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

Costs and benefits of photosynthetic stems in desert species from southern California

Eleinis Ávila-Lovera https://orcid.org/0000-0003-3529-3600 A B D , Roxana Haro A , Exequiel Ezcurra A and Louis S. Santiago A C
+ Author Affiliations
- Author Affiliations

A Department of Botany and Plant Sciences, University of California, 2150 Batchelor Hall, Riverside, CA 92521, USA.

B Evolution, Ecology and Organismal Biology Graduate Program, Department of Evolution, Ecology and Organismal Biology, University of California, Riverside, CA 92521, USA.

C Smithsonian Tropical Research Institute, Apartado 0843-03092. Balboa, Ancon, Panama, Republic of Panama.

D Corresponding author. Email: eleinis.avilalovera@email.ucr.edu

Functional Plant Biology 46(2) 175-186 https://doi.org/10.1071/FP18203
Submitted: 22 March 2018  Accepted: 19 September 2018   Published: 24 October 2018

Abstract

Woody plants with green photosynthetic stems are common in dry woodlands with the possible advantages of extra carbon gain, re-assimilation of CO2, and high water-use efficiency. However, their green stem tissue may also incur greater costs of water loss when stomata are closed. Our study focussed on evaluating the costs and benefits of having green stems in desert plants, addressing the water-use efficiency hypothesis. We measured water status, carbon and water exchange, and carbon, nitrogen and oxygen isotopic composition of 15 species in a desert wash scrub in Joshua Tree National Park, California, USA. We found that all woody species that have green stems relied on their green stems as the sole organ for carbon assimilation for most of the study period. Green stems had similar photosynthetic rate (Amax), stomatal conductance (gs) and intrinsic water-use efficiency (WUEi) to leaves of the same species. However, Amax, gs and cuticular conductance (gmin) were higher in green stems than in leaves of non-green stemmed species. Carbon isotopic composition (δ13C) was similar in both leaves and green stems, indicating no difference in integrated long-term WUE. Our results raise questions about the possible trade-off between carbon gain and water loss through the cuticle in green stems and how this may affect plant responses to current and future droughts.

Additional keywords: carbon isotopes, gas exchange, oxygen isotopes, water relations, water-use efficiency.


References

Adams M, Strain B (1968) Photosynthesis in stems and leaves of Cercidium floridum – spring and summer diurnal field response and relation to temperature. Oecologia Plantarum 3, 285–297.

Adams MS, Strain BR, Ting IP (1967) Photosynthesis in chlorophyllus stem tissue and leaves of Cercidium floridum: accumulation and distribution of 14C from 14CO2. Plant Physiology 42, 1797–1799.
Photosynthesis in chlorophyllus stem tissue and leaves of Cercidium floridum: accumulation and distribution of 14C from 14CO2.Crossref | GoogleScholarGoogle Scholar |

Aschan G, Pfanz H (2003) Non-foliar photosynthesis – a strategy of additional carbon acquisition. Flora – Morphology, Distribution, Functional Ecology of Plants 198, 81–97.
Non-foliar photosynthesis – a strategy of additional carbon acquisition.Crossref | GoogleScholarGoogle Scholar |

Ávila E, De Almeida J, Tezara W (2014a) Comparación ecofisiológica y anatómica de los tejidos fotosintéticos de Cercidium praecox (Ruiz & Pav. ex Hook.) Harms (Fabaceae, Caesalpinioideae). Acta Botanica Venezuelica 37, 59–76.

Ávila E, Herrera A, Tezara W (2014b) Contribution of stem CO2 fixation to whole-plant carbon balance in nonsucculent species. Photosynthetica 52, 3–15.
Contribution of stem CO2 fixation to whole-plant carbon balance in nonsucculent species.Crossref | GoogleScholarGoogle Scholar |

Ávila-Lovera E, Ezcurra E (2016) Stem-succulent trees from the Old and New World tropics. In ‘Tropical tree physiology’. (Eds G Goldstein, LS Santiago) pp. 45–65. (Springer International Publishing: Basel, Switzerland)

Ávila-Lovera E, Tezara W (2018) Water-use efficiency is higher in green stems than in leaves of a tropical tree species. Trees
Water-use efficiency is higher in green stems than in leaves of a tropical tree species.Crossref | GoogleScholarGoogle Scholar |

