Crassulacean acid metabolism (CAM) supersedes the turgor loss point (TLP) as an important adaptation across a precipitation gradient, in the genus Clusia
Alistair Leverett A B C E , Natalia Hurtado Castaño A D , Kate Ferguson A , Klaus Winter B and Anne M. Borland AA School of Natural and Environmental Sciences, Newcastle University, Newcastle Upon Tyne, NE1 7RU, UK.
B Smithsonian Tropical Research Institute, PO Box 0843-03092, Balboa, Ancón, Republic of Panama.
C Carl R. Woese Institute for Genomic Biology, 1206 West Gregory Drive, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.
D Department of Molecular Biology and Biotechnology, University of Sheffield, Western Bank, Sheffield, S10 2TN, UK.
E Corresponding author. Email: alilev93@illinois.edu
Functional Plant Biology 48(7) 703-716 https://doi.org/10.1071/FP20268
Submitted: 25 August 2020 Accepted: 30 January 2021 Published: 5 March 2021
Abstract
As future climates continue to change, precipitation deficits are expected to become more severe across tropical ecosystems. As a result, it is important that we identify plant physiological traits that act as adaptations to drought, and determine whether these traits act synergistically or independently of each other. In this study, we assessed the role of three leaf-level putative adaptations to drought: crassulacean acid metabolism (CAM), the turgor loss point (TLPΨ) and water storage hydrenchyma tissue. Using the genus Clusia as a model, we were able to explore the extent to which these leaf physiological traits co-vary, and also how they contribute to species’ distributions across a precipitation gradient in Central and South America. We found that CAM is independent of the TLPΨ and hydrenchyma depth in Clusia. In addition, we provide evidence that constitutive CAM is an adaptation to year-long water deficits, whereas facultative CAM appears to be more important for surviving acute dry seasons. Finally, we find that the other leaf traits tested did not correlate with environmental precipitation, suggesting that the reduced transpirational rates associated with CAM obviate the need to adapt the TLPΨ and hydrenchyma depth in this genus.
Keywords: crassulacean acid metabolism, CAM plants, hydrenchyma, turgor, Clusia spp., drought tolerance, tropical ecophysiology, rainforest ecology.
References
Ahl LI, Mravec J, Jørgensen B, Rudall PJ, Rønsted N, Grace OM (2019) Dynamics of intracellular mannan and cell wall folding in the drought responses of succulent Aloe species. Plant, Cell & Environment 42, 2458–2471.| Dynamics of intracellular mannan and cell wall folding in the drought responses of succulent Aloe species.Crossref | GoogleScholarGoogle Scholar |
Anderegg WRL, Kane JM, Anderegg LDL (2013) Consequences of widespread tree mortality triggered by drought and temperature stress. Nature Climate Change 3, 30–36.
| Consequences of widespread tree mortality triggered by drought and temperature stress.Crossref | GoogleScholarGoogle Scholar |
Arakaki M, Christin P-A, Nyffeler R, Lendel A, Eggli U, Ogburn RM, Spriggs E, Moore MJ, Edwards EJ (2011) Contemporaneous and recent radiations of the world’s major succulent plant lineages. Proceedings of the National Academy of Sciences of the United States of America 108, 8379–8384.
| Contemporaneous and recent radiations of the world’s major succulent plant lineages.Crossref | GoogleScholarGoogle Scholar | 21536881PubMed |
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 | 24510939PubMed |
Bartlett MK, Scoffoni C, Sack L (2012) The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: A global meta-analysis. Ecology Letters 15, 393–405.
| The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: A global meta-analysis.Crossref | GoogleScholarGoogle Scholar | 22435987PubMed |
Beadle CL, Ludlow MM, Honeysett JL (1985) Water relations. In ‘Techniques in bioproductivity and photosynthesis’, 2nd edn. (Eds J Coombs, DO Hall, SP Long, JMOScurlock) pp. 50–61. (Pergamon)
Bone RE, Smith JAC, Arrigo N, Buerki S (2015) A macro-ecological perspective on crassulacean acid metabolism (CAM) photosynthesis evolution in Afro-Madagascan drylands: Eulophiinae orchids as a case study. New Phytologist 208, 469–481.
