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

Bark and woody tissue photosynthesis: a means to avoid hypoxia or anoxia in developing stem tissues

Christiane Wittmann A B and Hardy Pfanz A
+ Author Affiliations
- Author Affiliations

A Department of Applied Botany, University of Duisburg-Essen, 45117 Essen, Germany.

B Corresponding author. Email: christiane.wittmann@uni-due.de

Functional Plant Biology 41(9) 940-953 https://doi.org/10.1071/FP14046
Submitted: 14 February 2014  Accepted: 21 March 2014   Published: 7 May 2014

Abstract

In woody plants, oxygen transport and delivery via the xylem sap are well described, but the contribution of bark and woody tissue photosynthesis to oxygen delivery in stems is poorly understood. Here, we combined stem chlorophyll fluorescence measurements with microsensor quantifications of bark O2 levels and oxygen gas exchange measurements of isolated current-year stem tissues of beech (Fagus sylvatica L.) and pedunculate oak (Quercus robur L.) to investigate how bark and woody tissue photosynthesis impairs the oxygen status of stems. Measurements were made before bud break, when the axial path of oxygen supply via the xylem sap is impeded. At that time, bark O2 levels showed O2 concentrations below the atmospheric concentration, indicating hypoxic conditions or O2 deficiency within the inner bark, but the values were always far away from anoxic. Under illumination bark and woody tissue photosynthesis rapidly increased internal oxygen concentrations compared with plants in the dark, and thereby counteracted against localised hypoxia. The highest photosynthetic activity and oxygen release rates were found in the outermost cortex tissues. By contrast, rates of woody tissue photosynthesis were considerably lower, due to the high light attenuation of the bark and cortex tissues, as well as resistances in radial oxygen diffusion. Therefore, our results confirm that bark and woody tissue photosynthesis not only play a role in plant carbon economy, but may also be important for preventing low oxygen-limitations of respiration in these dense and metabolically active tissues.

Additional keywords: corticular photosynthesis, oxygen deficiency, oxygen transport, stem photosynthesis, woody tissue photosynthesis, xylem.


References

Armstrong W, Brandle R, Jackson MB (1994) Mechanisms of flood tolerance in plants. Acta Botanica Neerlandica 43, 307–358.
Mechanisms of flood tolerance in plants.CrossRef | 1:CAS:528:DyaK2MXjtV2nsLo%3D&md5=1ebe8a941d9220ce0c96382709929808CAS |

Behnke HD, Sjolund RD (eds) (1990) ‘Sieve elements. Comparative structure, induction and development.’ (Springer-Verlag, Berlin)

Berveiller D, Kierzkowski D, Damesin C (2007) Interspecific variability of stem photosynthesis among tree species. Tree Physiology 27, 53–61.
Interspecific variability of stem photosynthesis among tree species.CrossRef | 1:CAS:528:DC%2BD2sXhsVOmtrc%3D&md5=ea4fd44c9429889cf4c722e0c815535eCAS | 17169906PubMed |

Bloemen J, McGuire MA, Aubrey DP, Teskey RO, Steppe K (2013) Assimilation of xylem-transported CO2 is dependent on transpiration rate but is small relative to atmospheric fixation. Journal of Experimental Botany
Assimilation of xylem-transported CO2 is dependent on transpiration rate but is small relative to atmospheric fixation.CrossRef | 23580747PubMed |

Borisjuk L, Rolletschek H (2009) The oxygen status of the developing seed. New Phytologist 182, 17–30.
The oxygen status of the developing seed.CrossRef | 1:CAS:528:DC%2BD1MXksVKhtb4%3D&md5=57a0caa7f0629b8e74e878e3e84b3cd5CAS | 19207684PubMed |

