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

Limited photosynthetic plasticity in the leaf-succulent CAM plant Agave angustifolia grown at different temperatures

Joseph A. M. Holtum A B C and Klaus Winter B
+ Author Affiliations
- Author Affiliations

A Tropical Biology, James Cook University, Townsville, Qld 4811, Australia.

B Smithsonian Tropical Research Institute, PO Box 0843-03092, Balboa, Ancon, Republic of Panama.

C Corresponding author. Email: joseph.holtum@jcu.edu.au

Functional Plant Biology 41(8) 843-849 https://doi.org/10.1071/FP13284
Submitted: 30 September 2013  Accepted: 19 February 2014   Published: 28 April 2014

Abstract

In Agave angustifolia Haw., a leaf-succulent constitutive crassulacean acid metabolism (CAM) plant of tropical Panama, we tested whether nocturnal CO2 uptake and growth were reduced at night temperatures above 20°C. Unlike some CAM model species from habitats with pronounced day-night temperature variations, in A. angustifolia temperature affected little the relative contributions of CAM and C3 photosynthesis to growth. In plants grown under 12 h light/dark regimes of 25/17, 30/22 and 35/27°C, biomass increased with temperature. Maintaining day temperature at 35°C and reducing night temperature from 27 to 17°C markedly lowered growth, a reduction partially reversed when roots were heated to 27°C. Across all treatments, whole-shoot δ13C values ranged between –14.6 and –13.2 ‰, indicating a stable proportion of CO2 was fixed at night, between 75 and 83%. Nocturnal acidification reflected growth, varying between 339 and 393 μmol H+ g–1 fresh mass and 63–87 μmol H+ cm–2. In outdoor open-top chambers, warming the air 3°C above ambient at night did not reduce biomass accumulation. The persistence of a high capacity for nocturnal CO2 fixation at the expense of a limited capacity for switching between C3 and CAM probably makes this Agave, and others like it, potential species for biomass production in seasonally-dry landscapes.

Additional keywords: biofuel, C3 photosynthesis, climate change, crassulacean acid metabolism, open-top chamber.


References

Antony E, Borland AM (2009) The role and regulation of sugar transporters in plants with crassulacean acid metabolism. Progress in Botany 70, 127–143.
The role and regulation of sugar transporters in plants with crassulacean acid metabolism.Crossref | GoogleScholarGoogle Scholar |

Borland AM, Dodd AN (2002) Carbohydrate partitioning in crassulacean acid metabolism plants: reconciling potential conflicts of interest. Functional Plant Biology 29, 707–716.
Carbohydrate partitioning in crassulacean acid metabolism plants: reconciling potential conflicts of interest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVWqur4%3D&md5=c0145a82d8cb3496af1fd38edfd63e97CAS |

Borland AM, Griffiths H, Hartwell J, Smith JAC (2009) Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands. Journal of Experimental Botany 60, 2879–2896.
Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosFWjuro%3D&md5=36d98c84e560d71e34ae292c63c90e26CAS | 19395392PubMed |

Borland AM, Zambrano VAB, Ceusters J, Shorrock K (2011) The photosynthetic plasticity of crassulacean acid metabolism: an evolutionary innovation for sustainable productivity in a changing world. New Phytologist 191, 619–633.
The photosynthetic plasticity of crassulacean acid metabolism: an evolutionary innovation for sustainable productivity in a changing world.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFWjtL%2FJ&md5=bd41ca1752f3aa12de8069cb0bfca38fCAS | 21679188PubMed |

Brandon PC (1967) Temperature features of enzymes affecting crassulacean acid metabolism. Plant Physiology 42, 977–984.
Temperature features of enzymes affecting crassulacean acid metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXks1WjurY%3D&md5=bce70a74c4f27f8141aca9c0ed4a8f5eCAS | 16656606PubMed |

Campbell JE, Lobell DB, Genova RC, Field CB (2008) The global potential of bioenergy on abandoned agriculture lands. Environmental Science & Technology 42, 5791–5794.
The global potential of bioenergy on abandoned agriculture lands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXns1Clsbc%3D&md5=ee481626e91c65bd74891ac33cbac1b0CAS |

