Diversity of CAM plant photosynthesis (crassulacean acid metabolism): a tribute to Barry Osmond
Klaus WinterSmithsonian Tropical Research Institute, PO Box 0843-03092, Balboa, Ancón, Republic of Panama. Email: winterk@si.edu
Functional Plant Biology 48(7) iii-ix https://doi.org/10.1071/FPv48n7_FO
Published: 7 June 2021
Abstract
This special issue is a tribute to the Australian plant biologist Professor Charles Barry Osmond – Fellow of the Australian Academy of Sciences, the Royal Society of London, and Leopoldina, the German National Academy of Sciences – and his many contributions to our understanding of the biochemistry and physiological ecology of CAM (crassulacean acid metabolism) photosynthesis. This water-conserving photosynthetic pathway is characterised by nocturnal uptake of atmospheric CO2 and typically enables succulent plants to perform and survive in warm semiarid terrestrial and epiphytic habitats. The idea for this issue is to mark the occasion of Barry’s 80th birthday in 2019. The foreword highlights some of his outstanding contributions and introduces the research papers of the special issue.
Throughout his long and rich scientific career, Barry Osmond has significantly advanced research on a wide range of topics in plant biology including halophytism, photorespiration, C4 photosynthesis, CAM photosynthesis, photoinhibition, and climate change. Here the focus is on his many contributions on or related to CAM. During his doctoral work, while studying the role of oxalate in a halophytic Atriplex species and using 14C labelling of leaves (Osmond 1967; Osmond 1997a), he was among the first to independently note similar 4-C label in malate and aspartate in the light and dark, a defining feature of C4 photosynthesis. In 1970, following the discovery and formal description of C4 photosynthesis, Barry, together with ‘Hal’ Hatch and Ralph Slatyer, assembled an illustrious group of photosynthesis researchers at the Australian National University (ANU) in Canberra to celebrate the recent advances on photosynthesis and photorespiration that had been made (Hatch et al. 1971; Fig. 1). This conference, considered the best-ever on photosynthesis by some (Björkman 2012), also addressed topics of CAM photosynthesis, with one conference contribution even referring to C4 photosynthesis as ‘CAM with Kranz’ (Laetsch 1971). The conference proceedings contain one of Barry’s earliest CAM papers, led by P.N. (‘Dani’) Avadhani, who had been conducting 14CO2 labelling experiments in Barry’s laboratory on a ANU visiting fellowship (Avadhani et al. 1971). Barry’s first contribution to CAM was about bisulfite inhibition of CO2 fixation in Sedum praealtum A.DC. (Osmond and Avadhani 1970).
In the years following the 1970 meeting, Barry and collaborators published a series of articles that fundamentally advanced our understanding of CAM. First, Sutton and Osmond (1972) provided evidence for a single β-carboxylation step during dark CO2 fixation of CAM plants, in analogy to phosphoenolpyruvate carboxylase-mediated CO2 uptake of C4 plants in the light. This refuted previous suggestions that two carboxylation events, the first via ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and the second via phosphoenolpyruvate carboxylase (PEPC), are involved in nocturnal CO2 fixation via CAM (Bradbeer et al. 1958). It also meant that the involvement of the pentose phosphate pathway in dark CO2-fixation as postulated previously was unnecessary and that glycolysis alone provided the precursors for malic acid synthesis. Pulse-chase experiments with 14CO2 in the CAM plant, Kalanchoë daigremontiana Raym.-Hamet & H.Perrier showed that steady-state photosynthesis in the late light period was similar to that in C3 plants and that the initial burst of photosynthesis following the night period still involved the primary carboxylation of phosphoenolpyruvate and malate synthesis (Osmond and Allaway 1974). A CO2 compensation point around 50 µL L–1 and substantial enhancement of CO2 uptake by lowering the O2 concentration to 4% were consistent with Rubisco-mediated steady-state photosynthesis in the light (Osmond and Björkman 1975). Furthermore, key enzymes of the CAM pathway were identified and studied (Kluge and Osmond 1971, 1972; Ting and Osmond 1973a, 1973b; Nott and Osmond 1982), the gluconeogenic recovery of pyruvate or PEP during deacidification was established (Holtum and Osmond 1981); and the CO2 : H+ stoichiometry of nocturnal CO2 fixation and the proportion of acid derived from CO2 recycling were determined (e.g. Medina and Osmond 1981).
Building on observations that carbon isotopic signatures (δ13C) separated C3 and C4 plants into two groups (Bender 1968; Smith and Epstein 1971), Barry immediately saw the potential of using δ13C values as indicators of the relative contributions of daytime and night-time CO2 fixation to the total carbon gain of CAM-exhibiting species. Evidence followed soon after (Osmond et al. 1973, 1976; Osmond and Ziegler 1975; see also Black and Osmond 2003), and further experimentation led to a sound theoretical understanding of how diffusional and biochemical components determine the δ13C values of CAM plants (O’Leary and Osmond 1980; Holtum et al. 1983; Osmond et al. 1988). Simultaneously, Barry started using the carbon isotopic technique to identify the CAM pathway in field-collected plants (Osmond et al. 1975), laying the foundations for other δ13C-based ecophysiological CAM studies (Osmond et al. 1982) and for large surveys on the distribution of CAM and C3 in species-rich plant families such as Bromeliaceae (Crayn et al. 2015), Orchidaceae (Winter et al. 1983; Silvera et al. 2010), and Euphorbiaceae (Horn et al. 2014).
