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

Induction and reversal of crassulacean acid metabolism in Calandrinia polyandra: effects of soil moisture and nutrients

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

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

B School of Marine and Tropical Biology, James Cook University, Townsville, Qld 4811, Australia.

C Corresponding author. Email: winterk@si.edu

Functional Plant Biology 38(7) 576-582 https://doi.org/10.1071/FP11028
Submitted: 25 January 2011  Accepted: 28 April 2011   Published: 12 July 2011

Abstract

Calandrinia polyandra Benth. (Montiaceae), an annual succulent herb endemic to Australia, is an exemplary facultative crassulacean acid metabolism (CAM) plant as demonstrated by continuous whole-plant lifetime CO2 exchange measurements under controlled conditions in the laboratory. Reduced soil water availability induced a shift from solely daytime CO2 fixation to dark CO2 fixation. The shift from C3 photosynthesis to CAM was reversible either upon rewatering alone, or upon a combination of rewatering and addition of nutrients. These observations highlight the role of edaphic conditions in controlling CAM expression in a plant that has the option of fixing CO2 either during the day or during the night, providing further evidence that this extreme form of photosynthetic plasticity is primarily controlled by the environment rather than plant ontogeny. The stimulating effect of soil nutrients on CO2 fixation in the light and its negative effect on dark CO2 fixation have not been described previously and deserve further attention. In the most widely used CAM model system, the halophytic Mesembryanthemum crystallinum L., CAM is typically induced by high salinity, and some metabolic responses may be CAM-unrelated and related to salt stress per se. C. polyandra could be an excellent complementary system for studying the biochemical and molecular foundations of CAM because drought stress elicits a complete C3 to CAM transition.

Additional keywords: constitutive CAM, Parakeelya, Portulacaceae.


References

Applequist WL, Wallace RS (2001) Phylogeny of the portulacaceous cohort based on ndhF sequence data. Systematic Botany 26, 406–419.

Australia’s Virtual Herbarium (2011) Council of Heads of Australasian Herbaria Inc.: Canberra. Available at http://avh.rbg.vic.gov.au/avh/ [Verified 22 January 2011].

Bentham G (1863) ‘Flora Australiensis: a description of the plants of the Australian territory. Volume 1: Ranunculaceae to Anacardiaceae.’ (Lovell Reeve and Co: London)

Carolin RC (1987) A review of the family Portulacaceae. Australian Journal of Botany 35, 383–412.
A review of the family Portulacaceae.Crossref | GoogleScholarGoogle Scholar |

Dampier WA (1703) ‘A voyage to New Holland etc in the year 1699.’ (James Knapton: London)

Guralnick LJ, Jackson MD (1993) Crassulacean acid metabolism activity in the family Portulacaceae. Plant Physiology 102, 139

Guralnick LJ, Cline A, Smith M, Sage RF (2008) Evolutionary physiology: the extent of C4 and CAM photosynthesis in the genera Anacampseros and Grahamia of the Portulacaceae. Journal of Experimental Botany 59, 1735–1742.
Evolutionary physiology: the extent of C4 and CAM photosynthesis in the genera Anacampseros and Grahamia of the Portulacaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtlelt7Y%3D&md5=65d616386923de5ded5161636e3eb600CAS | 18440927PubMed |

Herrera A (2009) Crassulacean acid metabolism and fitness under water deficit stress: if not for carbon gain, what is facultative CAM good for? Annals of Botany 103, 645–653.
Crassulacean acid metabolism and fitness under water deficit stress: if not for carbon gain, what is facultative CAM good for?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVGmsrw%3D&md5=41de9542f622e4c6f472966fc64c8062CAS | 18708641PubMed |

Hershkovitz MA (1991) Phylogenetic assessment and revised circumscription of Cistanthe Spach (Portulacaceae). Annals of the Missouri Botanical Garden 78, 1009–1021.
Phylogenetic assessment and revised circumscription of Cistanthe Spach (Portulacaceae).Crossref | GoogleScholarGoogle Scholar |