Cernusak L, Winter K, Martinez C, Correa E, Aranda J, Garcia M, Jaramillo C, Turner BL (2011) Responses of legume versus nonlegume tropical tree seedlings to elevated CO2 concentration. Plant Physiology 157, 372–385.
Responses of legume versus nonlegume tropical tree seedlings to elevated CO2 concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Sit7zF&md5=8434edc7d48c4243967cb6e27b1125b4CAS | 21788363PubMed |

Chambers D, Holtum JAM (2010) ‘Feasibility of Agave as a feedstock for biofuel production in Australia.’ (Rural Industries Research and Development Corporation: Canberra)

Cheesman A, Winter K (2013) Elevated night-time temperatures increase growth in seedlings of two tropical pioneer tree species. New Phytologist 197, 1185–1192.
Elevated night-time temperatures increase growth in seedlings of two tropical pioneer tree species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitVOju7g%3D&md5=4248669d77227c1ffbe3ffc06b0824c0CAS | 23278464PubMed |

Colunga-García Marín P, Coello-Coello J, Eguiarte LE, Piñero D (1999) Isozymatic variation and phylogenetic relationships between henequén (Agave fourcroydes) and its wild ancestor A. angustifolia (Agavaceae). American Journal of Botany 86, 115–123.
Isozymatic variation and phylogenetic relationships between henequén (Agave fourcroydes) and its wild ancestor A. angustifolia (Agavaceae).Crossref | GoogleScholarGoogle Scholar |

Crayn DM, Winter K, Smith JAC (2004) Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae. Proceedings of the National Academy of Sciences of the United States of America 101, 3703–3708.
Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXisFWmtb8%3D&md5=5ad4a72f81200f9d06c85978d2862139CAS | 14982989PubMed |

Davis SC, Dohleman FG, Long SP (2011) The global potential for Agave as a biofuel feedstock. Global Change Biology - Bioenergy 3, 68–78.
The global potential for Agave as a biofuel feedstock.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXps12guw%3D%3D&md5=0524db72afd5e0d8729c5e1882ac8c87CAS |

De Vries H (1884) Über die periodische Säurebildung der Fettpflanzen. Botanische Zeitung 42, 339–344.

Dodd AN, Borland AM, Haslam RP, Griffiths H, Maxwell K (2002) Crassulacean acid metabolism: plastic, fantastic. Journal of Experimental Botany 53, 569–580.
Crassulacean acid metabolism: plastic, fantastic.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitlCksro%3D&md5=a266605010143e76fb2022d954b1967dCAS | 11886877PubMed |

Gentry HS (1982) ‘Agaves of continental North America.’ (University of Arizona Press: Tucson, AR, USA)

Gouws LM, Osmond CB, Schurr U, Walter A (2005) Distinctive diel growth cycles in leaves and cladodes of CAM plants: differences from C3 plants and putative interactions with substrate availability, turgor and cytoplasmic pH. Functional Plant Biology 32, 421–428.
Distinctive diel growth cycles in leaves and cladodes of CAM plants: differences from C3 plants and putative interactions with substrate availability, turgor and cytoplasmic pH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1eiu7Y%3D&md5=39bb39cf68f4118bad0b3207f026be14CAS |

Griffiths HG, Smith JAC (1983) Photosynthetic pathways in the Bromeliaceae of Trinidad: relations between life-forms, habitat preference and occurrence of CAM. Oecologia 60, 176–184.