Barry, with Jon Keeley and John Raven, also highlighted limitations of the carbon isotope technique in estimating the degrees of dark and light CO2 fixation in plants with CAM. For example, in the high-elevation Andean fern ally Stylites andicola Amstutz (now considered a synonym of Isoetes andicola (Amstutz) L.D.Gómez), the carbon isotopic signature is not a good predictor of photosynthetic pathway (Keeley et al. 1984). I. andicola has aerial leaves (microphylls) that lack stomata and CO2 is almost exclusively absorbed by the large root system anchored in peat. Although microphylls engage in CAM in addition to C3, this is not reflected in their carbon isotopic composition, because plants and the substrate they grow in are essentially closed systems, causing the δ13C value of I. andicola to be similar to that of the peat and groundwater carbonate.
Barry pioneered yet another avenue of CAM research. At the 1981 meeting of the American Society of Plant Physiologists on CAM in Riverside (Ting and Gibbs 1982), because of a delayed flight, Barry stormed into the lecture room just in time to deliver an enthusiastic speech on the virtues of chlorophyll a fluorescence, measured with a small, portable, commercially available device, to unravel some of the secrets of CAM photosynthesis (Osmond 1982). Until then such measurements were limited to specialists and required relatively bulky equipment. The use of handheld equipment, starting with the ‘plant productivity fluorometer’ (Schreiber et al. 1975), the instrument Barry introduced to the CAM community, was followed by enhanced use of the 77K chlorophyll fluorescence methodology to address ecological questions of CAM- and non-CAM plant biology (Björkman and Demmig 1987; Adams et al. 1987), and eventually led to the invention of the pulse-amplitude-modulation (PAM) technique (Schreiber et al. 1986) that revolutionised plant physiological ecology and has become a widely applied tool for monitoring plant stress tolerance.
All the research activities in the early- to mid-1970s described above culminated in Barry’s probably most significant CAM publication, his landmark review in Annual Review of Plant Physiology entitled, ‘Crassulacean acid metabolism: a curiosity in context’ (Osmond 1978). As in all of Barry’s writings the clear and concise text, composed of beautifully drafted sentences, is a joy to read. One of the many highlights of the review is a figure (fig. 1 in Osmond 1978) that defines the four separate phases of CAM gas exchange. No other figure in the CAM literature has ever been referred to and reproduced more often. The review itself seems timeless. It is the most cited paper exclusively devoted to CAM, with 24 Web of Science (webofknowledge.com) citations in 2019 alone, 41 years after the review was published!
The word ‘curiosity’ in the review’s title does not merely refer to the unusual photosynthetic physiology of CAM plants and the rather eccentric growth forms of some CAM-exhibiting species such as Lithops (the ‘living stones’; Aizoaceae) and Welwitschia mirabilis Hook.f. (the ‘living fossil’; Welwitschiaceae) (von Willert et al. 2005) of southern Africa, the Alluaudia species (Didiereaceae) of Madagascar (Winter 1979), and the ‘shoot-less’ orchids (Winter et al. 1985) of the Palaeotropics and Neotropics. Barry’s use of the word ‘curiosity’ is notable for two other reasons. First, Barry was on a lifelong crusade to promote block-funded, basic, curiosity-driven research as the primary way to make new discoveries and to significantly advance knowledge (Osmond 1997b, 2014). Most scientists would agree (although science administrators might not). Second, in the narrower context of CAM, whether intentional or not, viewing CAM as a curiosity may also have reflected a general perception that working on CAM, although a rewarding intellectual exercise for a relatively small group of aficionados addicted to their subject, lacks the same socioeconomic implications as working on C4 photosynthesis which is assumed to be key for future food security. This perception of CAM research as being in the shadows of C4 photosynthesis studies is gradually changing. We now know that CAM species greatly outnumber C4 species. Also, the enormous physiological plasticity of many species with CAM – in terms of their flexible use of dark versus light CO2 fixation – has yielded some of the most spectacular examples of metabolic adaptation to environmental stress in plants (Winter and von Willert 1972; Winter and Holtum 2014; Winter 2019). In addition, serious efforts are now being undertaken to bioengineer CAM into C3 crop plants to make land that is currently not arable available for future food and energy production (Borland et al. 2009; Yang et al. 2015).
