Concerted anatomical change associated with crassulacean acid metabolism in the Bromeliaceae
Jamie MalesDepartment of Plant Sciences, University of Cambridge, Cambridge, UK. Email: jamie_males@hotmail.com
Functional Plant Biology 45(7) 681-695 https://doi.org/10.1071/FP17071
Submitted: 14 March 2017 Accepted: 5 January 2018 Published: 8 February 2018
Abstract
Crassulacean acid metabolism (CAM) is a celebrated example of convergent evolution in plant ecophysiology. However, many unanswered questions surround the relationships among CAM, anatomy and morphology during evolutionary transitions in photosynthetic pathway. An excellent group in which to explore these issues is the Bromeliaceae, a diverse monocot family from the Neotropics in which CAM has evolved multiple times. Progress in the resolution of phylogenetic relationships among the bromeliads is opening new and exciting opportunities to investigate how evolutionary changes in leaf structure has tracked, or perhaps preceded, photosynthetic innovation. This paper presents an analysis of variation in leaf anatomical parameters across 163 C3 and CAM bromeliad species, demonstrating a clear divergence in the fundamental aspects of leaf structure in association with the photosynthetic pathway. Most strikingly, the mean volume of chlorenchyma cells of CAM species is 22 times higher than that of C3 species. In two bromeliad subfamilies (Pitcairnioideae and Tillandsioideae), independent transitions from C3 to CAM are associated with increased cell succulence, whereas evolutionary trends in tissue thickness and leaf air space content differ between CAM origins. Overall, leaf anatomy is clearly and strongly coupled with the photosynthetic pathway in the Bromeliaceae, where the independent origins of CAM have involved significant anatomical restructuring.
Additional keywords: functional anatomy, succulence, vascular epiphytes, xerophytism.
References
Barfuss MHJ, Till W, Leme EMC, Pinzón JP, Manzanares JM, Halbritter H, Samuel R, Brown GK (2016) Taxonomic revision of Bromeliaceae subfam. Tillandsioideae based on a multi-locus DNA sequence phylogeny and morphology. Phytotaxa 279, 1–97.| Taxonomic revision of Bromeliaceae subfam. Tillandsioideae based on a multi-locus DNA sequence phylogeny and morphology.Crossref | GoogleScholarGoogle Scholar |
Barow M (2006) Endopolyploidy in seed plants. BioEssays 28, 271–281.
| Endopolyploidy in seed plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtVeju7s%3D&md5=7d4b6b38e26172969593a6b28fa64767CAS |
Beltrán JD, Lasso E, Madriñán S, Virgo A, Winter K (2013) Juvenile tank-bromeliads lacking tanks: do they engage in CAM photosynthesis? Photosynthetica 51, 55–62.
| Juvenile tank-bromeliads lacking tanks: do they engage in CAM photosynthesis?Crossref | GoogleScholarGoogle Scholar |
Benzing DH (2000) ‘Bromeliaceae: profile of an adaptive radiation.’ (Cambridge University Press: Cambridge, UK)
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 | 1:CAS:528:DyaK1cXjvVKrs78%3D&md5=4ff0684066e47f1cc657b3aed0fb43edCAS |
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=5413e84a1d5b4d08fe4c2368a5da4846CAS |
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 | 1:CAS:528:DC%2BC2cXivFCmsb4%3D&md5=20001be9e856aac5ac71a9169fbf44e6CAS |
Braun P, Winkelmann T (2016) Flow cytometric analyses of somatic and pollen nuclei in midday flowers (Aizoaceae). Caryologia 69, 303–314.
Butcher D, Gouda E (2016) The new Bromeliad Taxon list. Available at http://botu07.bio.uu.nl/bcg/taxonList.php
Carvalho V, Abreu ME, Mercier H, Nievola CC (2017) Adjustments in CAM and enzymatic scavenging of H2O2 in juvenile plants of the epiphytic bromeliad Guzmania monostachia as affected by drought and rewatering. Plant Physiology and Biochemistry 113, 32–39.
| Adjustments in CAM and enzymatic scavenging of H2O2 in juvenile plants of the epiphytic bromeliad Guzmania monostachia as affected by drought and rewatering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXitFentrw%3D&md5=2991019f42951d878e9e3405ee02b686CAS |
Christopher JT, Holtum JAM (1998) Carbohydrate partitioning in the leaves of Bromeliaceae performing C3 photosynthesis or crassulacean acid metabolism. Plant Physiology 25, 371–376.