| A macro-ecological perspective on crassulacean acid metabolism (CAM) photosynthesis evolution in Afro-Madagascan drylands: Eulophiinae orchids as a case study.Crossref | GoogleScholarGoogle Scholar |
Borland AM, Griffiths H, Maxwell C, Broadmeadow MSJ, Griffiths NM, Barnes JD (1992) On the ecophysiology of the Clusiaceae in Trinidad: expression of CAM in Clusia minor L. during the transition from wet to dry season and characterization of three endemic species. New Phytologist 122, 349–357.
| On the ecophysiology of the Clusiaceae in Trinidad: expression of CAM in Clusia minor L. during the transition from wet to dry season and characterization of three endemic species.Crossref | GoogleScholarGoogle Scholar |
Borland AM, Técsi LI, Leegood RC, Walker RP (1998) Inducibility of crassulacean acid metabolism (CAM) in Clusia species; physiological/biochemical characterisation and intercellular localization of carboxylation and decarboxylation processes in three species which exhibit different degrees of CAM. Planta 205, 342–351.
| Inducibility of crassulacean acid metabolism (CAM) in Clusia species; physiological/biochemical characterisation and intercellular localization of carboxylation and decarboxylation processes in three species which exhibit different degrees of CAM.Crossref | GoogleScholarGoogle Scholar |
Borland AM, Hartwell J, Weston DJ, Schlauch Ka, Tschaplinski TJ, Tuskan Ga, Yang X, Cushman JC (2014) Engineering crassulacean acid metabolism to improve water-use efficiency. Trends in Plant Science 19, 327–338.
| Engineering crassulacean acid metabolism to improve water-use efficiency.Crossref | GoogleScholarGoogle Scholar | 24559590PubMed |
Borland AM, Leverett A, Hurtado-Castano N, Hu R, Yang X (2018) Functional anatomical traits of the photosynthetic organs of plants with crassulacean acid metabolism. In ‘The leaf: a platform for performing photosynthesis’, 1st edn. (Eds WW Adams III, I Terashima) pp. 281–305. (Springer International Publishing AG: Cham, Switzerland)
Chiang JM, Lin TC, Luo YC, Te Chang C, Cheng JY, Martin CE (2013) Relationships among rainfall, leaf hydrenchyma, and Crassulacean acid metabolism in Pyrrosia lanceolata (L.) Fraw. (Polypodiaceae) in central Taiwan. Flora 208, 343–350.
| Relationships among rainfall, leaf hydrenchyma, and Crassulacean acid metabolism in Pyrrosia lanceolata (L.) Fraw. (Polypodiaceae) in central Taiwan.Crossref | GoogleScholarGoogle Scholar |
Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG, et al (2012) Global convergence in the vulnerability of forests to drought. Nature 491, 752–755.
| Global convergence in the vulnerability of forests to drought.Crossref | GoogleScholarGoogle Scholar | 23172141PubMed |
Choat B, Brodribb TJ, Brodersen CR, Duursma RA, López R, Medlyn BE (2018) Triggers of tree mortality under drought. Nature 558, 531–539.
| Triggers of tree mortality under drought.Crossref | GoogleScholarGoogle Scholar | 29950621PubMed |
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 | 14982989PubMed |
de Mattos EA, Scarano FR, Cavalin PO, Fernandes GW, Rennenberg H, Lüttge U (2019) Ecophysiological performance of four species of Clusiaceae with different modes of photosynthesis in a mosaic of riverine, rupestrian grasslands, and cerrado vegetation in SE-Brazil. Trees 33, 641–652.
