Photosynthetica 2014, 52(1):3-15 | DOI: 10.1007/s11099-014-0004-2

Contribution of stem CO2 fixation to whole-plant carbon balance in nonsucculent species

E. Ávila1,*, A. Herrera1, W. Tezara1
1 Centro de Botánica Tropical, Instituto de Biología Experimental, Universidad Central de Venezuela, Caracas, Venezuela

In many plant species that remain leafless part of the year, CO2 fixation occurring in green stems represents an important carbon gain. Traditionally, a distinction has been made between stem photosynthesis and corticular photosynthesis. All stem photosynthesis is, sensu stricto, cortical, since it is carried out largely by the stem cortex. We proposed the following nomenclature: stem net photosynthesis (SNP), which includes net CO2 fixation by stems with stomata in the epidermis and net corticular CO2 fixation in suberized stems, and stem recycling photosynthesis (SRP), which defines CO2 ling in suberized stems. The proposed terms should reflect differences in anatomical and physiological traits. SNP takes place in the chlorenchyma below the epidermis with stomata, where the net CO2 uptake occurs, and it resembles leaf photosynthesis in many characteristics. SRP is found in species where the chlorenchyma is beneath a well-developed stomata-free periderm and where reassimilation of internally respired CO2 occurs. SNP is common in plants from desert ecosystems, rates reaching up to 60% of the leaf photosynthetic rate. SRP has been demonstrated in trees from temperate forests and it offsets partially a carbon loss by respiration of stem nonphotosynthetic tissues. Reassimilation can vary between 7 and 123% of respired CO2, the latter figure implying net CO2 uptake from the atmosphere. Both types of stem photosynthesis contribute positively to the carbon economy of the species, in which they occur; they are advantageous to the plant because they allow the maintenance of physiological activity during stress, an increase of integrated water use efficiency, and they provide the carbon source used in the production of new organs.

Additional key words: carbon balance; CO2 reassimilation; green stem; stem net photosynthesis; stem photosynthesis; stem recycling photosynthesis

Received: January 30, 2013; Accepted: July 9, 2013; Published: March 1, 2014  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Ávila, E., Herrera, A., & Tezara, W. (2014). Contribution of stem CO2 fixation to whole-plant carbon balance in nonsucculent species. Photosynthetica52(1), 3-15. doi: 10.1007/s11099-014-0004-2
Download citation