Cockburn W, Ting IP, Sternberg LO (1979) Relationships between stomatal behaviour and internal carbon dioxide concentration in crassulacean acid metabolism plants. Plant Physiology 63, 1029–1032.
| Relationships between stomatal behaviour and internal carbon dioxide concentration in crassulacean acid metabolism plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXkslWrt7w%3D&md5=36b84e5290a12266c3742515effa49e6CAS |
Constable JVH, Longstreth DJ (1994) Aerenchyma carbon dioxide can be assimilated in Typha latifolia L. leaves. Plant Physiology 106, 1065–1072.
| Aerenchyma carbon dioxide can be assimilated in Typha latifolia L. leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitlentrw%3D&md5=d8535e4a76358ebbe7aec2e2939f8728CAS |
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=d06e22fbf6ef305144f22b059146d96cCAS |
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 |
Edwards EJ, Ogburn RM (2012) Angiosperm responses to a low-CO2 world: CAM and C4 photosynthesis as parallel evolutionary trajectories. International Journal of Plant Sciences 173, 724–733.
| Angiosperm responses to a low-CO2 world: CAM and C4 photosynthesis as parallel evolutionary trajectories.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVOqur%2FI&md5=715e063dbf489507b86128cac412b117CAS |
Escobedo-Sarti J, Ramírez I, Leopardi C, Carnevali G, Magallón S, Duno R, Mondragón D (2013) A phylogeny of Bromeliaceae (Poales, Monocotyledoneae) derived from an evaluation of nine supertree methods. Journal of Systematics and Evolution 51, 743–757.
| A phylogeny of Bromeliaceae (Poales, Monocotyledoneae) derived from an evaluation of nine supertree methods.Crossref | GoogleScholarGoogle Scholar |
Evans TM, Jabaily RS, de Faria APG, de Sousa LOF, Wendt T, Brown GK (2015) Phylogenetic relationships in Bromeliaceae subfamily Bromelioideae based on chloroplast DNA sequence data. Systematic Botany 40, 116–128.
| Phylogenetic relationships in Bromeliaceae subfamily Bromelioideae based on chloroplast DNA sequence data.Crossref | GoogleScholarGoogle Scholar |
Fetene M, Lüttge U (1991) Environmental influences on carbon recycling in a terrestrial CAM bromeliad, Bromelia humilis Jacq. Journal of Experimental Botany 42, 25–31.
| Environmental influences on carbon recycling in a terrestrial CAM bromeliad, Bromelia humilis Jacq.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhtl2ru7g%3D&md5=f103dc08a28c4378f599c3e374f3222fCAS |
Fioretto A, Alfani A (1988) Anatomy of succulence and CAM in 15 species of Senecio. Botanical Gazette 149, 142–152.
| Anatomy of succulence and CAM in 15 species of Senecio.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXmtVygtb8%3D&md5=8bf788f98ec240bada58503a3ea6de9eCAS |
Freschi L, Takahashi CA, Cambui CA, Semprebom TR, Cruz AB, Mioto PT, Versieux L, Calvente A, Latansio-Aidar SR, Aidar MP, Mercier H (2010) Specific leaf areas of the tank bromeliad Guzmania monostachia perform distinct functions in response to water shortage. Journal of Plant Physiology 167, 526–533.
| Specific leaf areas of the tank bromeliad Guzmania monostachia perform distinct functions in response to water shortage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlt1Krsro%3D&md5=0560bb4e684b226d259f15ddd33b63edCAS |
Gibson AC (1982) The anatomy of succulence. In ‘Crassulacean acid metabolism’. (Eds IP Ting, M Gibbs) pp. 1–30. (American Society of Plant Physiologists, Rockville, MD)
Givnish TJ, Barfuss MHJ, Van Ee B, Riina R, Schulte K, Horres R, Gonsiska PA, Jabaily RS, Crayn DM, Smith JAC, Winter K, Brown GK, Evans TM, Holst BK, Luther H, Till W, Zizka G, Berry PE, Systma KJ (2011) Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: insights from an eight-locus plastid phylogeny. American Journal of Botany 98, 872–895.
| Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: insights from an eight-locus plastid phylogeny.Crossref | GoogleScholarGoogle Scholar |
Givnish TJ, Barfuss MHJ, Van Ee B, Riina R, Schulte K, Horres R, Gonsiska PA, Jabaily RS, Crayn DM, Smith JAC, Winter K, Brown GK, Evans TM, Holst BK, Luther H, Till W, Zizka G, Berry PE, Systma KJ (2014) Adaptive radiation, correlated and contingent evolution, and net species diversification in Bromeliaceae. Molecular Phylogenetics and Evolution 71, 55–78.
| Adaptive radiation, correlated and contingent evolution, and net species diversification in Bromeliaceae.Crossref | GoogleScholarGoogle Scholar |
Grant JR (1993) True Tillandsias misplaced in Vriesea (Bromeliaceae: Tillandsioideae). Phytologia 75, 170–175.
| True Tillandsias misplaced in Vriesea (Bromeliaceae: Tillandsioideae).Crossref | GoogleScholarGoogle Scholar |
Griffiths H (1988) Carbon balance during CAM: an assessment of respiratory CO2 recycling in the epiphytic bromeliad Aechmea nudicaulis and Aechmea fendleri. Plant, Cell & Environment 11, 603–611.
| Carbon balance during CAM: an assessment of respiratory CO2 recycling in the epiphytic bromeliad Aechmea nudicaulis and Aechmea fendleri.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhsFWgtb0%3D&md5=8900c4c0da935b7727fe1e9a28d44b95CAS |
Griffiths H, Smith JAC (1983) Photosynthetic pathways in the Bromeliaceae of Trinidad: relations between life-forms, habitat preference and the occurrence of CAM. Oecologia 60, 176–184.
| Photosynthetic pathways in the Bromeliaceae of Trinidad: relations between life-forms, habitat preference and the occurrence of CAM.Crossref | GoogleScholarGoogle Scholar |
Guralnick LJ, Jackson MD (2001) The occurrence and phylogenetics of crassulacean acid metabolism in the Portulacaceae. International Journal of Plant Sciences 162, 257–262.
| The occurrence and phylogenetics of crassulacean acid metabolism in the Portulacaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtFKgtLc%3D&md5=b0bb0bbd1f20abe9611354d230b82b91CAS |
Hancock L, Edwards EJ (2014) Phylogeny and the inference of evolutionary trajectories. Journal of Experimental Botany 65, 3491–3498.
| Phylogeny and the inference of evolutionary trajectories.Crossref | GoogleScholarGoogle Scholar |
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=e789bc513918396aec4e1df2d598acddCAS |
Herrera A, Martin CE, Tezara W, Ballestrini C, Medina E (2010) Induction by drought of crassulacean acid metabolism in the terrestrial bromeliad, Puya floccosa. Photosynthetica 48, 383–388.
| Induction by drought of crassulacean acid metabolism in the terrestrial bromeliad, Puya floccosa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlSjtrnK&md5=d24ae8e308de7b6604874455fb823ff2CAS |
Heyduk K, McKain MR, Lalani F, Leebens-Mack J (2016) Evolution of a CAM anatomy predates the origin of Crassulacean acid metabolism in the Agavoideae (Asparagaceae). Molecular Phylogenetics and Evolution 105, 102–113.
| Evolution of a CAM anatomy predates the origin of Crassulacean acid metabolism in the Agavoideae (Asparagaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsVyitrbF&md5=cc3978aae771aeb42a20ce8cc743647bCAS |
Holthe PA, Patel A, Ting IP (1992) The occurrence of CAM in Peperomia. Selbyana 13, 77–87.