| Ecophysiological performance of four species of Clusiaceae with different modes of photosynthesis in a mosaic of riverine, rupestrian grasslands, and cerrado vegetation in SE-Brazil.Crossref | GoogleScholarGoogle Scholar |
Dias ATC, Scarano FR (2007) Clusia as nurse plant. In ‘Clusia: a woody neotropical genus of remarkable plasticity and diversity’. (Ed. U Lüttge) pp. 55–71. (Springer-Verlag: Berlin)
Duke NC, Kovacs JM, Griffiths AD, Preece L, Hill DJE, van Oosterzee P, Mackenzie J, Morning HS, Burrows D (2017) Large-scale dieback of mangroves in Australia’s Gulf of Carpentaria: a severe ecosystem response, coincidental with an unusually extreme weather event. Marine and Freshwater Research 68, 1816–1829.
| Large-scale dieback of mangroves in Australia’s Gulf of Carpentaria: a severe ecosystem response, coincidental with an unusually extreme weather event.Crossref | GoogleScholarGoogle Scholar |
Earnshaw MJ, Ziegler KWH, Stichler W, Cruttwell NEG, Kerenga K, Wood J, Croft JR, Carver KA, Gunn TC (1987) Altitudinal changes in the incidence of crassulacean acid metabolism in vascular epiphytes and related life forms in Papua New Guinea. Oecologia 73, 566–572.
| Altitudinal changes in the incidence of crassulacean acid metabolism in vascular epiphytes and related life forms in Papua New Guinea.Crossref | GoogleScholarGoogle Scholar | 28311975PubMed |
Edwards EJ (2019) Evolutionary trajectories, accessibility, and other metaphors: the case of C4 and CAM photosynthesis. New Phytologist 223, 1742–1755.
| Evolutionary trajectories, accessibility, and other metaphors: the case of C4 and CAM photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Fletcher LR, Cui H, Callahan H, Scoffoni C, John GP, Bartlett MK, Burge DO, Sack L (2018) Evolution of leaf structure and drought tolerance in species of Californian Ceanothus. American Journal of Botany 105, 1672–1687.
| Evolution of leaf structure and drought tolerance in species of Californian Ceanothus.Crossref | GoogleScholarGoogle Scholar | 30368798PubMed |
Grace OM, Buerki S, Symonds MRE, Forest F, Van Wyk AE, Smith GF, Klopper RR, Bjorå CS, Neale S, Demissew S, Simmonds MSJ, Rønsted N (2015) Evolutionary history and leaf succulence as explanations for medicinal use in aloes and the global popularity of Aloe vera. BMC Evolutionary Biology 15, 29
| Evolutionary history and leaf succulence as explanations for medicinal use in aloes and the global popularity of Aloe vera.Crossref | GoogleScholarGoogle Scholar | 25879886PubMed |
Griffin-Nolan RJ, Ocheltree TW, Mueller KE, Blumenthal DM, Kray JA, Knapp AK (2019) Extending the osmometer method for assessing drought tolerance in herbaceous species. Oecologia 189, 353–363.
| Extending the osmometer method for assessing drought tolerance in herbaceous species.Crossref | GoogleScholarGoogle Scholar | 30627784PubMed |
Gustafsson M, Winter K, Bittrich V (2007) Diversity, phylogeny and classification of Clusia. In ‘Clusia: a woody neotropical genus of remarkable plasticity and diversity’. (Ed. U Lüttge) pp. 95–116. (Springer-Verlag: Berlin)
Herrera A, Fernández MD, Taisma MA (2000) Effects of drought on CAM and water relations in plants of Peperomia carnevalii. Annals of Botany 86, 511–517.
| Effects of drought on CAM and water relations in plants of Peperomia carnevalii.Crossref | GoogleScholarGoogle Scholar |
Heyduk K (2021) The genetic control of succulent leaf development. Current Opinion in Plant Biology 59, 101978
| The genetic control of succulent leaf development.Crossref | GoogleScholarGoogle Scholar | 33454545PubMed |
Hochberg U, Rockwell FE, Holbrook NM, Cochard H (2018) Iso/Anisohydry: A Plant–Environment Interaction Rather Than a Simple Hydraulic Trait. Trends in Plant Science 23, 112–120.