Hershkovitz MA (1993a) Revised circumscriptions and subgeneric taxonomies of Calandrinia and Montiopsis (Portulacaceae) with notes on phylogeny of the portulacaceous alliance. Annals of the Missouri Botanical Garden 80, 333–365.
Revised circumscriptions and subgeneric taxonomies of Calandrinia and Montiopsis (Portulacaceae) with notes on phylogeny of the portulacaceous alliance.Crossref | GoogleScholarGoogle Scholar |

Hershkovitz MA (1993b) Leaf morphology of Calandrinia Kunth and Montiopsis Kuntze (Portulacaceae). Annals of the Missouri Botanical Garden 80, 366–396.
Leaf morphology of Calandrinia Kunth and Montiopsis Kuntze (Portulacaceae).Crossref | GoogleScholarGoogle Scholar |

Hershkovitz MA (1998) Parakeelya: a new genus segregated from Calandrinia (Portulacaceae). Phytologia 84, 98–106.

Hershkovitz MA, Zimmer EA (1997) On the evolutionary origins of the cacti. Taxon 46, 217–242.
On the evolutionary origins of the cacti.Crossref | GoogleScholarGoogle Scholar |

Holtum JAM, Winter K (2003) Photosynthetic CO2 uptake in seedlings of two tropical tree species exposed to oscillating elevated concentrations of CO2. Planta 218, 152–158.
Photosynthetic CO2 uptake in seedlings of two tropical tree species exposed to oscillating elevated concentrations of CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovV2ltLg%3D&md5=427c469047ddba9f42be4b22b5bbe874CAS | 12905026PubMed |

Holtum JAM, Aranda J, Virgo A, Gehrig HH, Winter K (2004) δ13C values and crassulacean acid metabolism in Clusia species from Panama. Trees – Structure and Function 18, 658–668.

Holtum JAM, Winter K, Weeks MA, Sexton TR (2007) Crassulacean acid metabolism in the ZZ plant, Zamioculcas zamiiofolia (Araceae). American Journal of Botany 94, 1670–1676.
Crassulacean acid metabolism in the ZZ plant, Zamioculcas zamiiofolia (Araceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlaqu77E&md5=59591f270ea0c6a7153e1d97603d99feCAS | 21636363PubMed |

Kapitany A (2007) ‘Australian succulent plants.’ (Kapitany Concepts: Boronia, Australia)

Kapitany A (2010) The Australian Calandrinia. Spinette July 2010. (The Cactus and Succulent Society of Australia Inc.: Braeside)

Kluge M, Ting IP (1978) ‘Crassulacean acid metabolism.’ (Springer-Verlag: Berlin)

Koch K, Kennedy RA (1980) Characteristics of crassulacean acid metabolism in the succulent C4 dicot, Portulaca oleracea L. Plant Physiology 65, 193–197.
Characteristics of crassulacean acid metabolism in the succulent C4 dicot, Portulaca oleracea L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhsVemsrw%3D&md5=40913bb22539384c8fd250ca78cfb9a0CAS | 16661159PubMed |

Lüttge U (1999) One morphotype, three physiotypes: sympatric species of Clusia with obligate C3 photosynthesis, obligate CAM and C3-CAM intermediate behaviour. Plant Biology 1, 138–148.
One morphotype, three physiotypes: sympatric species of Clusia with obligate C3 photosynthesis, obligate CAM and C3-CAM intermediate behaviour.Crossref | GoogleScholarGoogle Scholar |

Lüttge U (2007) ‘Clusia: a woody neotropical genus of remarkable plasticity and diversity.’ (Springer: Berlin)

Martin CE, Zee AK (1983) C3 photosynthesis and crassulacean acid metabolism in a Kansas rock outcrop succulent, Talinum calycinum Engelm (Portulacaceae). Plant Physiology 73, 718–723.
C3 photosynthesis and crassulacean acid metabolism in a Kansas rock outcrop succulent, Talinum calycinum Engelm (Portulacaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2cXitVKntA%3D%3D&md5=9d1dc7c33185e17b9115926ef6342009CAS | 16663289PubMed |

McNeill J (1974) Synopsis of a revised classification of the Portulacaceae. Taxon 23, 725–728.
Synopsis of a revised classification of the Portulacaceae.Crossref | GoogleScholarGoogle Scholar |

Melville R (1959) The identity of Calandrinia polyandra Bentham. Kew Bulletin 13, 400–401.
The identity of Calandrinia polyandra Bentham.Crossref | GoogleScholarGoogle Scholar |

Mooney HA, Troughton JH, Berry JA (1974) Arid climates and photosynthetic systems. Carnegie Institution Yearbook 73, 793–805.