Horres R, Zizka G, Kahl G, Weising K (2000) Molecular phylogenetics of Bromeliaceae: evidence from trnL(UAA) intron sequences of the chloroplast genome. Plant Biology 2, 306–315.
| Molecular phylogenetics of Bromeliaceae: evidence from trnL(UAA) intron sequences of the chloroplast genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXksFSktL0%3D&md5=f325f0e745fa8a1833e9cca5571a6a0bCAS |
Horres R, Schulte K, Weising K, Zizka G (2007) Systematics of Bromelioideae (Bromeliaceae) – evidence from molecular and anatomical studies. Aliso 23, 27–43.
| Systematics of Bromelioideae (Bromeliaceae) – evidence from molecular and anatomical studies.Crossref | GoogleScholarGoogle Scholar |
Jabaily RS, Sytsma KJ (2010) Phylogenetics of Puya (Bromeliaceae): placement, major lineages, and evolution of Chilean species. American Journal of Botany 97, 337–356.
| Phylogenetics of Puya (Bromeliaceae): placement, major lineages, and evolution of Chilean species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXivVChsLY%3D&md5=b3215a343744d34ebabada52ec5ed9edCAS |
Jabaily RS, Sytsma KJ (2013) Historical biogeography and life-history evolution of Andean Puya (Bromeliaceae). Botanical Journal of the Linnean Society 171, 201–224.
| Historical biogeography and life-history evolution of Andean Puya (Bromeliaceae).Crossref | GoogleScholarGoogle Scholar |
Keeley JE, Rundel PW (2003) Evolution of CAM and C4 carbon-concentrating mechanisms. International Journal of Plant Sciences 164, S55–S77.
| Evolution of CAM and C4 carbon-concentrating mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmt1Wht70%3D&md5=8a3a5225de962304901694fe31344223CAS |
Krapp F, Pinangé DSB, Benko-Iseppon AM, Leme EMC, Weising K (2014) Phylogeny and evolution of Dyckia (Bromeliaceae) inferred from chloroplast and nuclear sequences. Plant Systematics and Evolution 300, 1591–1614.
Lange OL, Medina E (1979) Stomata of the CAM plant Tillandsia recurvata respond directly to humidity. Oecologia 40, 357–363.
| Stomata of the CAM plant Tillandsia recurvata respond directly to humidity.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC1cznvVWhtQ%3D%3D&md5=79dfa113014498260e13357b0611aaa7CAS |
Loeschen VS, Martin CE, Smith M, Eder SL (1993) Leaf anatomy and CO2 recycling during crassulacean acid metabolism in twelve epiphytic species of Tillandsia (Bromeliaceae). International Journal of Plant Sciences 154, 100–106.
| Leaf anatomy and CO2 recycling during crassulacean acid metabolism in twelve epiphytic species of Tillandsia (Bromeliaceae).Crossref | GoogleScholarGoogle Scholar |
Lüttge U (2002) CO2-concentrating: consequences in crassulacean acid metabolism. Journal of Experimental Botany 53, 2131–2142.
| CO2-concentrating: consequences in crassulacean acid metabolism.Crossref | GoogleScholarGoogle Scholar |
Lüttge U, Ball E (1977) Water relation parameters of the CAM plant Kalanchoë daigremontiana in relation to diurnal malate oscillations. Oecologia 31, 85–94.
| Water relation parameters of the CAM plant Kalanchoë daigremontiana in relation to diurnal malate oscillations.Crossref | GoogleScholarGoogle Scholar |
Lüttge U, Nobel PS (1984) Day–night variations in malate concentration, osmotic pressure, and hydrostatic pressure in Cereus validus. Plant Physiology 75, 804–807.
| Day–night variations in malate concentration, osmotic pressure, and hydrostatic pressure in Cereus validus.Crossref | GoogleScholarGoogle Scholar |
Lüttge U, Stimmel K-H, Smith JAC, Griffiths H (1986) Comparative ecophysiology of CAM and C3 bromeliads. II. Field measurements of gas exchange of CAM bromeliads in the humid tropics. Plant, Cell & Environment 9, 377–383.
| Comparative ecophysiology of CAM and C3 bromeliads. II. Field measurements of gas exchange of CAM bromeliads in the humid tropics.Crossref | GoogleScholarGoogle Scholar |
Males J (2016) Think tank: water relations of the Bromeliaceae in their evolutionary context. Botanical Journal of the Linnean Society 181, 415–440.