References

  1. Adams, M.S., Strain, B.R.: Photosynthesis in stems and leaves of Cercidium floridum: spring and summer diurnal field response and relation to temperature. - Oecolog. Plantar. 3: 285-297, 1968.
  2. Adams, M.S., Strain, B.R., Ting, I.P.: Photosynthesis in chlorophyllous stem tissue and leaves of Cercidium floridium: Accumulation and distribution of 14C from 14CO2. - Plant Physiol. 42: 1797-1799, 1967. Go to original source...
  3. Aidar, M.P.M., Schmidt, S., Moss, G., et al.: Nitrogen use strategies of neotropical rainforest trees in threatened Atlantic Forest. - Plant Cell Environ. 26: 389-399, 2003. Go to original source...
  4. Alessio, G.A., Pietrini, F., Brilli, F., Loreto, F.: Characteristics of CO2 exchange between peach stems and the atmosphere. - Funct. Plant. Biol. 32: 787-795, 2005. Go to original source...
  5. Allen, O.N., Allen, E.K. The Leguminosae: A Source Book of Characteristics, Uses, and Nodulation. - Univ. Wisconsin Press, Madison 1981.
  6. Aschan, G., Pfanz, H.: Non-foliar photosynthesis - a strategy of additional carbon acquisition. - Flora 198: 81-97, 2003. Go to original source...
  7. Aschan, G., Pfanz, H., Vodnik, D., Batič, F.: Photosynthetic performance of vegetative and reproductive structures of green hellebore (Helleborus viridis L. agg.). - Photosynthetica 43: 55-64, 2005. Go to original source...
  8. Aschan, G., Wittmann, C., Pfanz, H.: Age-dependent bark photosynthesis of aspen twigs. - Trees-Struct. Funct. 15: 431-437, 2001. Go to original source...
  9. Berveiller, D., Damesin, C.: Carbon assimilation by tree stems: potential involvement of phosphoenolpyruvate carboxylase. - Trees-Struct. Funct. 22: 149-157, 2008. Go to original source...
  10. Berveiller, D., Fresneau, C., Damesin, C.: Effect of soil nitrogen supply on carbon assimilation by tree stems. - Ann. For. Sci. 67: 609, 2010. Go to original source...
  11. Berveiller, D., Kierzkowski, D., Damesin, C.: Interspecific variability of stem photosynthesis among tree species. - Tree Physiol. 27: 53-61, 2007. Go to original source...
  12. Björkman, O., Demmig, B.: Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. - Planta 170: 489-504, 1987. Go to original source...
  13. Bloemen, J., McGuire, M.A., Aubrey, D.P., et al.: Assimilation of xylem-transported CO2 is dependent on transpiration rate but is small relative to atmospheric fixation. - J. Exp. Bot. 64: 2129-2138, 2013. Go to original source...
  14. Bossard, C.C., Rejmanek, M.: Why have green stems? - Funct. Ecol. 6: 197-205, 1992. Go to original source...
  15. Bronson, D.R., English, N.B., Dettman, D.L., Williams, D.G.: Seasonal photosynthetic gas exchange and water-use efficiency in a constitutive CAM plant, the giant saguaro cactus (Carnegiea gigantea). - Oecologia 167: 861-871, 2011. Go to original source...
  16. Cerasoli, S., McGuire, M.A., Faria, J. et al.: CO2 efflux, CO2 concentration and photosynthetic refixation in stems of Eucalyptus globulus (Labill.). - J. Exp. Bot. 60: 99-105, 2009. Go to original source...
  17. Cernusak, L.A., Hutley, L.B.: Stable isotopes reveal the contribution of corticular photosynthesis to growth in branches of Eucalyptus miniata. - Plant Physiol. 155: 515-523, 2011. Go to original source...
  18. Cernusak, L.A., Hutley, L.B, Beringer, J., Tapper, N.J.: Stem and leaf gas exchange and their responses to fire in a north Australian tropical savanna. - Plant Cell Environ. 29: 632-646, 2006. Go to original source...
  19. Cernusak, L.A., Marshall, J.D.: Photosynthetic refixation in branches of Western White Pine. - Funct. Ecol. 14: 300-311, 2000. Go to original source...
  20. Cernusak, L.A., Marshall, J.D., Comstock, J.P., Balster, N.J.: Carbon isotope discrimination of photosynthetic bark. - Oecologia 128: 24-35, 2001. Go to original source...
  21. Cernusak, L.A., Tcherkez, G., Keitel, C. et al.: Why are non photosynthetic tissues generally 13C enriched compared with leaves in C3 plants? Review and synthesis of current hypotheses. - Funct. Plant Biol. 36: 199-213, 2009. Go to original source...
  22. Chaves, M.M., Pereira, J.S.: Water stress, CO2 and climate change. - J. Exp. Bot. 43: 1131-1139, 1992. Go to original source...
  23. Comstock, J.P., Ehleringer, J.R.: Contrasting photosynthetic behavior of leaves and stems of Hymenoclea salsola, a greentwigged warm desert shrub. - Am. J. Bot. 75: 1360-1370, 1988. Go to original source...
  24. Comstock, J.P., Ehleringer, J.R.: Effect of variations in leaf size on morphology and photosynthetic rate of twigs. - Funct. Ecol. 4: 209-221, 1990. Go to original source...
  25. Damesin, C.: Respiration and photosynthesis characteristics of current-year stems of Fagus sylvatica: from the seasonal patterns to an annual balance. - New Phytol. 158: 465-475, 2003. Go to original source...
