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

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Photosynthetica

Abstract

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.

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Abbreviations

CAM:

crassulacean acid metabolism

CE:

carboxylation efficiency

Chl:

chlorophyll

C i :

intercellular CO2 concentration

Fv/Fm :

maximum quantum yield of PSII

g s :

stomatal conductance

P N :

photosynthetic rate

P N-leaf :

leaf net P N

P N-recycling :

stem recycling P N

P N-stem :

stem net P N

PEP:

phosphoenolpyruvate

PEPCK:

phosphoenolpyruvate carboxykinase

PPFD:

photosynthetic photon flux density

R D :

dark-respiration rate

R L :

light-respiration rate

Rubisco:

ribulose-1,5-carboxylase/oxygenase

T:

temperature

SNP:

stem net photosynthesis

SRP:

stem recycling photosynthesis

VPD:

vapor pressure deficit

WUE:

water-use efficiency

δ13C:

isotopic carbon composition

ΦPSII :

effective quantum yield of PSII

References

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Allen, O.N., Allen, E.K. The Leguminosae: A Source Book of Characteristics, Uses, and Nodulation. — Univ. Wisconsin Press, Madison 1981.

    Google Scholar 

  • Aschan, G., Pfanz, H.: Non-foliar photosynthesis — a strategy of additional carbon acquisition. — Flora 198: 81–97, 2003.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Aschan, G., Wittmann, C., Pfanz, H.: Age-dependent bark photosynthesis of aspen twigs. — Trees-Struct. Funct. 15: 431–437, 2001.

    Article  Google Scholar 

  • Berveiller, D., Damesin, C.: Carbon assimilation by tree stems: potential involvement of phosphoenolpyruvate carboxylase. — Trees-Struct. Funct. 22: 149–157, 2008.

    Article  CAS  Google Scholar 

  • Berveiller, D., Fresneau, C., Damesin, C.: Effect of soil nitrogen supply on carbon assimilation by tree stems. — Ann. For. Sci. 67: 609, 2010.

    Article  Google Scholar 

  • Berveiller, D., Kierzkowski, D., Damesin, C.: Interspecific variability of stem photosynthesis among tree species. — Tree Physiol. 27: 53–61, 2007.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Bossard, C.C., Rejmanek, M.: Why have green stems? — Funct. Ecol. 6: 197–205, 1992.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Cernusak, L.A., Marshall, J.D.: Photosynthetic refixation in branches of Western White Pine. — Funct. Ecol. 14: 300–311, 2000.

    Article  Google Scholar 

  • Cernusak, L.A., Marshall, J.D., Comstock, J.P., Balster, N.J.: Carbon isotope discrimination of photosynthetic bark. — Oecologia 128: 24–35, 2001.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Chaves, M.M., Pereira, J.S.: Water stress, CO2 and climate change. — J. Exp. Bot. 43: 1131–1139, 1992.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Ehleringer, J.R., Comstock, J.P, Cooper, T.A: Leaf-twig carbon isotope ratio differences photosynthetic-twig desert shrubs. — Oecologia 71: 318–320, 1987.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Evans, J.R.: Photosynthesis and nitrogen relationships in leaves of C3 plants. — Oecologia 78: 9–19, 1989.

    Article  Google Scholar 

  • Filippou, M., Fasseas, C., Karabourniotis, G.: Photosynthetic characteristics of olive tree (Olea europaea) bark. — Tree Physiol. 27: 977–984, 2007.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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]

    Article  Google Scholar 

  • Gibson, A.C.: Anatomy of photosynthetic old stems of nonsucculent dicotyledons from North American deserts. — Bot. Gaz. 144: 347–362, 1983.

    Article  Google Scholar 

  • Gibson, A.C.: Photosynthetic organs of desert plants. — Bioscience 48: 911–920, 1998.

    Article  Google Scholar 

  • Hibberd, J.M., Quick, W.P.: Characteristics of C4 photosynthesis in stems and petioles of flowering plants. — Nature 415: 451–454, 2002.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • Kyriakis, G., Fasseas, C.: A novel type of tube network within the stem bark of Olea europaea L. — Flora 205: 90–93, 2010.

    Article  Google Scholar 

  • Langenfeld-Heyser, R.: CO2 fixation in stem slices of Picea abies (L.) Karst: microautoradiographic studies. — Trees-Struct. Funct. 3: 24–32, 1989.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Lindorf, H., De Parisca, L., Rodríguez, P.: [Botany. Classification, structure and reproduction].. — Ediciones de la Biblioteca-UCV, Pp. 295–356. Caracas 2006. [In Spanish]

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Mooney, H.A., Strain, B.R.: Bark photosynthesis in ocotillo. — Madroño 17: 230–233, 1964.

    Google Scholar 

  • Nilsen, E.T.: Partitioning growth and photosynthesis between leaves and stems during nitrogen limitation in Spartium junceum. — Am. J. Bot. 79: 1217–1223, 1992.

    Article  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Schulze, E.-D., Robichaux, R.H., Grace, J.: Plant water balance. — BioScience 37: 32–36, 1987.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Vick, J.K., Young, D.R.: Corticular photosynthesis: A mechanism to enhance shrub expansion in coastal environments. — Photosynthetica 47: 26–32, 2009.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

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Correspondence to E. Ávila.

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Acknowledgements. We thank Ilsa Coronel for critical reading of the manuscript and Consejo de Desarrollo Científico y Humanístico (CDCH, Venezuela) for financial support to WT (Grant PI 03-7458-2009).

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Ávila, E., Herrera, A. & Tezara, W. Contribution of stem CO2 fixation to whole-plant carbon balance in nonsucculent species. Photosynthetica 52, 3–15 (2014). https://doi.org/10.1007/s11099-014-0004-2

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