Ávila-Lovera E, Zerpa AJ, Santiago LS (2017) Stem photosynthesis and hydraulics are coordinated in desert plant species. New Phytologist 216, 1119–1129.
Stem photosynthesis and hydraulics are coordinated in desert plant species.Crossref | GoogleScholarGoogle Scholar |

Batschelet E (1981) ‘Circular statistics in biology.’ (Academic Press: New York)

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 | GoogleScholarGoogle Scholar |

Bloemen J, Vergeynst LL, Overlaet-Michiels L, Steppe K (2016) How important is woody tissue photosynthesis in poplar during drought stress? Trees 30, 63–72.
How important is woody tissue photosynthesis in poplar during drought stress?Crossref | GoogleScholarGoogle Scholar |

Bossard CC, Rejmanek M (1992) Why have green stems? Functional Ecology 6, 197–205.
Why have green stems?Crossref | GoogleScholarGoogle Scholar |

Butler R (1962) Further examples of exact integration using the trapezoidal rule. The American Mathematical Monthly 69, 534–538.
Further examples of exact integration using the trapezoidal rule.Crossref | GoogleScholarGoogle Scholar |

Cannon WA (1908) ‘The topography of the chlorophyll apparatus in desert plants.’ (Carniege Institution of Science: Washington DC)

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 | GoogleScholarGoogle Scholar |

Cernusak L, Marshall J (2000) Photosynthetic refixation in branches of western white pine. Functional Ecology 14, 300–311.
Photosynthetic refixation in branches of western white pine.Crossref | GoogleScholarGoogle Scholar |

Cernusak LA, Marshall JD, Comstock JP, Balster NJ (2001) Carbon isotope discrimination in photosynthetic bark. Oecologia 128, 24–35.
Carbon isotope discrimination in photosynthetic bark.Crossref | GoogleScholarGoogle Scholar |

Cernusak LA, Tcherkez G, Keitel C, Cornwell WK, Santiago LS, Knohl A, Barbour MM, Williams DG, Reich PB, Ellsworth DS, Dawson TE, Griffiths HG, Farquhar GD, Wright IJ (2009) Why are non-photosynthetic tissues generally 13C enriched compared with leaves in C3 plants? Review and synthesis of current hypotheses. Functional Plant Biology 36, 199–213.
Why are non-photosynthetic tissues generally 13C enriched compared with leaves in C3 plants? Review and synthesis of current hypotheses.Crossref | GoogleScholarGoogle Scholar |

Chen JM, Black TA (1992) Defining leaf area index for non-flat leaves. Plant, Cell & Environment 15, 421–429.
Defining leaf area index for non-flat leaves.Crossref | GoogleScholarGoogle Scholar |

Comstock JP, Ehleringer JR (1988) Contrasting photosynthetic behavior in leaves and twigs of Hymenoclea salsola, a green-twigged warm desert shrub. American Journal of Botany 75, 1360–1370.
Contrasting photosynthetic behavior in leaves and twigs of Hymenoclea salsola, a green-twigged warm desert shrub.Crossref | GoogleScholarGoogle Scholar |

Comstock J, Ehleringer J (1990) Effect of variations in leaf size on morphology and photosynthetic rate of twigs. Functional Ecology 4, 209–221.
Effect of variations in leaf size on morphology and photosynthetic rate of twigs.Crossref | GoogleScholarGoogle Scholar |

Comstock JP, Ehleringer JR (1992) Correlating genetic variation in carbon isotopic composition with complex climatic gradients. Proceedings of the National Academy of Sciences of the United States of America 89, 7747–7751.
Correlating genetic variation in carbon isotopic composition with complex climatic gradients.Crossref | GoogleScholarGoogle Scholar |

Comstock JP, Cooper TA, Ehleringer JR (1988) Seasonal patterns of canopy development and carbon gain in nineteen warm desert shrub species. Oecologia 75, 327–335.
Seasonal patterns of canopy development and carbon gain in nineteen warm desert shrub species.Crossref | GoogleScholarGoogle Scholar |

De Baerdemaeker NJF, Salomón RL, De Roo L, Steppe K (2017) Sugars from woody tissue photosynthesis reduce xylem vulnerability to cavitation. New Phytologist 216, 720–727.
Sugars from woody tissue photosynthesis reduce xylem vulnerability to cavitation.Crossref | GoogleScholarGoogle Scholar |