| Think tank: water relations of the Bromeliaceae in their evolutionary context.Crossref | GoogleScholarGoogle Scholar |
Males J (2017) Secrets of succulence. Journal of Experimental Botany 68, 2121–2134.
| Secrets of succulence.Crossref | GoogleScholarGoogle Scholar |
Males J, Griffiths H (2017) Stomatal biology of CAM plants. Plant Physiology 174, 550–560.
| Stomatal biology of CAM plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXht1Cru7%2FL&md5=3b7592c886b9afc622019b66a540cef7CAS |
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 | 1:CAS:528:DC%2BC2sXhvF2gs7nO&md5=097033209041a00c2910c09942f5bc64CAS |
Martin CE (1994) Physiological ecology of the Bromeliaceae. Botanical Review 60, 1–82.
| Physiological ecology of the Bromeliaceae.Crossref | GoogleScholarGoogle Scholar |
Martin CE, Adams WW (1987) Crassulacean acid metabolism, CO2-recycling, and tissue desiccation in the Mexican epiphyte Tillandsia schiedeana Steud (Bromeliaceae). Photosynthesis Research 11, 237–244.
| Crassulacean acid metabolism, CO2-recycling, and tissue desiccation in the Mexican epiphyte Tillandsia schiedeana Steud (Bromeliaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXksFGqtLg%3D&md5=595da1f0cb7997d0286cb18c619bbd34CAS |
Martorell C, Ezcurra E (2007) The narrow-leaf syndrome: a functional and evolutionary approach to the form of fog-harvesting rosette plants. Oecologia 151, 561–573.
| The narrow-leaf syndrome: a functional and evolutionary approach to the form of fog-harvesting rosette plants.Crossref | GoogleScholarGoogle Scholar |
Maxwell C, Griffiths H, Borland AM, Broadmeadow MSJ, McDavid CR (1992) Photoinhibitory responses of the epiphytic bromeliad Guzmania monostachia during the dry season in Trinidad maintain photochemical integrity under adverse conditions. Plant, Cell & Environment 15, 37–47.
| Photoinhibitory responses of the epiphytic bromeliad Guzmania monostachia during the dry season in Trinidad maintain photochemical integrity under adverse conditions.Crossref | GoogleScholarGoogle Scholar |
Maxwell C, Griffiths H, Young AJ (1994) Photosynthetic acclimation to light regime and water stress by the C3-CAM epiphyte Guzmania monostachia: gas-exchange characteristics, photochemical efficiency and the xanthophyll cycle. Functional Ecology 8, 746–754.
| Photosynthetic acclimation to light regime and water stress by the C3-CAM epiphyte Guzmania monostachia: gas-exchange characteristics, photochemical efficiency and the xanthophyll cycle.Crossref | GoogleScholarGoogle Scholar |
Maxwell C, Griffiths H, Borland AM, Young AJ, Broadmeadow MSJ, Fordham MC (1995) Short-term photosynthetic responses of the C3-CAM epiphyte Guzmania monostachia var. monostachia to tropical seasonal transitions under field conditions. Australian Journal of Plant Physiology 22, 771–781.
| Short-term photosynthetic responses of the C3-CAM epiphyte Guzmania monostachia var. monostachia to tropical seasonal transitions under field conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpt12hs78%3D&md5=a68865989870577a4df2d51ce39429aeCAS |
Maxwell K, von Caemmerer S, Evans JR (1997) Is a low internal conductance to CO2 diffusion a consequence of succulence in plants with crassulacean acid metabolism? Australian Journal of Plant Physiology 24, 777–786.
| Is a low internal conductance to CO2 diffusion a consequence of succulence in plants with crassulacean acid metabolism?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtVGjtLg%3D&md5=b15e8375753ef720c743d355e5498abbCAS |
Maxwell K, Marrison JL, Leech RM, Griffiths H, Horton P (1999) Chloroplast acclimation in leaves of Guzmania monostachia in response to high light. Plant Physiology 121, 89–96.
| Chloroplast acclimation in leaves of Guzmania monostachia in response to high light.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtFGlsLo%3D&md5=a2c74c51a65dbd0df76f333be717eac2CAS |
McWilliams EL (1970) Comparative rates of dark CO2 uptake and acidification in the Bromeliaceae, Orchidaceae, and Euphorbiaceae. Botanical Gazette 131, 285–290.
| Comparative rates of dark CO2 uptake and acidification in the Bromeliaceae, Orchidaceae, and Euphorbiaceae.Crossref | GoogleScholarGoogle Scholar |
Medina E (1974) Dark CO2 fixation, habitat preference and evolution within the Bromeliaceae. Evolution 28, 677–686.