| Iso/Anisohydry: A Plant–Environment Interaction Rather Than a Simple Hydraulic Trait.Crossref | GoogleScholarGoogle Scholar | 29223922PubMed |
Holl KD, Loik ME, Lin EHV, Samuels IA (2000) Tropical montane forest restoration in Costa Rica: Overcoming barriers to dispersal and establishment. Restoration Ecology 8, 339–349.
| Tropical montane forest restoration in Costa Rica: Overcoming barriers to dispersal and establishment.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 | 25302554PubMed |
John GP, Henry C, Sack L (2018) Leaf rehydration capacity: Associations with other indices of drought tolerance and environment. Plant, Cell & Environment 41, 2638–2653.
| Leaf rehydration capacity: Associations with other indices of drought tolerance and environment.Crossref | GoogleScholarGoogle Scholar |
Kaul RB (1977) The Role of the Multiple Epidermis in Foliar Succulence of Peperomia (Piperaceae). Botanical Gazette 138, 213–218.
| The Role of the Multiple Epidermis in Foliar Succulence of Peperomia (Piperaceae).Crossref | GoogleScholarGoogle Scholar |
Kornas A, Fischer-Schliebs E, Lüttge U, Miszalski Z (2009) Adaptation of the obligate CAM plant Clusia alata to light stress: Metabolic responses. Journal of Plant Physiology 166, 1914–1922.
| Adaptation of the obligate CAM plant Clusia alata to light stress: Metabolic responses.Crossref | GoogleScholarGoogle Scholar | 19592134PubMed |
Kunert N, Zailaa J, Herrmann V, Muller-Landau HC, Wright SJ, Pérez R, McMahon SM, Condit RC, Hubbell SP, Sack L, Davies SJ, Anderson-Teixeira KJ (2021) Leaf turgor loss point shapes local and regional distributions of evergreen but not deciduous tropical trees. New Phytologist
| Leaf turgor loss point shapes local and regional distributions of evergreen but not deciduous tropical trees.Crossref | GoogleScholarGoogle Scholar |
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 (Ed.) (2007) ‘Clusia: a woody neotropical genus of remarkable plasticity and diversity.’ (Springer-Verlag: Berlin)
Lüttge U, Scarano FR, de Mattos EA, Franco AC, Broetto F, Dias ATC, Duarte HM, Uehlein N, Wendt T (2015) Does ecophysiological behaviour explain habitat occupation of sympatric Clusia species in a Brazilian Atlantic rainforest? Trees 29, 1973–1988.
| Does ecophysiological behaviour explain habitat occupation of sympatric Clusia species in a Brazilian Atlantic rainforest?Crossref | GoogleScholarGoogle Scholar |
Males J (2018) Concerted anatomical change associated with crassulacean acid metabolism in the Bromeliaceae. Functional Plant Biology 45, 681–695.
| Concerted anatomical change associated with crassulacean acid metabolism in the Bromeliaceae.Crossref | GoogleScholarGoogle Scholar | 32291044PubMed |
Males J, Griffiths H (2017) Functional types in the Bromeliaceae: relationships with drought-resistance traits and bioclimatic distributions. Functional Ecology 31, 1868–1880.
| Functional types in the Bromeliaceae: relationships with drought-resistance traits and bioclimatic distributions.Crossref | GoogleScholarGoogle Scholar |
Males J, Griffiths H (2018) Economic and hydraulic divergences underpin ecological differentiation in the Bromeliaceae. Plant, Cell & Environment 41, 64–78.
| Economic and hydraulic divergences underpin ecological differentiation in the Bromeliaceae.Crossref | GoogleScholarGoogle Scholar |
Maréchaux I, Saint-André L, Bartlett MK, Sack L, Chave J (2020) Leaf drought tolerance cannot be inferred from classic leaf traits in a tropical rainforest. Journal of Ecology 108, 1030–1045.
