttge U, Fetene M, Liebig M, Rascher U, Beck E (2001) Ecophysiology of niche occupation by two giant rosette plants, Lobelia gibberoa Hemsl and Solanecio gigas (Vatke) C. Jeffrey, in an Aftromontane forest valley. Annals of Botany 88, 267–278.
Crossref | GoogleScholarGoogle Scholar | open url image1

Matsubara S, Naumann M, Martin R, Nichol C, Rascher U, Morosinotto T, Bassi R, Osmond CB (2005) Slowly reversible de-epoxidation of lutein-epoxide in deep shade leaves of a tropical tree legume may ‘lock-in’ lutein-based photoprotection during acclimation to strong light. Journal of Experimental Botany 56, 461–468.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Matsubara S, Morosinotto T, Osmond CB, Bassi R (2007) Short- and long-term operation of the lutein-epoxide cycle in light-harvesting antenna complexes. Plant Physiology 144, 926–941.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Matus Z, Molnar P, Szabo LG (1993) Main carotenoids in pressed seeds (Cucurbitae semen) of oil pumpkin (Cucurbita pepo convar. pepo var. styriaca). Acta Pharmaceutica Hungarica 63, 247–256.
CAS | PubMed |
open url image1

Maxwell K, Johnson GN (2000) Chlorophyll flurorescence – a practical guide. Journal of Experimental Botany 51, 659–668.
CAS | Crossref | PubMed |
open url image1

Meeuse BJD (1975) Thermogenic respiration in aroids. Annual Review of Plant Physiology 26, 117–126.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Merzlyak MN, Solovchenko AE (2002) Photostability of pigments in ripening apple fruit: a possible photoprotective role of carotenoids during plant senescence. Plant Science 163, 881–888.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Peng C-L, Lin Z-F, Su Y-Z, Lin G-Z, Dou H-Y, Zhao C-X (2006) The antioxidative function of lutein: electron spin resonance studies and chemical detection. Functional Plant Biology 33, 839–846.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Rabinowitch HD, Budowski P, Kedar N (1975) Carotenoids and epoxide cycles in mature-green tomatoes. Planta 122, 91–97.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Razungles AJ, Babic I, Sapis J-C, Bayonove CL (1996) Particular behavior of epoxy xanthophylls during veraison and maturation of grape. Journal of Agricultural and Food Chemistry 44, 3821–3825.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Robinson SA , Russell AW (1999) Development of the photosynthetic apparatus in Australian rainforest leaves. In ‘Photosynthesis: mechanisms and effects’. (Ed. G Gareb) pp. 3991–3994. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Ruuska SA, Schwender J, Ohlrogge JB (2004) The capacity of green oilseeds to utilize photosynthesis to drive biosynthetic processes. Plant Physiology 136, 2700–2709.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Salopek-Sondi B, Kovac M, Ljubesic N, Magnus V (2000) Fruit initiation in Helleborus niger L. triggers chloroplast formation and photosynthesis in the perianth. Journal of Plant Physiology 157, 357–364.
CAS |
open url image1

Santoni V, Bellini C, Caboche M (1994) Use of two-dimensional protein-pattern analysis for the characterization of Arabidopsis thaliana mutants. Planta 192, 557–566.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Schleser GH (1990) Investigations of the δ13C pattern in leaves of Fagus sylvatica L. Journal of Experimental Botany 41, 565–572.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Smillie RM, Hetherington SE, Davies WJ (1999) Photosynthetic activity of the calyx, green shoulder, pericarp, and locular parenchyma of tomato fruit. Journal of Experimental Botany 50, 707–718.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Sternberg L, Moreira MZ, Martinelli LA, Victoria RL, Barbosa EM, Bonates LCM, Nepstad DC (1997) Carbon dioxide recycling in two Amazonian tropical forests. Agricultural and Forest Meteorology 88, 259–268.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tai C-Y, Chen BH (2000) Analysis and stability of carotenoids in the flowers of daylily (Hemerocallis disticha) as affected by various treatments. Journal of Agricultural and Food Chemistry 48, 5962–5968.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Thayer SS, Björkman O (1990) Leaf xanthophyll content and composition in sun and shade determined by HPLC. Photosynthesis Research 23, 331–343.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Vemmos SN, Goldwin GK (1994) The photosynthetic activity of Cox’s orange pippin apple flowers in relation to fruit setting. Annals of Botany 73, 385–391.
Crossref | GoogleScholarGoogle Scholar | 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. Plant Physiology 140, 1367–1373.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Watson TL, Close DC, Davidson NJ, Davies NW (2004) Pigment dynamics during cold-induced photoinhibition of Acacia melanoxylon. Functional Plant Biology 31, 481–489.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Whitney SM, Andrews TJ (2001) Plastome-encoded bacterial ribulose-1,5-bisphosphate carboxylase oxygenase (Rubisco) supports photosynthesis and growth in tobacco. Proceedings of the National Academy of Sciences of the United States of America 98, 14738–14743.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Wullschleger SD, Oosterhuis DM, Hurren RG, Hanson PJ (1991) Evidence for light-dependent recycling of respired carbon dioxide by the cotton fruit. Plant Physiology 97, 574–579.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1