Mooney HA, Troughton JH, Berry JA (1977) Carbon isotope ratio measurements of succulent plants in southern Africa. Oecologia 30, 295–305.
Carbon isotope ratio measurements of succulent plants in southern Africa.Crossref | GoogleScholarGoogle Scholar |

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

Nyananyo BL (1990) Tribal and generic relationship in the Portulacaceae (Centrospermae). Feddes Repertorium 101, 237–241.
Tribal and generic relationship in the Portulacaceae (Centrospermae).Crossref | GoogleScholarGoogle Scholar |

Nyffeler R, Eggli U (2010a) Disintegrating Portulacaceae: a new familial classification of the suborder Portulacineae (Caryophyllales) based on molecular and morphological data. Taxon 59, 227–240.

Nyffeler R, Eggli U (2010b) An up-to-date familial and suprafamilial classification of succulent plants. Bradleya 28, 125–144.

Obbens FJ (2006) A review of the tuberous Calandrinia species (section Tuberosae), including three new species for Western Australia. Nuytsia 16, 95–115.

Pate JS, Dixon K (1981) Plants with fleshy underground storage organs. In ‘The biology of Australian plants’. (Eds JS Pate, AJ McComb) pp. 181–215. (University of Western Australia Press: Perth)

Smirnoff N (1996) Regulation of crassulacean acid metabolism by water status in the C3/CAM intermediate Sedum telephium. In ‘Crassulacean acid metabolism’. (Eds K Winter, JAC Smith) pp. 176–191. (Springer-Verlag: Berlin)

Smith JAC, Winter K (1996). Taxonomic distribution of crassulacean acid metabolism. In ‘Crassulacean acid metabolism.’ (Eds K Winter, JAC Smith) pp. 427–436. (Springer-Verlag: Berlin)

Ting IP, Hanscom Z (1977) Induction of acid metabolism in Portulacaria afra. Plant Physiology 59, 511–514.
Induction of acid metabolism in Portulacaria afra.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXhsFars7o%3D&md5=fc1cee8cc1f200f27380d2e21a9213d3CAS | 16659882PubMed |

Troughton JH, Card KA, Hendy CH (1974) Photosynthetic pathways and carbon isotope discrimination by plants. Carnegie Institution Yearbook 73, 768–780.

Vernon DM, Ostrem JA, Schmitt JM, Bohnert HJ (1988) PEPCase transcript levels in Mesembryanthemum crystallinum decline rapidly upon relief from salt stress. Plant Physiology 86, 1002–1004.
PEPCase transcript levels in Mesembryanthemum crystallinum decline rapidly upon relief from salt stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXktVCjtbo%3D&md5=e07c3a02c59fc0a1b0f7197e47123445CAS | 16666021PubMed |

Veste M, Herppich WB, von Willert DJ (2001) Variability of CAM in leaf-deciduous succulents from the Succulent Karoo (South Africa). Basic and Applied Ecology 2, 283–288.
Variability of CAM in leaf-deciduous succulents from the Succulent Karoo (South Africa).Crossref | GoogleScholarGoogle Scholar |

von Willert DJ, Eller BM, Werger MJA, Brinckmann E, Ihlenfeldt HD (1992) ‘Life strategies of succulent plants in deserts, with special reference to the Namib desert.’ (University of Cambridge Press: Cambridge, UK)

Winter K (1974) NaCl-induzierter Crassulaceen-Säurestoffwechsel bei der Salzpflanze Mesembryanthemum crystallinum. Oecologia 15, 383–392.
NaCl-induzierter Crassulaceen-Säurestoffwechsel bei der Salzpflanze Mesembryanthemum crystallinum.Crossref | GoogleScholarGoogle Scholar |