Haider MS, Barnes JD, Cushman JC, Borland AM (2012) A CAM- and starch-deficient mutant of the facultative CAM species Mesembryanthemum crystallinum reconciles sink demands by repartitioning carbon during acclimation to salinity. Journal of Experimental Botany 63, 1985–1996.
A CAM- and starch-deficient mutant of the facultative CAM species Mesembryanthemum crystallinum reconciles sink demands by repartitioning carbon during acclimation to salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjslehsLo%3D&md5=0f1d330a36ff0f7d45adc25b442917f6CAS | 22219316PubMed |

Holtum JAM, Winter K (1999) Degrees of crassulacean acid metabolism in tropical epiphytic and lithophytic ferns. Australian Journal of Plant Physiology 26, 749–757.
Degrees of crassulacean acid metabolism in tropical epiphytic and lithophytic ferns.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1Ogtw%3D%3D&md5=c17b1ac6ad2db4e31ffb03a60268eb9aCAS |

Holtum JAM, Aranda J, Virgo A, Winter K (2004) δ13C values and crassulacean acid metabolism in Clusia species from Panama. Trees 18, 658–668.
δ13C values and crassulacean acid metabolism in Clusia species from Panama.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVKqsbY%3D&md5=9bead4da9582044754bb7d46a64a1811CAS |

Holtum JAM, Chambers D, Morgan T, Tan DY (2011) Agave as a biofuel feedstock in Australia. Global Change Biology – Bioenergy 3, 58–67.
Agave as a biofuel feedstock in Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXps12gug%3D%3D&md5=b447389836a805dc437982716f5f7fbbCAS |

Kaplan A, Gale J, Poljakoff-Mayber A (1976) Resolution of net dark fixation of carbon dioxide into its respiration and gross fixation components in Bryophyllum daigremontianum. Journal of Experimental Botany 27, 220–230.
Resolution of net dark fixation of carbon dioxide into its respiration and gross fixation components in Bryophyllum daigremontianum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XktFOhs74%3D&md5=d342a1ab860958fde51c9009e994ad13CAS |

Kluge M, Ting IP (1978) ‘Crassulacean acid metabolism. Analysis of an ecological adaptation.’ (Springer-Verlag: Berlin)

Königer M, Winter K (1993) Growth and photosynthesis of Gossypium hirsutum L. at high photon flux densities: effects of soil temperatures and nocturnal air temperatures. Agronomie 13, 423–431.
Growth and photosynthesis of Gossypium hirsutum L. at high photon flux densities: effects of soil temperatures and nocturnal air temperatures.Crossref | GoogleScholarGoogle Scholar |

Medina E, Osmond CB (1981) Temperature dependence of dark CO2 fixation and acid accumulation in Kalanchoe daigremontiana. Australian Journal of Plant Physiology 8, 641–649.

Milburn TR, Pearson DJ, Ndegwe NA (1968) Crassulacean acid metabolism under natural tropical conditions. New Phytologist 67, 883–897.
Crassulacean acid metabolism under natural tropical conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1MXhtFansbs%3D&md5=1c7a19bd6950596ce998c094d5e9ef2bCAS |

Neales TF (1973a) The effect of night temperature on CO2 assimilation, transpiration, and water use efficiency in Agave americana L. Australian Journal of Biological Sciences 26, 705–714.

Neales TF (1973b) The effect of night temperature on the assimilation of carbon dioxide by mature pineapple plants, Ananas comosus (L.) Merr. Australian Journal of Biological Sciences 26, 539–546.

Neales TF, Sale PJM, Meyer CP (1980) Carbon dioxide assimilation by pineapple plants, Ananas comosus (L.) Merr. Effects of variation of the day/night temperature regime. Australian Journal of Plant Physiology 7, 375–385.
Carbon dioxide assimilation by pineapple plants, Ananas comosus (L.) Merr. Effects of variation of the day/night temperature regime.Crossref | GoogleScholarGoogle Scholar |

Nobel PS (1984) Productivity of Agave deserti: measurement by dry weight and monthly prediction using physiological responses to environmental parameters. Oecologia 64, 1–7.
Productivity of Agave deserti: measurement by dry weight and monthly prediction using physiological responses to environmental parameters.Crossref | GoogleScholarGoogle Scholar |

Nobel PS (1985) PAR, water, and temperature limitations on the productivity of cultivated Agave fourcroydes (henequen). Journal of Applied Ecology 22, 157–173.
PAR, water, and temperature limitations on the productivity of cultivated Agave fourcroydes (henequen).Crossref | GoogleScholarGoogle Scholar |