Cernusak LA, Hutley LB (2011) Stable isotopes reveal the contribution of corticular photosynthesis to growth in branches of Eucalyptus miniata. Plant Physiology 155, 515–523.
Stable isotopes reveal the contribution of corticular photosynthesis to growth in branches of Eucalyptus miniata.CrossRef | 1:CAS:528:DC%2BC3MXksFagtLw%3D&md5=0d6a716c5671cd66c22b63c789edf58dCAS | 21078864PubMed |

Ceschia E, Damesin C, Lebaube S, Pontailler J-Y, Dufrêne E (2002) Spatial and seasonal variations in stem respiration of beech trees (Fagus sylvatica). Annals of Forest Science 59, 801–812.
Spatial and seasonal variations in stem respiration of beech trees (Fagus sylvatica).CrossRef |

Chase WW (1934) ‘The composition, quantity, and physiological significance of gases in tree stems.’ Minnesota Agricultural Experiment Station Technical Bulletin 99. (University of Minnesota: St Paul)

del Hierro AM, Kronberger W, Hietz P, Offenthaler I, Richter H (2002) A new method to determine the oxygen concentration inside the sapwood of trees. Journal of Experimental Botany 53, 559–563.
A new method to determine the oxygen concentration inside the sapwood of trees.CrossRef | 1:CAS:528:DC%2BD38XitVegtLo%3D&md5=2da5af3a4110ae77ed86afac4524bbaeCAS | 11847255PubMed |

Drew MC (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annual Review of Plant Physiology and Plant Molecular Biology 48, 223–250.
Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia.CrossRef | 1:CAS:528:DyaK2sXjs1ensLc%3D&md5=cc84af26832a7698c97ef4d62da7171bCAS | 15012263PubMed |

Eklund L (2000) Internal oxygen levels decrease during the growing season and with increasing stem height. Trees 14, 177–180.
Internal oxygen levels decrease during the growing season and with increasing stem height.CrossRef |

Gansert D, Burgdorf M, Lösch R (2001) A novel approach to the in situ measurement of oxygen concentrations in the sapwood of woody plants. Plant, Cell & Environment 24, 1055–1064.
A novel approach to the in situ measurement of oxygen concentrations in the sapwood of woody plants.CrossRef | 1:CAS:528:DC%2BD3MXnvVylsLc%3D&md5=d6bee571bf1a5860eeaf36d799f305f3CAS |

Geigenberger P (2003) Response of plant metabolism to too little oxygen. Current Opinion in Plant Biology 6, 247–256.
Response of plant metabolism to too little oxygen.CrossRef | 1:CAS:528:DC%2BD3sXjs1Gitrg%3D&md5=58bda27bb9e10ec0f205f4af6c3c6edaCAS | 12753974PubMed |

Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.
The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.CrossRef | 1:CAS:528:DyaL1MXhsFWntL4%3D&md5=0a2fcf683627435ee7561c410f9e266bCAS |

Greenway H, Gibbs J (2003) Mechanisms of anoxia tolerance in plants. II. Energy requirements for maintenance and energy distribution to essential processes. Functional Plant Biology 30, 999–1036.
Mechanisms of anoxia tolerance in plants. II. Energy requirements for maintenance and energy distribution to essential processes.CrossRef | 1:CAS:528:DC%2BD3sXot1Cgtbs%3D&md5=04a26e32e21ddcae7bf438b1f18475aeCAS |

Hook DD, Brown CL, Wetmore RH (1972) Aeration in trees. Botanical Gazette 133, 443–454.
Aeration in trees.CrossRef |

Lendzian K (2006) Survival strategies of plants during secondary growth: barrier properties of phellems and lenticels towards water, oxygen, and carbon dioxide. Journal of Experimental Botany 57, 2535–2546.
Survival strategies of plants during secondary growth: barrier properties of phellems and lenticels towards water, oxygen, and carbon dioxide.CrossRef | 1:CAS:528:DC%2BD28Xotl2mtrk%3D&md5=be034be69d5f9469a92c623576ab2ceaCAS | 16820395PubMed |