Indeed, it is often overlooked that CAM plants can achieve colossal growth rates in mesic subtropical-tropical environments as evidenced by the prickly pear invasion in eastern central Australia in the late 19th and the early 20th centuries. In a 2007 lecture presented at the C4-CAM meeting in Cambridge that was later published in the conference proceedings (Osmond et al. 2008), Barry provided a vivid historical account of how an introduced species of Opuntia spread from a few plants in 1840 to occupy >25 million ha of land, producing a total biomass of ~1.5 billion tons in roughly 80 years. The audience was equally astounded to learn that initial warfare-like attempts to eradicate the cacti included the use of massive amounts of crude arsenic acid, arsenic pentoxide, and sulfuric acid. Smarter biological control techniques involving the introduced moth, Cactoblastis cactorum, eventually eliminated most of the cactus plants. In the 1970s, Barry and collaborators made several visits to remnant populations at four sites in Eastern Australia to study the physiological underpinnings that may have contributed to the huge success of Opuntia decades earlier (Osmond et al. 1979a, 1979b). Fig. 2 shows a photo of Barry during one of these field campaigns. He demonstrated that very active CO2 fixation in the dark and during the late afternoon following summer rainfall could have been key factors for the vigorous growth of this species in this habitat. A recent assessment of the status of Opuntia in Australia is given in Holtum et al. (2016). Research on agaves and cacti using the ‘Kluge-Lüttge Kammer’ at the Biosphere 2 facility in Arizona, where Barry was director later in his career, provided the first experimental data of CAM gas exchange at the mesocosm level (Rascher et al. 2006), eventually leading others to conduct detailed eddy covariance studies of CO2 fluxes over a field of Agave tequilana F.A.C.Weber in Mexico (Owen et al. 2016).
After presenting his Opuntia invasion story at the 2007 meeting, Barry said that this would be his last contribution to CAM. Fortunately, it wasn’t. The same year, another large CAM review appeared (Osmond 2007), and almost a decade later he took the lead in updating the chapter on CAM for the second edition of Plants in Action (Holtum et al. 2015), published by the Australian and New Zealand societies of plant sciences.
Barry’s current research is on novel aspects of PSII photochemistry in C3 plants (Osmond et al. 2019, 2021) using a state-of-the-art prototype light induced fluorescence transient (LIFT) instrument (Osmond et al. 2017).
The eight research papers in this issue cover a wide range of topics on CAM photosynthesis and highlight the extraordinary diversity of CAM-exhibiting species, both taxonomically and in terms of the relative proportions of atmospheric CO2 they incorporate at night via CAM and during the day via regular C3 photosynthesis (or C4 photosynthesis). One of the most interesting facets of CAM is its occurrence in C4 and in C3-C4 intermediate species of the genus Portulaca (Portulacaceae) (Koch and Kennedy 1980; Winter et al. 2019; Ferrari et al. 2020). For this issue, Ferrari et al. (2021) developed molecular tools to facilitate functional genomics studies in the C4/CAM model species Portulaca oleracea L., from the optimisation of RNA isolation protocols to a method for stable genetic transformation. Winter et al. (2021a) provide evidence for the presence of the CAM cycle in leaves and stems of a C4 species outside the Portulacaceae, i.e. in the pantropical herb Trianthema portulacastrum L. (Aizoaceae). Furthermore, CAM is reported for the first time in a species of the nettle family Urticaceae, Pilea peperomioides Diels, native to Yunnan and Sichuan provinces in south-western China (Winter et al. 2021b). This paper also contains an updated list of all plant families in which the CAM cycle has been confirmed. Winter et al. (2021c) highlight the co-occurrence of both stress-induced facultative and developmentally controlled constitutive CAM in a species of the Lamiaceae, Coleus amboinicus Lour., which is widely cultivated in the tropics as a spice and ornamental plant. Holtum et al. (2021) study CAM in two species of Cistanthe (Montiaceae) from the Atacama desert where these species contribute to spectacular desert blooms after rare massive rainfall events.
CAM tissues are typically succulent. Thereby, adequate vacuolar volume of chloroplast-containing cells is provided for nocturnal storage of malic acid per unit of CO2-assimilating surface area. In some taxa such as the neotropical tree genus Clusia, which contains CAM, C3-CAM, and C3 species (Lüttge 2006; Barrera Zambrano et al. 2014; Winter et al. 2015), hydrenchyma cells that lack chlorophyll and do not participate in CAM, contribute significantly to succulence. Using Clusia as a model, Leverett et al. (2021) investigate the relative roles of the CAM pathway, the turgor loss point, and the water-storage hydrenchyma tissue in the adaptation of plants to drought, and explore how these three leaf physiological traits contribute to species’ distribution across a precipitation gradient in Central and South America. Furthermore, Mejia-Chang et al. (2021) show for C3 and CAM bromeliads along an elevational gradient in western Panama, how epiphyte water balance during gas exchange is reflected in the δ18O signals of organic material and leaf water. Finally, to better understand water-deficit responses of the archetypal CAM species, Opuntia ficus-indica (L.) Mill., Mayer et al. (2021) provide a wealth of data on metabolic profiling of mesophyll and epidermal tissue from well hydrated and water-stressed cladodes.