  26. Dima, E., Manetas, Y., Psaras, G.K.: Chlorophyll distribution pattern in inner stem tissues: evidence from epifluorescence microscopy and reflectance measurements in 20 woody species. - Trees-Struct. Funct. 20: 515-521, 2006. Go to original source...
  27. Ehleringer, J.R., Comstock, J.P, Cooper, T.A: Leaf-twig carbon isotope ratio differences photosynthetic-twig desert shrubs. - Oecologia 71: 318-320, 1987. Go to original source...
  28. Ehleringer, J.R., Cooper, T.A.: On the role of orientation in reducing photoinhibitory damage in photosynthetic-twig desert shrubs. - Plant Cell Environ. 15: 301-306, 1992. Go to original source...
  29. Evans, J.R.: Photosynthesis and nitrogen relationships in leaves of C3 plants. - Oecologia 78: 9-19, 1989. Go to original source...
  30. Filippou, M., Fasseas, C., Karabourniotis, G.: Photosynthetic characteristics of olive tree (Olea europaea) bark. - Tree Physiol. 27: 977-984, 2007. Go to original source...
  31. Foote, K.C., Schaedle, M.: Diurnal and seasonal patterns of photosynthesis and respiration by stems of Populus tremuloides Michx. - Plant Physiol. 58: 651-655, 1976. Go to original source...
  32. Francino, D., Sant'Anna-Santos, B., Silva, K., Thadeo, M., Meira, R., Azevedo, A.: [Leaf and stem anatomy of Chamaecrista trichopoda (Caesalpinoideae) and histochemistry of extrafloral nectary.] - Planta Daninha 24: 695-705, 2006. [In Portuguese] Go to original source...
  33. Gibson, A.C.: Anatomy of photosynthetic old stems of nonsucculent dicotyledons from North American deserts. - Bot. Gaz. 144: 347-362, 1983. Go to original source...
  34. Gibson, A.C.: Photosynthetic organs of desert plants. - Bioscience 48: 911-920, 1998. Go to original source...
  35. Hibberd, J.M., Quick, W.P.: Characteristics of C4 photosynthesis in stems and petioles of flowering plants. - Nature 415: 451-454, 2002. Go to original source...
  36. Kauppi, A.: Seasonal fluctuations in chlorophyll content in birch stems with special reference to bark thickness and light transmission, a comparison between sprouts and seedlings. - Flora 185: 107-125, 1991. Go to original source...
  37. Kyriakis, G., Fasseas, C.: A novel type of tube network within the stem bark of Olea europaea L. - Flora 205: 90-93, 2010. Go to original source...
  38. Langenfeld-Heyser, R.: CO2 fixation in stem slices of Picea abies (L.) Karst: microautoradiographic studies. - Trees-Struct. Funct. 3: 24-32, 1989. Go to original source...
  39. Levizou, E., Petropoulou, Y., Manetas, Y.: Carotenoid composition of peridermal twigs does not fully conform to a shade acclimation hypothesis. - Photosynthetica 42: 591-596, 2004. Go to original source...
  40. Levizou, E., Manetas, Y.: Photosynthetic pigment contents in twigs of 24 woody species assessed by in vivo reflectance spectroscopy indicate low chlorophyll levels but high carotenoid/chlorophyll ratios. - Environ. Exp. Bot. 59: 293-298, 2007. Go to original source...
  41. Levizou, E., Manetas, Y.: Maximum and effective PSII yields in the cortex of the main stem of young Prunus cerasus trees: effects of seasons and exposure. - Trees-Struct. Funct. 22: 159-164, 2008. Go to original source...
  42. Lindorf, H., De Parisca, L., Rodríguez, P.: [Botany. Classification, structure and reproduction].. - Ediciones de la Biblioteca-UCV, Pp. 295-356. Caracas 2006. [In Spanish]
  43. Manetas, Y.: Probing corticular photosynthesis through in vivo chlorophyll fluorescence measurements: evidence that high internal CO2 levels suppress electron flow and increase the risk of photoinhibition. - Physiol. Plantarum 120: 509-517, 2004. Go to original source...
  44. Manetas, Y., Pfanz, H.: Spatial heterogeneity of light penetration through periderm and lenticels and concomitant patchy acclimation of corticular photosynthesis. - Trees-Struct. Funct. 19: 409-414, 2005. Go to original source...
  45. McGuire, M.A., Cerasoli, S., Teskey, R.O.: CO2 fluxes and respiration of branch segments of sycamore (Platanus occidentalis L.) examined at different sap velocities, branch diameters, and temperatures. - J. Exp. Bot. 58: 2159-2168, 2007. Go to original source...
  46. McGuire, M.A., Marshall, J.D., Teskey, R.O.: Assimilation of xylem-transported 13C-labelled CO2 in leaves and branches of sycamore (Platanus occidentalis L.). - J. Exp Bot. 60: 3809-3817, 2009. Go to original source...
  47. McGuire, M.A., Teskey, R.O.: Estimating stem respiration in trees by a mass balance approach that accounts for internal and external fluxes of CO2. - Tree Physiol. 24: 571-578, 2004. Go to original source...
  48. Mooney, H.A., Strain, B.R.: Bark photosynthesis in ocotillo. - Madroño 17: 230-233, 1964.
  49. Nilsen, E.T.: Partitioning growth and photosynthesis between leaves and stems during nitrogen limitation in Spartium junceum. - Am. J. Bot. 79: 1217-1223, 1992. Go to original source...
  50. Nilsen, E.T.: Stem photosynthesis: extent, patterns, and role in plant carbon economy. - In: Gartner, B. (ed.): Plant Stems: Physiology and Functional Morphology. Pp. 223-240. Acad. Press, San Diego 1995. Go to original source...