Medina E, Delgado M, Troughton JH, Medina JD (1977) Physiological ecology of CO2 fixation in Bromeliaceae. Flora 166, 137–152.
| Physiological ecology of CO2 fixation in Bromeliaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXhvVKju7w%3D&md5=3b29cecba3b43682745b23cc6bc008e4CAS |
Ming R, VanBuren R, Wai CM, Tang H, Schatz MC, Bowers JE, Lyons E, Wang M-L, Chen J, Biggers E, Zhang J, Huang L, Zhang L, Miao W, Zhang J, Ye Z, Miao C, Lin Z, Wang H, Zhou H, et al (2015) The pineapple genome and the evolution of CAM photosynthesis. Nature Genetics 47, 1435–1442.
| The pineapple genome and the evolution of CAM photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhslKgt7nN&md5=4a88c5523033a13c273f16c9972cb10fCAS |
Mishiba K, Mii M (2000) Polysomaty analysis in diploid and tetraploid Portulaca grandiflora. Plant Science 156, 213–219.
| Polysomaty analysis in diploid and tetraploid Portulaca grandiflora.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsFCjtro%3D&md5=db120d0c4478b6fce3c3ed11f3ae79efCAS |
Nelson EA, Sage RF (2008) Functional constraints of CAM leaf anatomy: tight cell packing is associated with increased CAM function across a gradient of CAM expression. Journal of Experimental Botany 59, 1841–1850.
| Functional constraints of CAM leaf anatomy: tight cell packing is associated with increased CAM function across a gradient of CAM expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtleltLo%3D&md5=e57ceb18e171488ef894d3b9139d99edCAS |
Nelson EA, Sage TL, Sage RF (2005) Functional leaf anatomy of plants with crassulacean acid metabolism. Functional Plant Biology 32, 409–419.
| Functional leaf anatomy of plants with crassulacean acid metabolism.Crossref | GoogleScholarGoogle Scholar |
Nyffeler R, Eggli U, Ogburn RM, Edwards EJ (2008) Variations on a theme: repeated evolution of succulent life forms in the Portulacineae (Caryophyllales). Haseltonia 14, 26–36.
| Variations on a theme: repeated evolution of succulent life forms in the Portulacineae (Caryophyllales).Crossref | GoogleScholarGoogle Scholar |
Ogburn RM, Edwards EJ (2010) The ecological water-use strategies of succulent plants. In ‘Advances in botanical research, Vol. 55’. (Eds J-C Kader, M Delseny) pp. 179–225. (Academic Press: Burlington, NJ)
Olivares E, Urich R, Montes G, Coronel I, Herrera A (1984) Occurrence of crassulacean acid metabolism in Cissus trifoliata L. (Vitaceae). Oecologia 61, 358–362.
| Occurrence of crassulacean acid metabolism in Cissus trifoliata L. (Vitaceae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC1cznvFGksA%3D%3D&md5=49f790e8ee49532a3dff2b6e4517e432CAS |
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=a1f537b05e0927270da9ee7ce4e34728CAS |
Palma-Silva C, Leal BSS, Chaves CJN, Fay MF (2016) Advances in and perspectives on evolution in Bromeliaceae. Botanical Journal of the Linnean Society 181, 305–322.
| Advances in and perspectives on evolution in Bromeliaceae.Crossref | GoogleScholarGoogle Scholar |
Pierce S, Winter K, Griffiths H (2002a) Carbon isotope ratio and the extent of daily CAM use by Bromeliaceae. New Phytologist 156, 75–83.