Conflicts of interest
The author declares no conflicts of interest.
Declaration of funding
No specific funding was received to write this foreword.
Acknowledgements
In the late 1970s, the author was postdoctoral fellow in Barry Osmond’s laboratory in the Department of Environmental Biology, Research School of Biological Sciences (RSBS), Australian National University, Canberra. Barry’s unconditional support and the inspirational RSBS experience had a lasting formative impact on the author’s scientific career.
References
Adams WW, Smith SD, Osmond CB (1987) Photoinhibition of the CAM succulent Opuntia basilaris growing in Death Valley: evidence from 77K fluorescence and quantum yield. Oecologia 71, 221–228.| Photoinhibition of the CAM succulent Opuntia basilaris growing in Death Valley: evidence from 77K fluorescence and quantum yield.Crossref | GoogleScholarGoogle Scholar |
Avadhani PN, Osmond CB, Tan KK (1971) Crassulacean acid metabolism and the C4 pathway of photosynthesis in succulent plants. In ‘Photosynthesis and photorespiration’. pp. 288–293. (Wiley-Interscience: New York)
Barrera Zambrano VA, Lawson T, Olmos E, Fernández-García N, Borland AM (2014) Leaf anatomical traits which accommodate the facultative engagement of crassulacean acid metabolism in tropical trees of the genus Clusia. Journal of Experimental Botany 65, 3513–3523.
| Leaf anatomical traits which accommodate the facultative engagement of crassulacean acid metabolism in tropical trees of the genus Clusia.Crossref | GoogleScholarGoogle Scholar |
Bender MM (1968) Mass spectrometric studies of carbon 13 variations in corn and other grasses. Radiocarbon 10, 468–472.
| Mass spectrometric studies of carbon 13 variations in corn and other grasses.Crossref | GoogleScholarGoogle Scholar |
Björkman O (2012) Letter from Olle Björkman. Photosynthesis Research 113, 3–4.
| Letter from Olle Björkman.Crossref | GoogleScholarGoogle Scholar |
Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77K among vascular plants of diverse origins. Planta 170, 489–504.
| Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77K among vascular plants of diverse origins.Crossref | GoogleScholarGoogle Scholar |
Black CC, Osmond B (2003) Crassulacean acid metabolism photosynthesis: ‘working the night shift’. Photosynthesis Research 76, 329–341.
| Crassulacean acid metabolism photosynthesis: ‘working the night shift’.Crossref | GoogleScholarGoogle Scholar |
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 |
Bradbeer JW, Ranson SL, Stiller ML (1958) Malate synthesis in crassulacean leaves. I. The distribution of 14C in malate in leaves exposed to 14CO2 in the dark. Plant Physiology 33, 66–70.
| Malate synthesis in crassulacean leaves. I. The distribution of 14C in malate in leaves exposed to 14CO2 in the dark.Crossref | GoogleScholarGoogle Scholar |
Crayn DM, Winter K, Schulte K, Smith JAC (2015) Photosynthetic pathways in Bromeliaceae: phylogenetic and ecological significance of CAM and C3 based on carbon isotope ratios for 1893 species. Botanical Journal of the Linnean Society 178, 169–221.
| Photosynthetic pathways in Bromeliaceae: phylogenetic and ecological significance of CAM and C3 based on carbon isotope ratios for 1893 species.Crossref | GoogleScholarGoogle Scholar |
Ferrari RC, Bittencourt PP, Rodrigues MA, Moreno-Villena JJ, Alves FRR, Gastaldi VD, Boxall SF, Dever LV, Demarco D, Andrade SCS, Edwards EJ, Hartwell J, Freschi L (2020) C4 and crassulacean acid metabolism within a single leaf: deciphering key components behind a rare photosynthetic adaptation. New Phytologist 225, 1699–1714.
| C4 and crassulacean acid metabolism within a single leaf: deciphering key components behind a rare photosynthetic adaptation.Crossref | GoogleScholarGoogle Scholar |
Ferrari RC, Bittencourt PP, Nagumo PY, Oliveira WS, Rodrigues MA, Hartwell J, Freschi L (2021) Developing Portulaca oleracea as a model system for functional genomics analysis of C4/CAM photosynthesis. Functional Plant Biology 48, 666–682.
| Developing Portulaca oleracea as a model system for functional genomics analysis of C4/CAM photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Hatch MD, Osmond CB, Slatyer RO (Eds) (1971) ‘Photosynthesis and photorespiration.’ (Wiley-Interscience: New York)
Holtum JAM, Osmond CB (1981) The gluconeogenic metabolism of pyruvate during deacidification in plants with crassulacean acid metabolism. Australian Journal of Plant Physiology 8, 31–44.