McDougal DT, Working EB (1933) ‘The pneumatic system of plants, especially trees.’ Publication 441. (Carnegie Institute of Washington: Washington DC)

McGuire MA, Marshall JD, Teskey RO (2009) Assimilation of xylem-transported 13C-labelled CO2 in leaves and branches of sycamore (Platanus occidentalis L.). Journal of Experimental Botany 60, 3809–3817.
Assimilation of xylem-transported 13C-labelled CO2 in leaves and branches of sycamore (Platanus occidentalis L.).CrossRef | 1:CAS:528:DC%2BD1MXhtV2ks77L&md5=2702fbb631192189f3d4e46998d21ed8CAS | 19602545PubMed |

Pfanz H, Aschan G, Langenfeld-Heyser R, Wittmann C, Loose M (2002) Ecology and ecophysiology of tree stems: corticular and wood photosynthesis. Naturwissenschaften 89, 147–162.
Ecology and ecophysiology of tree stems: corticular and wood photosynthesis.CrossRef | 1:CAS:528:DC%2BD38Xis1GhsL4%3D&md5=1aaa29666a4a93a8819fd7ae985a5a98CAS | 12061398PubMed |

Pruyn ML, Gartner BL, Harmon ME (2002) Within-stem variation of respiration in Pseudotsuga menziesii (Douglas-fir) trees. New Phytologist 154, 359–372.
Within-stem variation of respiration in Pseudotsuga menziesii (Douglas-fir) trees.CrossRef |

Rolletschek H, Stangelmayer A, Borisjuk L (2009) Methodology and significance of microsensor-based oxygen mapping in plant seeds – an overview. Sensors 9, 3218–3227.
Methodology and significance of microsensor-based oxygen mapping in plant seeds – an overview.CrossRef | 1:CAS:528:DC%2BD1MXlvFaitLY%3D&md5=22ea671d5ba6e1df60b382a00d9265bfCAS | 22412307PubMed |

Saglio PH, Rancillac M, Bruzan F, Pradet A (1984) Critical oxygen pressure for growth and respiration of excised and intact roots. Plant Physiology 76, 151–154.
Critical oxygen pressure for growth and respiration of excised and intact roots.CrossRef | 1:CAS:528:DyaL2cXls1Ogtr0%3D&md5=6c3340f8e27411faeab4e77f98972eb0CAS | 16663787PubMed |

Schönherr J, Ziegler H (1980) Water permeability of Betula periderm. Planta 147, 345–354.
Water permeability of Betula periderm.CrossRef | 24311086PubMed |

Sorz J, Hietz P (2006) Gas diffusion through wood: implications for oxygen supply. Trees 20, 34–41.
Gas diffusion through wood: implications for oxygen supply.CrossRef |

Sorz J, Hietz P (2008) Is oxygen involved in beech (Fagus sylvatica) red heartwood formation? Trees 22, 175–185.
Is oxygen involved in beech (Fagus sylvatica) red heartwood formation?CrossRef | 1:CAS:528:DC%2BD1cXjsF2gsLg%3D&md5=7334bebf00c696c9b3689f04399246c5CAS |

Spicer R, Holbrook NM (2005) Within-stem oxygen concentration and sap flow in four temperate tree species: does long-lived xylem parenchyma experience hypoxia? Plant, Cell & Environment 28, 192–201.
Within-stem oxygen concentration and sap flow in four temperate tree species: does long-lived xylem parenchyma experience hypoxia?CrossRef |

Stadler R, Brandner J, Schulz A, Gahrtz M, Sauer N (1995) Phloem loading by the PmSuc2 sucrose carrier from Plantago major occurs into companion cells. The Plant Cell 7, 1545–1554.