| Carbon isotope ratio and the extent of daily CAM use by Bromeliaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvFyhtr0%3D&md5=54d700c47736d88d861d3a80de1846bfCAS |
Pierce S, Winter K, Griffiths H (2002b) The role of CAM in high rainfall cloud forests: an in situ comparison of photosynthetic pathways in Bromeliaceae. Plant, Cell & Environment 25, 1181–1189.
| The role of CAM in high rainfall cloud forests: an in situ comparison of photosynthetic pathways in Bromeliaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVWitLo%3D&md5=660a5a26039ae96bfe673a40beb125b2CAS |
Pinangé DSB, Krapp F, Zizka G, Silvestro D, Leme EMC, Weising K, Benko-Iseppon AM (2017) Molecular phylogenetics, historical biogeography and character evolution in Dyckia (Bromeliaceae, Pitcairnioideae). Botanical Journal of the Linnean Society
Quezada IM, Zotz G, Gianoli E (2014) Latitudinal variation in the degree of crassulacean acid metabolism in Puya chilensis. Plant Biology 16, 848–852.
| Latitudinal variation in the degree of crassulacean acid metabolism in Puya chilensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVSqtbrN&md5=f43b4b9f181611d83b528f83bfefeb82CAS |
R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Austria. Available at http://www.R-project.org
Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3, 217–223.
| phytools: an R package for phylogenetic comparative biology (and other things).Crossref | GoogleScholarGoogle Scholar |
Reyes-García C, Mejia-Chang M, Griffiths H (2012) High but not dry: diverse epiphytic bromeliad adaptations to exposure within a seasonally dry tropical forest community. New Phytologist 193, 745–754.
| High but not dry: diverse epiphytic bromeliad adaptations to exposure within a seasonally dry tropical forest community.Crossref | GoogleScholarGoogle Scholar |
Ripley BS, Abraham T, Klak C, Cramer MD (2013) How succulence leaves of Aizoaceae avoid mesophyll conductance limitations of photosynthesis and survive drought. Journal of Experimental Botany 64, 5485–5496.
| How succulence leaves of Aizoaceae avoid mesophyll conductance limitations of photosynthesis and survive drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXotleq&md5=f5c640b5158b20bb0e458a78791e0868CAS |
Rodrigues MA, Hamachi L, Mioto PT, Purgatto E, Mercier H (2016) Implications of leaf ontogeny on drought-induced gradients of CAM expression and ABA levels in rosettes of the epiphytic tank bromeliad Guzmania monostachia. Plant Physiology and Biochemistry 108, 400–411.
| Implications of leaf ontogeny on drought-induced gradients of CAM expression and ABA levels in rosettes of the epiphytic tank bromeliad Guzmania monostachia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhtl2murbL&md5=ccdb7468ea3f160eec67378f72a7add6CAS |
Sage RF, Khoshravesh R (2016) Passive CO2 concentration in higher plants. Current Opinion in Plant Biology 31, 58–65.
| Passive CO2 concentration in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XlsF2hsr0%3D&md5=94275f80725d4f015c521e3d80d05713CAS |
Saraiva DP, Mantovani A, Forzza RC (2015) Insights into the evolution of Pitcairnia (Pitcairnioideae-Bromeliaceae), based on morphological evidence. Systematic Botany 40, 726–736.
| Insights into the evolution of Pitcairnia (Pitcairnioideae-Bromeliaceae), based on morphological evidence.Crossref | GoogleScholarGoogle Scholar |
Schulte K, Barfuss MHJ, Zizka G (2009) Phylogeny of Bromelioideae (Bromeliaceae) inferred from nuclear and plastid DNA loci reveals the evolution of the tank habit within the subfamily. Molecular Phylogenetics and Evolution 51, 327–339.
| Phylogeny of Bromelioideae (Bromeliaceae) inferred from nuclear and plastid DNA loci reveals the evolution of the tank habit within the subfamily.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltFemur8%3D&md5=0b24dea987c02158c34672b27c71e93aCAS |
Schütz N, Krapp F, Wagner N, Weising K (2016) Phylogenetics of Pitcairnioideae s.s. (Bromeliaceae): evidence from nuclear and plastid DNA sequence data. Botanical Journal of the Linnean Society 181, 323–342.