Holtum JAM, O’Leary MH, Osmond CB (1983) Effect of varying CO2 partial pressure on photosynthesis and on carbon isotope composition of carbon-4 of malate from the crassulacean acid metabolism plant Kalanchoë daigremontiana Hamet et Perr. Plant Physiology 71, 602–609.
| Effect of varying CO2 partial pressure on photosynthesis and on carbon isotope composition of carbon-4 of malate from the crassulacean acid metabolism plant Kalanchoë daigremontiana Hamet et Perr.Crossref | GoogleScholarGoogle Scholar |
Holtum JAM, Winter K, Osmond CB (2015) Crassulacean acid metabolism (CAM). In ‘Plants in action’, 2nd edn. Chapter 2, 30–41. (Australian Society of Plant Scientists). Available at plantsinaction.science.uq.edu.au
Holtum JAM, Hancock LP, Edwards EJ, Crisp MD, Crayn DM, Sage R, Winter K (2016) Australia lacks stem succulents but is it depauperate in plants with crassulacean acid metabolism (CAM)? Current Opinion in Plant Biology 31, 109–117.
| Australia lacks stem succulents but is it depauperate in plants with crassulacean acid metabolism (CAM)?Crossref | GoogleScholarGoogle Scholar |
Holtum JAM, Hancock LP, Edwards EJ, Winter K (2021) CAM photosynthesis in desert blooming Cistanthe of the Atacama, Chile. Functional Plant Biology 48, 691–702.
| CAM photosynthesis in desert blooming Cistanthe of the Atacama, Chile.Crossref | GoogleScholarGoogle Scholar |
Horn JW, Xi Z, Riina R, Peirson JA, Yang Y, Dorsey BL, Berry PE, Davis CC, Wurdack KJ (2014) Evolutionary bursts in Euphorbia (Euphorbiaceae) are linked with photosynthetic pathway. Evolution 68, 3485–3504.
| Evolutionary bursts in Euphorbia (Euphorbiaceae) are linked with photosynthetic pathway.Crossref | GoogleScholarGoogle Scholar |
Keeley JE, Osmond CB, Raven JA (1984) Stylites, a vascular land plant without stomata absorbs CO2 via its roots. Nature 310, 694–695.
| Stylites, a vascular land plant without stomata absorbs CO2 via its roots.Crossref | GoogleScholarGoogle Scholar |
Kluge M, Osmond CB (1971) Pyruvate Pi dikinase in crassulacean acid metabolism. Naturwissenschaften 58, 414–415.
| Pyruvate Pi dikinase in crassulacean acid metabolism.Crossref | GoogleScholarGoogle Scholar |
Kluge M, Osmond CB (1972) Studies on phosphoenolpyruvate carboxylase and other enzymes of crassulacean acid metabolism of Bryophyllum tubiflorum and Sedum praealtum. Zeitschrift für Pflanzenphysiologie 66, 97–105.
| Studies on phosphoenolpyruvate carboxylase and other enzymes of crassulacean acid metabolism of Bryophyllum tubiflorum and Sedum praealtum.Crossref | GoogleScholarGoogle Scholar |
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 |
Laetsch WM (1971) Chloroplast structural relationships in leaves of C4 plants. In ‘Photosynthesis and photorespiration’. pp. 323–349. (Wiley-Interscience: New York)
Leverett A, Castaño NH, Ferguson K, Winter K, Borland AM (2021) Crassulacean acid metabolism (CAM) supersedes the turgor loss point (TLP) as an important adaptation across a precipitation gradient, in the genus Clusia. Functional Plant Biology 48, 703–715.
| Crassulacean acid metabolism (CAM) supersedes the turgor loss point (TLP) as an important adaptation across a precipitation gradient, in the genus Clusia.Crossref | GoogleScholarGoogle Scholar |
Lüttge U (2006) Photosynthetic flexibility and ecophysiological plasticity: questions and lessons from Clusia, the only CAM tree, in the neotropics. New Phytologist 171, 7–25.
| Photosynthetic flexibility and ecophysiological plasticity: questions and lessons from Clusia, the only CAM tree, in the neotropics.Crossref | GoogleScholarGoogle Scholar |
Mayer JA, Wone BWM, Alexander DC, Guo L, Ryals JA, Cushman JC (2021) Metabolic profiling of epidermal and mesophyll tissues under water-deficit stress in Opuntia ficus-indica reveals stress-adaptive metabolic responses. Functional Plant Biology 48, 716–730.
| Metabolic profiling of epidermal and mesophyll tissues under water-deficit stress in Opuntia ficus-indica reveals stress-adaptive metabolic responses.Crossref | GoogleScholarGoogle Scholar |
Medina E, Osmond CB (1981) Temperature dependence of dark CO2 fixation and acid accumulation in Kalanchoë daigremontiana. Australian Journal of Plant Physiology 8, 641–649.