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 (2005) The effects of salinity, crassulacean acid metabolism and plant age on the carbon isotope composition of Mesembryanthemum crystallinum L., a halophytic C3-CAM species. Planta 222, 201–209.
The effects of salinity, crassulacean acid metabolism and plant age on the carbon isotope composition of Mesembryanthemum crystallinum L., a halophytic C3-CAM species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVektr3F&md5=a06676a2dc6fd7a8fdeb6f743dccd62dCAS | 15968514PubMed |

Winter K, Holtum JAM (2007) Environment or development? Lifetime net CO2 exchange and control of the expression of crassulacean acid metabolism in Mesembryanthemum crystallinum. Plant Physiology 143, 98–107.
Environment or development? Lifetime net CO2 exchange and control of the expression of crassulacean acid metabolism in Mesembryanthemum crystallinum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpt1Ogtw%3D%3D&md5=6776ff65722824edb3fb16521d3eaacdCAS | 17056756PubMed |

Winter K, Troughton JH (1978) Carbon assimilation pathways in Mesembryanthemum nodiflorum L. under natural conditions. Zeitschrift für Pflanzenphysiologie 88, 153–162.

Winter K, von Willert DJ (1972) NaCl-induzierter Crassulaceensäurestoffwechsel bei Mesembryanthemum crystallinum. Zeitschrift für Pflanzenphysiologie 67, 166–170.

Winter K, Lüttge U, Winter E, Troughton JH (1978) Seasonal shift from C3 photosynthesis to crassulacean acid metabolism in Mesembryanthemum crystallinum growing in its natural environment. Oecologia 34, 225–237.
Seasonal shift from C3 photosynthesis to crassulacean acid metabolism in Mesembryanthemum crystallinum growing in its natural environment.Crossref | GoogleScholarGoogle Scholar |

Winter K, Osmond CB, Pate JS (1981) Coping with salinity. In ‘The biology of Australian plants’. (Eds JS Pate, AJ McComb) pp. 88–113. (University of Western Australia Press: Perth)

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=9b1a020631970e4b9dfb9d9754945168CAS |

Winter K, Garcia M, Holtum JAM (2008) On the nature of facultative and constitutive CAM: environmental and developmental control of CAM expression during early growth of Clusia, Kalanchoë, and Opuntia. Journal of Experimental Botany 59, 1829–1840.
On the nature of facultative and constitutive CAM: environmental and developmental control of CAM expression during early growth of Clusia, Kalanchoë, and Opuntia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtleltrs%3D&md5=c8f70ba8fc539d2890eaf0fbc10b0c97CAS | 18440928PubMed |

Winter K, Garcia M, Holtum JAM (2009) Canopy CO2 exchange of two neotropical tree species exhibiting constitutive and facultative CAM photosynthesis, Clusia rosea and Clusia cylindrica. Journal of Experimental Botany 60, 3167–3177.
Canopy CO2 exchange of two neotropical tree species exhibiting constitutive and facultative CAM photosynthesis, Clusia rosea and Clusia cylindrica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsValsLc%3D&md5=7e4253baec4e442eb145d599404d65f4CAS | 19487388PubMed |

Winter K, Garcia M, Holtum JAM (2011) Drought-stress induced up-regulation of CAM in seedlings of a tropical cactus, Opuntia elatior, operating predominantly in the C3 mode. Journal of Experimental Botany
Drought-stress induced up-regulation of CAM in seedlings of a tropical cactus, Opuntia elatior, operating predominantly in the C3 mode.Crossref | GoogleScholarGoogle Scholar | 21504876PubMed |

Zotz G, Winter K (1993) Short-term regulation of crassulacean acid metabolism activity in a tropical hemiepiphyte, Clusia uvitana. Plant Physiology 102, 835–841.

Zotz G, Winter K (1994) 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=77c343ff53abdd8e13fa6db2b7caf0a1CAS |