| Phylogenetics of Pitcairnioideae s.s. (Bromeliaceae): evidence from nuclear and plastid DNA sequence data.Crossref | GoogleScholarGoogle Scholar |
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=228aefc3a10f7f639e00317ad06cd330CAS |
Silvera K, Neubig KM, Whitten WM, Williams NH, Winter K, Cushman JC (2010a) Evolution along the crassulacean acid metabolism continuum. Functional Plant Biology 37, 995–1010.
| Evolution along the crassulacean acid metabolism continuum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlaqtL%2FN&md5=f071e401a48ad7d6185f1fc3d930c0adCAS |
Silvera K, Santiago LS, Cushman JC, Winter K (2010b) 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 |
Silvestro D, Zizka G, Schulte K (2014) Disentangling the effects of key innovations on the diversification of Bromelioideae (Bromeliaceae). Evolution 68, 163–175.
| Disentangling the effects of key innovations on the diversification of Bromelioideae (Bromeliaceae).Crossref | GoogleScholarGoogle Scholar |
Smith JAC, Heuer S (1981) Determination of the volume of intercellular spaces in leaves and some values for CAM plants. Annals of Botany 48, 915–917.
| Determination of the volume of intercellular spaces in leaves and some values for CAM plants.Crossref | GoogleScholarGoogle Scholar |
Smith JAC, Griffiths H, Lüttge U (1986) Comparative ecophysiology of CAM and C3 bromeliads. I. The ecology of the Bromeliaceae in Trinidad. Plant, Cell & Environment 9, 359–376.
| Comparative ecophysiology of CAM and C3 bromeliads. I. The ecology of the Bromeliaceae in Trinidad.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 |
Teeri JA, Tonsor SJ, Turner M (1981) Leaf thickness and carbon isotope composition in the Crassulaceae. Oecologia 50, 367–369.
| Leaf thickness and carbon isotope composition in the Crassulaceae.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC1cznslGltg%3D%3D&md5=277ead47e2e868706d424a5c71cf7161CAS |
Tomlinson PB (1969) ‘Anatomy of the aonocotyledons. Vol. III. Commelinales–Zingiberales.’ (Ed. CR Metcalfe). (Clarendon Press: Oxford)
Virzo de Santo A, Alfani A, Russo G, Fioretto A (1983) Relationship between CAM and succulence in some species of Vitaceae and Piperaceae. International Journal of Plant Sciences 144, 342–346.
Wagner N, Silvestro D, Brie D, Ibisch PL, Zizka G, Weising K, Schulte K (2013) Spatio-temporal evolution of Fosterella (Bromeliaceae) in the Central Andean biodiversity hotspot. Journal of Biogeography 40, 869–880.
| Spatio-temporal evolution of Fosterella (Bromeliaceae) in the Central Andean biodiversity hotspot.Crossref | GoogleScholarGoogle Scholar |
Winter K, Holtum JAM (2002) How closely do the δ13C values of CAM plants reflect the proportion of CO2 fixed during day and night? Plant Physiology 129, 1843–1851.
| How closely do the δ13C values of CAM plants reflect the proportion of CO2 fixed during day and night?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xmtl2gtLs%3D&md5=b5a923cea21468a69a83265119d004a9CAS |
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, Smith JAC (1996) An introduction to crassulacean acid metabolism: Biochemical principles and ecological diversity. In ‘Crassulacean acid metabolism ’. (Eds K Winter K, JAC Smith). Springer.
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 | 1:CAS:528:DC%2BC2MXhsVChsr%2FJ&md5=30569ad6729ce0fb91a163659c867d9cCAS |
Xiong D, Flexas J, Yu T, Peng S, Huang J (2017) Leaf anatomy mediates coordination of leaf hydraulic conductance and mesophyll conductance to CO2 in Oryza. New Phytologist 213, 572–583.
| Leaf anatomy mediates coordination of leaf hydraulic conductance and mesophyll conductance to CO2 in Oryza.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XitFGgtLfN&md5=71bbdafe43e0e604b0cb3acbe067a6bbCAS |
Zambrano VAB, 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 |