Mejia-Chang M, Reyes-Garcia C, Seibt U, Royles J, Meyer MT, Jones GD, Winter K, Arnedo M, Griffiths H (2021) Leaf water δ18O reflects water vapour exchange and uptake by C3 and CAM epiphytic bromeliads in Panama. Functional Plant Biology 48, 731–741.
| Leaf water δ18O reflects water vapour exchange and uptake by C3 and CAM epiphytic bromeliads in Panama.Crossref | GoogleScholarGoogle Scholar |
Nott DL, Osmond CB (1982) Purification and properties of phosphoenolpyruvate carboxylase from plants with crassulacean acid metabolism. Australian Journal of Plant Physiology 9, 409–422.
O’Leary MH, Osmond CB (1980) Diffusional contribution to carbon isotope fractionation during dark CO2 fixation in CAM plants. Plant Physiology 66, 931–934.
| Diffusional contribution to carbon isotope fractionation during dark CO2 fixation in CAM plants.Crossref | GoogleScholarGoogle Scholar |
Osmond CB (1967) β-Carboxylation in Atriplex. Biochimica et Biophysica Acta 141, 197–199.
| β-Carboxylation in Atriplex.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 |
Osmond CB (1982) Carbon cycling and the stability of the photosynthetic apparatus in CAM. In ‘Crassulacean acid metabolism’. pp. 112–127. (American Society of Plant Physiologists: Rockville, USA)
Osmond CB (1997a) C4 photosynthesis: thirty or forty years on. Australian Journal of Plant Physiology 24, 409–412.
Osmond CB (1997b) To change the way we think about things. In ‘Nurturing creativity in research: ideas as the foundations of innovation’. pp. 2–11. (Research School of Biological Sciences: Canberra, Australia)
Osmond CB (2007) Crassulacean acid metabolism: now and then. Progress in Botany 68, 3–32.
| Crassulacean acid metabolism: now and then.Crossref | GoogleScholarGoogle Scholar |
Osmond B (2014) Our eclectic adventures in the slower eras of photosynthesis: from New England down under to Biosphere 2 and beyond. Annual Review of Plant Biology 65, 1–32.
| Our eclectic adventures in the slower eras of photosynthesis: from New England down under to Biosphere 2 and beyond.Crossref | GoogleScholarGoogle Scholar |
Osmond CB, Allaway WG (1974) Pathways of CO2 fixation in the CAM plant Kalanchoe daigremontiana. I Patterns of 14CO2 fixation in the light. Australian Journal of Plant Physiology 1, 503–511.
Osmond CB, Avadhani PN (1970) Inhibition of the β-carboxylation pathway of CO2 fixation by bisulfite compounds. Plant Physiology 45, 228–230.
| Inhibition of the β-carboxylation pathway of CO2 fixation by bisulfite compounds.Crossref | GoogleScholarGoogle Scholar |
Osmond CB, Björkman O (1975) Pathways of CO2 fixation in the CAM plant Kalanchoë daigremontiana. II Effects of O2 and CO2 concentration on light and dark CO2 fixation. Australian Journal of Plant Physiology 2, 155–162.
Osmond CB, Ziegler H (1975) Schwere Pflanzen und leichte Pflanzen: Stabile Isotope im Photosynthesestoffwechsel und in der Biochemischen Ökologie. Naturwissenschaftliche Rundschau 28, 323–328.
Osmond CB, Allaway WG, Sutton BG, Troughton JH, Queiroz O, Lüttge U, Winter K (1973) Carbon isotope discrimination in photosynthesis of CAM-plants. Nature 246, 41–42.
| Carbon isotope discrimination in photosynthesis of CAM-plants.Crossref | GoogleScholarGoogle Scholar |
Osmond CB, Ziegler H, Stichler W, Trimborn P (1975) Carbon isotope discrimination in alpine succulent plants supposed to be capable of crassulacean acid metabolism (CAM). Oecologia 18, 209–217.
| Carbon isotope discrimination in alpine succulent plants supposed to be capable of crassulacean acid metabolism (CAM).Crossref | GoogleScholarGoogle Scholar |
Osmond CB, Bender MM, Burris RH (1976) Pathways of CO2 fixation in the CAM plant Kalanchoe daigremontiana. III. Correlation with δ13C value during growth and water stress. Australian Journal of Plant Physiology 3, 787–799.
Osmond CB, Nott DL, Firth PM (1979a) Carbon assimilation patterns and growth of the introduced CAM plant Opuntia inermis in Eastern Australia. Oecologia 40, 331–350.
| Carbon assimilation patterns and growth of the introduced CAM plant Opuntia inermis in Eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Osmond CB, Ludlow MM, Davies R, Cowan IR, Powles SB, Winter K (1979b) Stomatal responses to humidity in Opuntia inermis in relation to control of CO2 and H2O exchange patterns. Oecologia 41, 65–76.
| Stomatal responses to humidity in Opuntia inermis in relation to control of CO2 and H2O exchange patterns.Crossref | GoogleScholarGoogle Scholar |
Osmond CB, Winter K, Ziegler H (1982) Functional significance of different pathways of CO2 fixation in photosynthesis. In ‘Physiological Plant Ecology II’. pp. 479–547. (Springer: Berlin, Germany)
Osmond CB, Holtum JAM, O’Leary MH, Roeske C, Wong OC, Summons RE, Avadhani PN (1988) Regulation of malic-acid metabolism in Crassulacean-acid-metabolism plants in the dark and light: in-vivo evidence from 13C-labeling patterns after 13CO2 fixation. Planta 175, 184–192.