Ehleringer JR, Comstock JP, Cooper TA (1987) Leaf–twig carbon isotope ratio differences in photosynthetic-twig desert shrubs. Oecologia 71, 318–320.
Leaf–twig carbon isotope ratio differences in photosynthetic-twig desert shrubs.Crossref | GoogleScholarGoogle Scholar |

Ehleringer JR, Phillips SL, Comstock JP (1992) Seasonal variation in the carbon isotopic composition of desert plants. Functional Ecology 6, 396–404.
Seasonal variation in the carbon isotopic composition of desert plants.Crossref | GoogleScholarGoogle Scholar |

Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78, 9–19.
Photosynthesis and nitrogen relationships in leaves of C3 plants.Crossref | GoogleScholarGoogle Scholar |

Evans JR, Santiago LS (2014) PrometheusWiki gold leaf protocol: gas exchange using LI-COR 6400. Functional Plant Biology 41, 223–226.
PrometheusWiki gold leaf protocol: gas exchange using LI-COR 6400.Crossref | GoogleScholarGoogle Scholar |

Farquhar GD, O’leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Functional Plant Biology 9, 121–137.

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

Garrec J-P, Barrois A (1992) Caracteristiques de la fixation et de la penetration corticale. Passage du phosphite dipotassique et de l’eau au travers d’ecorces isolees. Environmental and Experimental Botany 32, 11–23.
Caracteristiques de la fixation et de la penetration corticale. Passage du phosphite dipotassique et de l’eau au travers d’ecorces isolees.Crossref | GoogleScholarGoogle Scholar |

Gibson AC (1983) Anatomy of photosynthetic old stems of nonsucculent dicotyledons from North American deserts. Botanical Gazette 144, 347–362.
Anatomy of photosynthetic old stems of nonsucculent dicotyledons from North American deserts.Crossref | GoogleScholarGoogle Scholar |

Gibson AC (1996) ‘Structure-function relations of warm desert plants.’ (Springer: Berlin)

Gibson AC (1998) Photosynthetic organs of desert plants. Bioscience 48, 911–920.
Photosynthetic organs of desert plants.Crossref | GoogleScholarGoogle Scholar |

Groh B, Hübner C, Lendzian KJ (2002) Water and oxygen permeance of phellems isolated from trees: the role of waxes and lenticels. Planta 215, 794–801.
Water and oxygen permeance of phellems isolated from trees: the role of waxes and lenticels.Crossref | GoogleScholarGoogle Scholar |

Kerstiens G (1996) Cuticular water permeability and its physiological significance. Journal of Experimental Botany 47, 1813–1832.
Cuticular water permeability and its physiological significance.Crossref | GoogleScholarGoogle Scholar |

Kocurek M, Kornas A, Pilarski J, Tokarz K, Lüttge U, Miszalski Z (2015) Photosynthetic activity of stems in two Clusia species. Trees 29, 1029–1040.
Photosynthetic activity of stems in two Clusia species.Crossref | GoogleScholarGoogle Scholar |

Lulai EC, Orr PH (1994) Techniques for detecting and measuring developmental and maturational changes in tuber native periderm. American Potato Journal 71, 489–505.
Techniques for detecting and measuring developmental and maturational changes in tuber native periderm.Crossref | GoogleScholarGoogle Scholar |

Lulai EC, Glynn MT, Orr PH (1996) Cellular changes and physiological responses to tuber pressure-bruising. American Potato Journal 73, 197–209.
Cellular changes and physiological responses to tuber pressure-bruising.Crossref | GoogleScholarGoogle Scholar |

Mooney HA, Strain BR (1964) Bark photosynthesis in Ocotillo. Madrono 17, 230–233.