| Leaf drought tolerance cannot be inferred from classic leaf traits in a tropical rainforest.Crossref | GoogleScholarGoogle Scholar |
Marengo JA, Jones R, Alves L, Valverde MC (2009) Future change of temperature and precipitation extremes in South America as derived from the PRECIS regional climate modeling system. International Journal of Climatology 29, 2241–2255.
| Future change of temperature and precipitation extremes in South America as derived from the PRECIS regional climate modeling system.Crossref | GoogleScholarGoogle Scholar |
Medeiros CD, Scoffoni C, John GP, Bartlett MK, Inman-Narahari F, Ostertag R, Cordell S, Giardina C, Sack L (2019) An extensive suite of functional traits distinguishes Hawaiian wet and dry forests and enables prediction of species vital rates. Functional Ecology 33, 712–734.
| An extensive suite of functional traits distinguishes Hawaiian wet and dry forests and enables prediction of species vital rates.Crossref | GoogleScholarGoogle Scholar |
Nolan RH, Fairweather KA, Tarin T, Santini NS, Cleverly J, Faux R, Eamus D (2017) Divergence in plant water-use strategies in semiarid woody species. Functional Plant Biology 44, 1134–1146.
| Divergence in plant water-use strategies in semiarid woody species.Crossref | GoogleScholarGoogle Scholar | 32480639PubMed |
Nowak EJ, Martin CE (1997) Physiological and anatomical responses to water deficits in the CAM epiphyte Tillandsia ionantha (Bromeliaceae). International Journal of Plant Sciences 158, 818–826.
| Physiological and anatomical responses to water deficits in the CAM epiphyte Tillandsia ionantha (Bromeliaceae).Crossref | GoogleScholarGoogle Scholar |
Phillips OL, Aragão LEOC, Lewis SL, Fisher JB, Lloyd J, López-gonzález G, Malhi Y, Monteagudo A, Peacock J, Quesada CA, et al (2009) Drought Sensitivity of the Amazon Rainforest. Science 323, 1344–1347.
| Drought Sensitivity of the Amazon Rainforest.Crossref | GoogleScholarGoogle Scholar | 19265020PubMed |
Popp M, Kramer D, Lee H, Diaz M, Ziegler H, Lüttge U (1987) Crassulacean acid metabolism in tropical dicotyledonous trees of the genus Clusia. Trees 1, 238–247.
| Crassulacean acid metabolism in tropical dicotyledonous trees of the genus Clusia.Crossref | GoogleScholarGoogle Scholar |
Roberts A, Griffiths H, Borland AM, Reinert F (1996) Is crassulacean acid metabolism activity in sympatric species of hemi-epiphytic stranglers such as Clusia related to carbon cycling as a photoprotective process? Oecologia 106, 28–38.
| Is crassulacean acid metabolism activity in sympatric species of hemi-epiphytic stranglers such as Clusia related to carbon cycling as a photoprotective process?Crossref | GoogleScholarGoogle Scholar | 28307154PubMed |
Schmidt JE, Kaiser WM (1987) Response of the succulent leaves of Peperomia magnoliaefolia to Dehydration. Plant Physiology 83, 190–194.
| Response of the succulent leaves of Peperomia magnoliaefolia to Dehydration.Crossref | GoogleScholarGoogle Scholar | 16665200PubMed |
Schulte PJ, Nobel PS (1989) Responses of a CAM plant to drought and rainfall: capacitance and osmotic pressure influences on water movement. Journal of Experimental Botany 40, 61–70.
| Responses of a CAM plant to drought and rainfall: capacitance and osmotic pressure influences on water movement.Crossref | GoogleScholarGoogle Scholar |
Scoffoni C, McKown AD, Rawls M, Sack L (2012) Dynamics of leaf hydraulic conductance with water status: Quantification and analysis of species differences under steady state. Journal of Experimental Botany 63, 643–658.