Nobel PS (1988) ‘Environmental biology of agaves and cacti.’ (Cambridge University Press: Cambridge)

Nobel PS (1989) A nutrient index quantifying productivity of agaves and cacti. Journal of Applied Ecology 26, 635–645.
A nutrient index quantifying productivity of agaves and cacti.Crossref | GoogleScholarGoogle Scholar |

Nobel PS (1991) Environmental productivity indices and productivity for Opuntia ficus-indica under current and elevated atmospheric CO2 levels. Plant, Cell & Environment 14, 637–646.
Environmental productivity indices and productivity for Opuntia ficus-indica under current and elevated atmospheric CO2 levels.Crossref | GoogleScholarGoogle Scholar |

Nobel PS, Hartsock TL (1978) Resistance analysis of nocturnal carbon dioxide uptake by a crassulacean acid metabolism plant, Agave deserti. Plant Physiology 61, 510–514.
Resistance analysis of nocturnal carbon dioxide uptake by a crassulacean acid metabolism plant, Agave deserti.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnht1yksQ%3D%3D&md5=25e51ca4a94f07b1269f17558d56f8b8CAS | 16660695PubMed |

Nobel PS, Hartsock TL (1981) Shifts in the optimal temperature for nocturnal CO2 uptake caused by changes in growth temperature for cacti and agaves. Physiologia Plantarum 53, 523–527.
Shifts in the optimal temperature for nocturnal CO2 uptake caused by changes in growth temperature for cacti and agaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XkvFagsw%3D%3D&md5=b0eb9b33890b493f238713a4970bca72CAS |

Nobel PS, McDaniel RG (1988) Low-temperature tolerances, nocturnal acid accumulation, and biomass increases for seven species of Agave. Journal of Arid Environments 15, 147–155.

Nobel PS, Meyer SE (1985) Field productivity of a CAM plant, Agave salmiana, estimated using daily acidity changes under various environmental conditions. Physiologia Plantarum 65, 397–404.
Field productivity of a CAM plant, Agave salmiana, estimated using daily acidity changes under various environmental conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XosFCqsA%3D%3D&md5=9193d8ce09cf955364ca02cfe99ea7eaCAS |

Nobel PS, Quero E (1986) Environmental productivity indices for a Chihuahuan Desert CAM plant, Agave lechuguilla. Ecology 67, 1–11.
Environmental productivity indices for a Chihuahuan Desert CAM plant, Agave lechuguilla.Crossref | GoogleScholarGoogle Scholar |

Nobel PS, Valenzuela AG (1987) Environmental responses and productivity of the CAM plant, Agave tequilana. Agricultural and Forest Meteorology 39, 319–334.
Environmental responses and productivity of the CAM plant, Agave tequilana.Crossref | GoogleScholarGoogle Scholar |

Osmond CB (1978) Crassulacean acid metabolism: a curiosity in context. Annual Review of Plant Physiology 29, 379–414.
Crassulacean acid metabolism: a curiosity in context.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXktl2gt7c%3D&md5=9785c7e2f087c48cf736b1b90a733142CAS |

Owen NA, Griffiths H (2013) Marginal land bioethanol yield potential of four crassulacean acid metabolism candidates (Agave fourcroydes, Agave salmiana, Agave tequilana and Opuntia ficus-indica) in Australia. Global Change Biology - Bioenergy
Marginal land bioethanol yield potential of four crassulacean acid metabolism candidates (Agave fourcroydes, Agave salmiana, Agave tequilana and Opuntia ficus-indica) in Australia.Crossref | GoogleScholarGoogle Scholar |

Pimienta-Barrios E, Robles-Murguia C, Nobel PS (2001) Net CO2 uptake for Agave tequilana in a warm and a temperate environment. Biotropica 33, 312–318.

Queiroz O (1966) Sur le métabolisme acide des Crassulacées.II. Action à long terme de la température de jour sur les variations de la teneur en acide malique en jours courts. Physiologie Vegetale 4, 323–339.