| Regulation of malic-acid metabolism in Crassulacean-acid-metabolism plants in the dark and light: in-vivo evidence from 13C-labeling patterns after 13CO2 fixation.Crossref | GoogleScholarGoogle Scholar |
Osmond B, Neales T, Stange G (2008) Curiosity and context revisited: crassulacean acid metabolism in the Anthropocene. Journal of Experimental Botany 59, 1489–1502.
| Curiosity and context revisited: crassulacean acid metabolism in the Anthropocene.Crossref | GoogleScholarGoogle Scholar |
Osmond B, Chow WS, Wyber R, Zavafer A, Keller B, Pogson BJ, Robinson SA (2017) Relative functional and optical absorption cross-sections of PSII and other photosynthetic parameters monitored in situ, using a prototype light induced fluorescence transient (LIFT) device. Functional Plant Biology 44, 985–1006.
| Relative functional and optical absorption cross-sections of PSII and other photosynthetic parameters monitored in situ, using a prototype light induced fluorescence transient (LIFT) device.Crossref | GoogleScholarGoogle Scholar |
Osmond B, Chow WS, Pogson BJ, Robinson SA (2019) Probing functional and optical cross-sections of PSII in leaves during state transitions using fast repetition rate light induced fluorescence transients. Functional Plant Biology 46, 567–583.
| Probing functional and optical cross-sections of PSII in leaves during state transitions using fast repetition rate light induced fluorescence transients.Crossref | GoogleScholarGoogle Scholar |
Osmond CB, Chow WS, Robinson SA (2021) Inhibition of non-photochemical quenching increases functional absorption cross section of photosystem II as excitation from closed reaction centres is transferred to open centres, facilitating earlier light saturation of photosynthetic electron transport. Functional Plant Biology
| Inhibition of non-photochemical quenching increases functional absorption cross section of photosystem II as excitation from closed reaction centres is transferred to open centres, facilitating earlier light saturation of photosynthetic electron transport.Crossref | GoogleScholarGoogle Scholar |
Owen NA, Choncubhair ÓN, Males J, de Real Laborde JI, Rubio-Cortés R, Griffiths H, Lanigan G (2016) Eddy covariance captures four-phase crassulacean acid metabolism (CAM) gas exchange signature in Agave. Plant, Cell & Environment 39, 295–309.
| Eddy covariance captures four-phase crassulacean acid metabolism (CAM) gas exchange signature in Agave.Crossref | GoogleScholarGoogle Scholar |
Rascher U, Bobich EG, Osmond CB (2006) The “Kluge-Lüttge Kammer”: a preliminary evaluation of an enclosed, crassulacean acid metabolism (CAM) mesocosm that allows separation of synchronized and desynchronized contributions of plants to whole system gas exchange. Plant Biology 8, 167–174.
| The “Kluge-Lüttge Kammer”: a preliminary evaluation of an enclosed, crassulacean acid metabolism (CAM) mesocosm that allows separation of synchronized and desynchronized contributions of plants to whole system gas exchange.Crossref | GoogleScholarGoogle Scholar |
Schreiber U, Groberman L, Vidaver W (1975) Portable, solid-state fluorometer for the measurement of chlorophyll fluorescence induction in plants. The Review of Scientific Instruments 46, 538–542.
| Portable, solid-state fluorometer for the measurement of chlorophyll fluorescence induction in plants.Crossref | GoogleScholarGoogle Scholar |
Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Research 10, 51–62.
| Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer.Crossref | GoogleScholarGoogle Scholar |
Silvera K, Santiago LS, Cushman JC, Winter K (2010) The incidence of crassulacean acid metabolism in Orchidaceae derived from carbon isotope ratios: a checklist of the flora of Panama and Costa Rica. Botanical Journal of the Linnean Society 163, 194–222.
| The incidence of crassulacean acid metabolism in Orchidaceae derived from carbon isotope ratios: a checklist of the flora of Panama and Costa Rica.Crossref | GoogleScholarGoogle Scholar |
Smith BN, Epstein S (1971) Two categories of 13C/12C ratios for higher plants. Plant Physiology 47, 380–384.
| Two categories of 13C/12C ratios for higher plants.Crossref | GoogleScholarGoogle Scholar |
Sutton BG, Osmond CB (1972) Dark fixation of CO2 by crassulacean plants. Evidence for a single carboxylation step. Plant Physiology 50, 360–365.