Nilsen ET (1992a) The influence of water stress on leaf and stem photosynthesis in Spartium junceum L. Plant, Cell & Environment 15, 455–461.
The influence of water stress on leaf and stem photosynthesis in Spartium junceum L.Crossref | GoogleScholarGoogle Scholar |

Nilsen ET (1992b) Partitioning growth and photosynthesis between leaves and stems during nitrogen limitation in Spartium junceum. American Journal of Botany 79, 1217–1223.
Partitioning growth and photosynthesis between leaves and stems during nitrogen limitation in Spartium junceum.Crossref | GoogleScholarGoogle Scholar |

Nilsen ET (1995) Stem photosynthesis: extent, patterns, and role in plant carbon economy. In ‘Plant stems: physiology and functional morphology.’ (Ed. BL Gartner) pp. 223–240. (Academic Press: San Diego, CA, USA)

Nilsen ET, Bao Y (1990) The influence of water stress on stem and leaf photosynthesis in Glycine max and Sparteum junceum (Leguminosae). American Journal of Botany 77, 1007–1015.
The influence of water stress on stem and leaf photosynthesis in Glycine max and Sparteum junceum (Leguminosae).Crossref | GoogleScholarGoogle Scholar |

Nilsen ET, Sharifi MR (1994) Seasonal acclimation of stem photosynthesis in woody legume species from the Mojave and Sonoran deserts of California. Plant Physiology 105, 1385–1391.
Seasonal acclimation of stem photosynthesis in woody legume species from the Mojave and Sonoran deserts of California.Crossref | GoogleScholarGoogle Scholar |

Nilsen E, Sharifi M (1997) Carbon isotopic composition of legumes with photosynthetic stems from mediterranean and desert habitats. American Journal of Botany 84, 1707–1713.
Carbon isotopic composition of legumes with photosynthetic stems from mediterranean and desert habitats.Crossref | GoogleScholarGoogle Scholar |

Nilsen ET, Meinzer FC, Rundel PW (1989) Stem photosynthesis in Psorothamnus spinosus (smoke tree) in the Sonoran Desert of California. Oecologia 79, 193–197.
Stem photosynthesis in Psorothamnus spinosus (smoke tree) in the Sonoran Desert of California.Crossref | GoogleScholarGoogle Scholar |

Nilsen ET, Sharifi MR, Rundel PW, Forseth IN, Ehleringer JR (1990) Water relations of stem succulent trees in north-central Baja California. Oecologia 82, 299–303.
Water relations of stem succulent trees in north-central Baja California.Crossref | GoogleScholarGoogle Scholar |

Nilsen ET, Rundel PW, Sharifi MR (1996) Diurnal gas exchange characteristics of two stem photosynthesizing legumes in relation to the climate at two contrasting sites in the California desert. Flora 191, 105–116.
Diurnal gas exchange characteristics of two stem photosynthesizing legumes in relation to the climate at two contrasting sites in the California desert.Crossref | GoogleScholarGoogle Scholar |

Osmond CB, Smith SD, Gui-Ying B, Sharkey TD (1987) 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.
Stem photosynthesis in a desert ephemeral, Eriogonum inflatum. Characterization of leaf and stem CO2 fixation and H2O vapor exchange under controlled conditions.Crossref | GoogleScholarGoogle Scholar |

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 | GoogleScholarGoogle Scholar |

Pivovaroff AL, Pasquini SC, De Guzman ME, Alstad KP, Stemke JS, Santiago LS (2016) Multiple strategies for drought survival among woody plant species. Functional Ecology 30, 517–526.
Multiple strategies for drought survival among woody plant species.Crossref | GoogleScholarGoogle Scholar |

R Core Team (2017) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at http://www.R-project.org/ [Verified 2 October 2018]

Sack L, Scoffoni C (2011) PrometheusWiki. Protocols in ecological and environmental plant physiology. (Minimum epidermal conductance (g min, a.k.a. cuticular conductance)). http://prometheuswiki.publish.csiro.au/tiki-index.php?page=Minimum+epidermal+conductance+%28gmin%2C+a.k.a.+cuticular+conductance%29. [Verified 2 October 2018]

Santiago LS, Bonal D, De Guzman ME, Ávila-Lovera E (2016) Drought survival strategies of tropical trees. In ‘Tropical tree physiology’. (Eds G Goldstein, LS Santiago) pp. 243–258. (Springer International Publishing, Cham, Switzerland)

Saveyn A, Steppe K, Ubierna N, Dawson TE (2010) Woody tissue photosynthesis and its contribution to trunk growth and bud development in young plants. Plant, Cell & Environment 33, 1949–1958.
Woody tissue photosynthesis and its contribution to trunk growth and bud development in young plants.Crossref | GoogleScholarGoogle Scholar |