Silvera K, Santiago LS, Winter K (2005) Distribution of crassulacean acid metabolism in orchids of Panama: evidence of selection for weak and strong modes. Functional Plant Biology 32, 397–407.
Distribution of crassulacean acid metabolism in orchids of Panama: evidence of selection for weak and strong modes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1ehsrw%3D&md5=c4a6755460c368bb72e9ca19dc71115cCAS |

Szarek SR, Ting IP (1974) Seasonal patterns of acid metabolism and gas exchange in Opuntia basilaris. Plant Physiology 54, 76–81.
Seasonal patterns of acid metabolism and gas exchange in Opuntia basilaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXls1KnsLY%3D&md5=0ca07bd04487c44e9796bda84cf6efafCAS | 16658842PubMed |

Winter K (1985) Crassulacean acid metabolism. In ‘Photosynthetic mechanisms and the environment’. (Eds J Barber, NR Baker) pp. 329–387. (Elsevier: Amsterdam)

Winter K, Holtum JAM (2002) How closely do the δ13C values of crassulacean acid metabolism plants reflect the proportion of CO2 fixed during day and night? Plant Physiology 129, 1843–1851.
How closely do the δ13C values of crassulacean acid metabolism plants reflect the proportion of CO2 fixed during day and night?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xmtl2gtLs%3D&md5=75d62bf651cc3e5d56ee892462cd357cCAS | 12177497PubMed |

Winter K, Holtum JAM (2014) Facultative crassulacean acid metabolism (CAM) plants: powerful tools for unravelling the functional elements of CAM photosynthesis. Journal of Experimental Botany
Facultative crassulacean acid metabolism (CAM) plants: powerful tools for unravelling the functional elements of CAM photosynthesis.Crossref | GoogleScholarGoogle Scholar | 24648568PubMed |

Winter K, Aranda J, Holtum JAM (2005) Carbon isotope composition and water use efficiency in plants with crassulacean acid metabolism. Functional Plant Biology 32, 381–388.
Carbon isotope composition and water use efficiency in plants with crassulacean acid metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1ehsr0%3D&md5=758e47850eab712a42eda0174ea5d97cCAS |

Winter K, Garcia M, Holtum JAM (2014) Nocturnal versus diurnal CO2 uptake: how flexible is Agave angustifolia? Journal of Experimental Botany
Nocturnal versus diurnal CO2 uptake: how flexible is Agave angustifolia?Crossref | GoogleScholarGoogle Scholar | 24648568PubMed |

Wong SC, Hew CS (1976) Diffusive resistance, titratable acidity and CO2 fixation in two tropical epiphytic ferns. American Fern Journal 66, 121–124.
Diffusive resistance, titratable acidity and CO2 fixation in two tropical epiphytic ferns.Crossref | GoogleScholarGoogle Scholar |

Yamori W, Hikosaka K, Way DA (2014) Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynthesis Research 119, 101–117.
Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFKgsLrP&md5=e0c57aacfc98f87f54e46efbabfbce73CAS | 23801171PubMed |

Zhu J, Goldstein G, Bartholomew DP (1999) Gas exchange and carbon isotope composition of Ananas comosus in response to elevated CO2 and temperature. Plant, Cell & Environment 22, 999–1007.
Gas exchange and carbon isotope composition of Ananas comosus in response to elevated CO2 and temperature.Crossref | GoogleScholarGoogle Scholar |

Zotz G, Winter K (1994a) Annual carbon balance and nitrogen-use efficiency in tropical C3 and CAM epiphytes. New Phytologist 126, 481–492.
Annual carbon balance and nitrogen-use efficiency in tropical C3 and CAM epiphytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXltVCiur0%3D&md5=e9a07724dc56de397e8391c32d862905CAS |

Zotz G, Winter K (1994b) A one-year study on carbon, water and nutrient relationships in a tropical C3-CAM hemi-epiphyte, Clusia uvitana Pittier. New Phytologist 127, 45–60.
A one-year study on carbon, water and nutrient relationships in a tropical C3-CAM hemi-epiphyte, Clusia uvitana Pittier.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlslGhtrw%3D&md5=12a9559af2cb6153ee65b71d05fd08bfCAS |