| Dark fixation of CO2 by crassulacean plants. Evidence for a single carboxylation step.Crossref | GoogleScholarGoogle Scholar |
Ting IP, Gibbs M (1982) (Eds) ‘Crassulacean acid metabolism.’ (American Society of Plant Physiologists: Rockville, USA)
Ting IP, Osmond CB (1973a) Multiple forms of plant phosphoenolpyruvate carboxylase associated with different metabolic pathways. Plant Physiology 51, 448–453.
| Multiple forms of plant phosphoenolpyruvate carboxylase associated with different metabolic pathways.Crossref | GoogleScholarGoogle Scholar |
Ting IP, Osmond CB (1973b) Activation of plant p-enolpyruvate carboxylases by glucose-6-phosphate: a particular role in crassulacean acid metabolism. Plant Science Letters 1, 123–128.
| Activation of plant p-enolpyruvate carboxylases by glucose-6-phosphate: a particular role in crassulacean acid metabolism.Crossref | GoogleScholarGoogle Scholar |
von Willert DJ, Armbrüster N, Drees T, Zaborowski M (2005) Welwitschia mirabilis: CAM or not CAM – what is the answer? Functional Plant Biology 32, 389–395.
| Welwitschia mirabilis: CAM or not CAM – what is the answer?Crossref | GoogleScholarGoogle Scholar |
Winter K (1979) δ13C values of some succulent plants from Madagascar. Oecologia 40, 103–112.
| δ13C values of some succulent plants from Madagascar.Crossref | GoogleScholarGoogle Scholar |
Winter K (2019) Ecophysiology of constitutive and facultative CAM photosynthesis. Journal of Experimental Botany 70, 6495–6508.
| Ecophysiology of constitutive and facultative CAM photosynthesis.Crossref | GoogleScholarGoogle Scholar |
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 65, 3425–3441.
| Facultative crassulacean acid metabolism (CAM) plants: powerful tools for unravelling the functional elements of CAM photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Winter K, von Willert DJ (1972) NaCl-induzierter Crassulaceensäurestoffwechsel bei Mesembryanthemum crystallinum. Zeitschrift für Pflanzenphysiologie 67, 166–170.
| NaCl-induzierter Crassulaceensäurestoffwechsel bei Mesembryanthemum crystallinum.Crossref | GoogleScholarGoogle Scholar |
Winter K, Wallace BJ, Stocker GC, Roksandic Z (1983) Crassulacean acid metabolism in Australian vascular epiphytes and some related species. Oecologia 57, 129–141.
| Crassulacean acid metabolism in Australian vascular epiphytes and some related species.Crossref | GoogleScholarGoogle Scholar |
Winter K, Medina E, Garcia V, Mayoral ML, Munoz R (1985) Crassulacean acid metabolism in roots of a leafless orchid, Campylocentrum tyrridion Garay & Dunsterv. Journal of Plant Physiology 118, 73–78.
| Crassulacean acid metabolism in roots of a leafless orchid, Campylocentrum tyrridion Garay & Dunsterv.Crossref | GoogleScholarGoogle Scholar |
Winter K, Holtum JAM, Smith JAC (2015) Crassulacean acid metabolism: a continuous or discrete trait? New Phytologist 208, 73–78.
| Crassulacean acid metabolism: a continuous or discrete trait?Crossref | GoogleScholarGoogle Scholar |
Winter K, Sage RF, Edwards EJ, Virgo A, Holtum JAM (2019) Facultative crassulacean acid metabolism in a C3-C4 intermediate. Journal of Experimental Botany 70, 6571–6579.
| Facultative crassulacean acid metabolism in a C3-C4 intermediate.Crossref | GoogleScholarGoogle Scholar |
Winter K, Garcia M, Virgo A, Ceballos J, Holtum JAM (2021a) Does the C4 plant Trianthema portulacastrum (Aizoaceae) exhibit weakly expressed crassulaceam acid metabolism (CAM)? Functional Plant Biology 48, 655–665.
| Does the C4 plant Trianthema portulacastrum (Aizoaceae) exhibit weakly expressed crassulaceam acid metabolism (CAM)?Crossref | GoogleScholarGoogle Scholar |
Winter K, Garcia M, Virgo A, Smith JAC (2021b) Low-level CAM photosynthesis in a succulent-leaved member of the Urticaceae, Pilea peperomioides. Functional Plant Biology 48, 683–690.
| Low-level CAM photosynthesis in a succulent-leaved member of the Urticaceae, Pilea peperomioides.Crossref | GoogleScholarGoogle Scholar |
Winter K, Virgo A, Garcia M, Aranda J, Holtum JAM (2021c) Constitutive and facultative crassulacean acid metabolism (CAM) in Cuban oregano, Coleus amboinicus (Lamiaceae). Functional Plant Biology 48, 647–654.
| Constitutive and facultative crassulacean acid metabolism (CAM) in Cuban oregano, Coleus amboinicus (Lamiaceae).Crossref | GoogleScholarGoogle Scholar |
Yang X, Cushman JC, Borland AM, et al (2015) A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world. New Phytologist 207, 491–504.
| A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world.Crossref | GoogleScholarGoogle Scholar |