| Dynamics of leaf hydraulic conductance with water status: Quantification and analysis of species differences under steady state.Crossref | GoogleScholarGoogle Scholar | 22016424PubMed |
Scoffoni C, Albuquerque C, Brodersen CR, Townes SV, John GP, Bartlett MK, Buckley TN, McElrone AJ, Sack L (2017) Outside-xylem vulnerability, not xylem embolism, controls leaf hydraulic decline during dehydration. Plant Physiology 173, 1197–1210.
| Outside-xylem vulnerability, not xylem embolism, controls leaf hydraulic decline during dehydration.Crossref | GoogleScholarGoogle Scholar | 28049739PubMed |
Shameer S, Baghalian K, Cheung CYM, Ratcliffe RG, Sweetlove LJ (2018) Computational analysis of the productivity potential of CAM. Nature Plants 4, 165–171.
| Computational analysis of the productivity potential of CAM.Crossref | GoogleScholarGoogle Scholar | 29483685PubMed |
Silvera K, Lasso E (2016) Ecophysiology and crassulacean acid metabolism of tropical epiphytes. In ‘Tropical tree physiology’, 6th edn. (Eds G Goldstein, LS Santiago) pp. 25–43. (Springer)
Silvera K, Santiago LS, Cushman JC, Winter K (2009) Crassulacean acid metabolism and epiphytism linked to adaptive radiations in the Orchidaceae. Plant Physiology 149, 1838–1847.
| Crassulacean acid metabolism and epiphytism linked to adaptive radiations in the Orchidaceae.Crossref | GoogleScholarGoogle Scholar | 19182098PubMed |
Smith JAC, Lüttge U (1985) Day-night changes in leaf water relations associated with the rhythm of crassulacean acid metabolism in Kalanchoë daigremontiana. Planta 163, 272–282.
| Day-night changes in leaf water relations associated with the rhythm of crassulacean acid metabolism in Kalanchoë daigremontiana.Crossref | GoogleScholarGoogle Scholar |
Smith JAC, Schulte PJ, Nobel PS (1987) Water flow and water storage in Agave deserti: osmotic implications of crassulacean acid metabolism. Plant, Cell & Environment 10, 639–648.
| Water flow and water storage in Agave deserti: osmotic implications of crassulacean acid metabolism.Crossref | GoogleScholarGoogle Scholar |
Tinoco Ojanguren C, Vázquez Yanes C (1983) Especies CAM en la selva húmeda tropical de los Tuxtlas, Veracruz. Boletín de la Sociedad Botánica de México 45, 150–153.
Trueba S, Pan R, Scoffoni C, John GP, Davis SD, Sack L (2019) Thresholds for leaf damage due to dehydration: declines of hydraulic function, stomatal conductance and cellular integrity precede those for photochemistry. New Phytologist 223, 134–149.
| Thresholds for leaf damage due to dehydration: declines of hydraulic function, stomatal conductance and cellular integrity precede those for photochemistry.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 | 30810162PubMed |
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 | 24642847PubMed |
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 | 32689140PubMed |
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 | 18440928PubMed |
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, Garcia M, Virgo A, Holtum JAM (2019) Operating at the very low end of the crassulacean acid metabolism spectrum: Sesuvium portulacastrum (Aizoaceae). Journal of Experimental Botany 70, 6561–6570.
| Operating at the very low end of the crassulacean acid metabolism spectrum: Sesuvium portulacastrum (Aizoaceae).Crossref | GoogleScholarGoogle Scholar | 30535159PubMed |
Zhang Y-J, Rockwell FE, Graham AC, Alexander T, Holbrook NM (2016) Reversible Leaf Xylem Collapse: A Potential “Circuit Breaker” against Cavitation. Plant Physiology 172, 2261–2274.
| Reversible Leaf Xylem Collapse: A Potential “Circuit Breaker” against Cavitation.Crossref | GoogleScholarGoogle Scholar | 27733514PubMed |