Steppe K, Saveyn A, McGuire MA, Lemeur R, Teskey RO (2007) Resistance to radial CO2 diffusion contributes to between-tree variation in CO2 efflux of Populus deltoides stems. Functional Plant Biology 34, 785–792.
Resistance to radial CO2 diffusion contributes to between-tree variation in CO2 efflux of Populus deltoides stems.CrossRef | 1:CAS:528:DC%2BD2sXhtVSgsL%2FF&md5=693aa27c84301cea456d41955714a1f2CAS |

Stockfors J, Linder S (1998) Effect of nitrogen on the seasonal course of growth and maintenance respiration in stems of Norway spruce trees. Tree Physiology 18, 155–166.
Effect of nitrogen on the seasonal course of growth and maintenance respiration in stems of Norway spruce trees.CrossRef | 12651385PubMed |

van Bel AJE, Knoblauch M (2000) Sieve element and companion cell: the story of the comatose patient and the hyperactive nurse. Australian Journal of Plant Physiology 27, 477–487.

van Dongen JT, Schurr U, Pfister M, Geigenberger P (2003) Phloem metabolism and function have to cope with low internal oxygen. Plant Physiology 131, 1529–1543.
Phloem metabolism and function have to cope with low internal oxygen.CrossRef | 1:CAS:528:DC%2BD3sXjt1Sqsrs%3D&md5=bcb424eb5057486bb58770bb4ad5c94fCAS | 12692313PubMed |

Walker D (1987) ‘The use of oxygen electrode and fluorescence probes in simple measurements of photosynthesis.’ (Sheffield University Press: Sheffield)

Walker DA, Delieu T (1981) Polarographic measurement of photosynthetic oxygen evolution by leaf discs. New Phytologist 89, 165–178.
Polarographic measurement of photosynthetic oxygen evolution by leaf discs.CrossRef |

Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144, 307–313.
The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution.CrossRef | 1:CAS:528:DyaK2cXmsFShsbY%3D&md5=8fb203d13ab88e3c514b492bc7f98853CAS |

Wittmann C, Pfanz H (2007) Temperature dependency of bark photosynthesis in beech (Fagus sylvatica L.) and birch (Betula pendula Roth.) trees. Journal of Experimental Botany 58, 4293–4306.
Temperature dependency of bark photosynthesis in beech (Fagus sylvatica L.) and birch (Betula pendula Roth.) trees.CrossRef | 1:CAS:528:DC%2BD1cXitlymu74%3D&md5=afe382eac038118adc7401439fab17afCAS | 18182432PubMed |

Wittmann C, Pfanz H (2008a) General trait relationships in stems: a study on the performance and interrelationships of several functional and structural parameters involved in corticular photosynthesis. Physiologia Plantarum 134, 636–648.
General trait relationships in stems: a study on the performance and interrelationships of several functional and structural parameters involved in corticular photosynthesis.CrossRef | 1:CAS:528:DC%2BD1cXhsV2js7zL&md5=7891d950f66814c7d8f5729732b6a6bfCAS | 19000198PubMed |

Wittmann C, Pfanz H (2008b) Antitranspirant functions of stem periderms and their influence on corticular photosynthesis under drought stress. Trees 22, 187–196.
Antitranspirant functions of stem periderms and their influence on corticular photosynthesis under drought stress.CrossRef | 1:CAS:528:DC%2BD1cXjsF2gsLo%3D&md5=b9da319db26445ece20dff17389e9858CAS |

Wittmann C, Pfanz H, Loreto F, Centritto M, Pietrini F, Alessio G (2006) Light-induced reduction of carbon release from branches of birch trees: corticular photosynthesis, photorespiration or inhibition of mitochondrial respiration? Plant, Cell & Environment 29, 1149–1158.
Light-induced reduction of carbon release from branches of birch trees: corticular photosynthesis, photorespiration or inhibition of mitochondrial respiration?CrossRef | 1:CAS:528:DC%2BD28XlvFakurY%3D&md5=0f02dda7769851796cec0464032d0881CAS |



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