  51. Nilsen, E.T., Bao, Y.: The influence of water stress on stem and leaf photosynthesis in Glycine max and Sparteum junceum (Leguminosae). - Am. J. Bot. 77: 1007-1015, 1990. Go to original source...
  52. Nilsen, E.T., Karpa, D., Mooney, H.A., Field, C.: Patterns of stem photosynthesis in two invasive legumes (Spartium junceum, Cytisus scoparius) of the California coastal region. - Am. J. Bot. 80: 1126-1136, 1993. Go to original source...
  53. Nilsen, E.T., Meinzer, F.C., Rundel, P.W.: Stem photosynthesis in Psorothamnus spinosus (smoke tree) in the Sonoran desert of California. - Oecologia 79: 193-197, 1989. Go to original source...
  54. Nilsen, E.T., Sharifi, M.R.: Seasonal acclimation of stem photosynthesis in woody legume species from the Mojave and Sonoran Deserts of California. - Plant Physiol. 105: 1385-1391, 1994. Go to original source...
  55. Nilsen, E.T., Sharifi, M.R.: Carbon isotopic composition of legumes with photosynthetic stems from Mediterranean and desert habitats. - Am. J. Bot. 84: 1707-1713, 1997. Go to original source...
  56. Osmond, C.B., Smith, S.D., Gui-Ying, B., Sharkey, T.D.: Stem photosynthesis in a desert ephemeral, Eriogonum inflatum. Characterization of leaf and stem CO2 fixation and H2O vapor exchange under controlled conditions. - Oecologia 72: 542-549, 1987. Go to original source...
  57. Pfanz, H., Aschan, G., Langenfeld-Heyser, R., Wittmann, C., Loose, M.: Ecology and ecophysiology of tree stems: corticular and wood photosynthesis. - Naturwissenschaften 89: 147-162, 2002. Go to original source...
  58. Rentzou, A., Psaras, G.K.: Green plastids, maximal PSII photochemical efficiency and starch content of inner stem tissues of three Mediterranean woody species during the year. - Flora 203: 350-357, 2008. Go to original source...
  59. Saveyn, A., Steppe, K., McGuire, M.A., Lemeur, R., Teskey, R.O.: Stem respiration and carbon dioxide efflux of young Populus deltoides trees in relation to temperature and xylem carbon dioxide concentration. - Oecologia 154: 637-649, 2008. Go to original source...
  60. Saveyn, A., Steppe, K., Ubierna, N., Dawson, T.E.: Woody tissue photosynthesis and its contribution to trunk growth and bud development in young plants. - Plant Cell Environ. 33: 1949-1958, 2010. Go to original source...
  61. Schulze, E.-D., Robichaux, R.H., Grace, J.: Plant water balance. - BioScience 37: 32-36, 1987. Go to original source...
  62. Smith, S.D., Nobel, P.S.: Deserts. - In: Baker, N.R., Long, S.P. (ed.): Photosynthesis in Contrasting Environments. Pp. 13-62. Elsevier Sci. Publ. B.V., Amsterdam 1986.
  63. Smith, S.D., Osmond, C.B.: Stem photosynthesis in a desert ephemeral, Eriogonum inflatum. Morphology, stomatal conductance and water-use efficiency in field populations. - Oecologia 72: 533-541, 1987. Go to original source...
  64. Teskey, R.O., McGuire, M.A.: Carbon dioxide transport in xylem causes errors in estimation of rates of respiration in stems and branches of trees. - Plant Cell Environ. 25: 1571-1577, 2002. Go to original source...
  65. Teskey, R.O., McGuire, M.A.: Measurement of stem respiration of sycamore (Platanus occidentalis L.) trees involves internal and external fluxes of CO2 and possible transport of CO2 from roots. - Plant Cell Environ. 30: 570-579, 2007. Go to original source...
  66. Teskey, R.O., Saveyn, A., Steppe, K., McGuire, M.A.: Origin, fate and significance of CO2 in tree stems. - New Phytol. 177: 17-32, 2008. Go to original source...
  67. Tinoco-Ojanguren, C.: Diurnal and seasonal patterns of gas exchange and carbon gain contribution of leaves and stems of Justicia californica in the Sonoran Desert. - J. Arid Environ. 72: 127-140, 2008. Go to original source...
  68. Vick, J.K., Young, D.R.: Corticular photosynthesis: A mechanism to enhance shrub expansion in coastal environments. - Photosynthetica 47: 26-32, 2009. Go to original source...
  69. Wittmann, C., Aschan, G., Pfanz, H.: Leaf and twig photosynthesis of young beech (Fagus sylvatica) and aspen (Populus tremula) trees grown under different light regimes. - Basic Appl. Ecol. 2: 145-154, 2001. Go to original source...
  70. Wittmann, C., Pfanz, H.: General trait relationships in stems: a study on the performance and interrelationships of several functional and structural parameters involved in corticular photosynthesis. - Physiol. Plant. 134: 636-648, 2008. Go to original source...
  71. Yiotis, C., Manetas, Y., Psaras, G.K.: Leaf and green stem anatomy of the drought deciduous Mediterranean shrub Calicotome villosa (Poiret) Link. (Leguminosae). - Flora 201: 102-107, 2006. Go to original source...
  72. Yiotis, C., Psaras, G.K., Manetas, Y.: Seasonal photosynthetic changes in the green-stemmed Mediterranean shrub Calicotome villosa: a comparison with leaves. - Photosynthetica 46: 262-267, 2008. Go to original source...