Scheidegger Y, Saurer M, Bahn M, Siegwolf R (2000) Linking stable oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity: a conceptual model. Oecologia 125, 350–357.
Linking stable oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity: a conceptual model.Crossref | GoogleScholarGoogle Scholar |

Schmitz N, Egerton JJG, Lovelock CE, Ball MC (2012) Light-dependent maintenance of hydraulic function in mangrove branches: do xylary chloroplasts play a role in embolism repair?: Rapid report. New Phytologist 195, 40–46.
Light-dependent maintenance of hydraulic function in mangrove branches: do xylary chloroplasts play a role in embolism repair?: Rapid report.Crossref | GoogleScholarGoogle Scholar |

Schönherr J, Ziegler H (1980) Water permeability of Betula periderm. Planta 147, 345–354.
Water permeability of Betula periderm.Crossref | GoogleScholarGoogle Scholar |

Schreiber L, Franke R, Hartmann K (2005) Wax and suberin development of native and wound periderm of potato (Solanum tuberosum L.) and its relation to peridermal transpiration. Planta 220, 520–530.
Wax and suberin development of native and wound periderm of potato (Solanum tuberosum L.) and its relation to peridermal transpiration.Crossref | GoogleScholarGoogle Scholar |

Shumway RH, Stoffer DS (2017) ‘Time series analysis and its applications: with R examples.’ (4th edn) (Springer International Publishing: Basel, Switzerland)

Simbo DJ, Van den Bilcke N, Samson R (2013) Contribution of corticular photosynthesis to bud development in African baobab (Adansonia digitata L.) and Castor bean (Ricinus communis L.) seedlings. Environmental and Experimental Botany 95, 1–5.
Contribution of corticular photosynthesis to bud development in African baobab (Adansonia digitata L.) and Castor bean (Ricinus communis L.) seedlings.Crossref | GoogleScholarGoogle Scholar |

Smith SD, Nobel PS (1986) Deserts. In ‘Photosynthesis in contrasting environments’. (Eds NR Baker, SP Long) pp. 13–62. (Elsevier Science Publishers BV: Amsterdam, The Netherlands)

Smith SD, Osmond CB (1987) Stem photosynthesis in a desert ephemeral, Eriogonum inflatum. Morphology, stomatal conductance and water-use efficiency in field populations. Oecologia 72, 533–541.
Stem photosynthesis in a desert ephemeral, Eriogonum inflatum. Morphology, stomatal conductance and water-use efficiency in field populations.Crossref | GoogleScholarGoogle Scholar |

Szarek SR, Woodhouse RM (1978) Ecophysiological studies of Sonoran Desert plants. IV. Seasonal photosynthetic capacities of Acacia greggii and Cercidium microphyllum. Oecologia 37, 221–229.
Ecophysiological studies of Sonoran Desert plants. IV. Seasonal photosynthetic capacities of Acacia greggii and Cercidium microphyllum.Crossref | GoogleScholarGoogle Scholar |

Tezara W, Mitchell VJ, Driscoll SD, Lawlor DW (1999) Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401, 914–917.
Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP.Crossref | GoogleScholarGoogle Scholar |

Tinoco-Ojanguren C (2008) Diurnal and seasonal patterns of gas exchange and carbon gain contribution of leaves and stems of Justicia californica in the Sonoran Desert. Journal of Arid Environments 72, 127–140.
Diurnal and seasonal patterns of gas exchange and carbon gain contribution of leaves and stems of Justicia californica in the Sonoran Desert.Crossref | GoogleScholarGoogle Scholar |

Valladares F, Hernández LG, Dobarro I, García‐Pérez C, Sanz R, Pugnaire FI (2003) The ratio of leaf to total photosynthetic area influences shade survival and plastic response to light of green‐stemmed leguminous shrub seedlings. Annals of Botany 91, 577–584.
The ratio of leaf to total photosynthetic area influences shade survival and plastic response to light of green‐stemmed leguminous shrub seedlings.Crossref | GoogleScholarGoogle Scholar |

Vogt E, Schönherr J, Schmidt HW (1983) Water permeability of periderm membranes isolated enzymatically from potato tubers (Solanum tuberosum L.). Planta 158, 294–301.
Water permeability of periderm membranes isolated enzymatically from potato tubers (Solanum tuberosum L.).Crossref | GoogleScholarGoogle Scholar |

von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.
Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves.Crossref | GoogleScholarGoogle Scholar |