Diurnal CO2 Assimilation Patterns in Nine Species of CAM-Type Succulent Plants

CO2 assimilation rate of Crassula hybrid `Himaturi', a succulent ornamental species with the crassulacean acid metabolism (CAM) photosynthetic pathway, was affected by light intensity (50, 100, 300 μmol·m–2·s–1), photoperiod (16/8, 8/16 h day/night), and temperature (30/25, 25/20 °C day/night). Maximum assimilation of CO2 occurred at 300 μmol·m–2·s–1 of diurnal irradiance, 16/8 h day/night photoperiod, and a day/night temperature of 30/25 °C. Diurnal CO2 assimilation patterns of nine succulent ornamental CAM species were evaluated (300 μmol·m–2 s–1, 35/25 °C day/night and a 16/8-h day/night photoperiod) for CO2 fixation. Of the nine ornamentals, Crassula `Himaturi' had the highest and Echeveria derembergii the lowest maximum CO2 absorption rate (13.0 vs 2.4 μmol kg–1·s–1), total nighttime (179.3 vs 13.4 mmol·kg–1), and 24 h total (200.6 vs 19.0 mmol·kg–1) absorption. Based on the CO2 assimilation patterns, the nine ornamentals were separated into two groups: 1) full CAM (Faucaria tigrina, Gasteria gracilis var. minima, Haworthia cymbiformis, and Haworthia fasciata); and 2) weakly CAM (Adromischus clarifolius, Crassula hybrids `Moonglow' and `Himaturi', E. derembergii, and Haworthia retusa).

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Is a Low Internal Conductance to CO2 Diffusion a Consequence of Succulence in Plants with Crassulacean Acid Metabolism?

Functional Plant Biology ◽

10.1071/pp97088 ◽

1997 ◽

Vol 24 (6) ◽

pp. 777 ◽

Cited By ~ 44

Author(s):

Kate Maxwell ◽

Susanne von Caemmerer ◽

John R. Evans

Keyword(s):

Crassulacean Acid Metabolism ◽

Acid Metabolism ◽

Ambient Air ◽

Co2 Assimilation ◽

Co2 Partial Pressure ◽

Co2 Diffusion ◽

Internal Conductance ◽

C3 Species ◽

Cam Species ◽

Transient Phases

Leaf internal conductance to CO2 (gi) from substomatal cavity to the carboxylation sites of Rubisco was measured in the leaf succulent CAM species, Kalanchoe daigremontiana Hamet et Perr. Measurements were made during Rubisco-mediated atmospheric C3 carboxylation in phase IV photosynthesis. Using simultaneous gas exchange and chlorophyll fluorescence techniques, internal conductance was calculated to be 0.05 mol m-2 s-1 bar-1 , when measured at both saturating and limiting light. This is one of the lowest recorded values for gi as compared to a range of C3 species with comparable Rubisco content and indicates a large diffusion limitation to atmospheric CO2 fixation through the C3 pathway in K. daigremontiana. In ambient air, CO2 partial pressure at the carboxylation sites of Rubisco was 109 µbar. Internal diffusion is limited by a thick leaf consisting of densely packed, succulent mesophyll with a small portion of airspace. We speculate that a low internal conductance to CO2 diffusion results from the compromise between a succulent mesophyll required for C4 acid storage and access for CO2 diffusion to both PEPC in the cytoplasm and Rubisco in the chloroplasts. Restricted diffusion of CO2 within the leaf makes CO2 assimilation less efficient during the transient phases of crassulacean acid metabolism.

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Concerted anatomical change associated with crassulacean acid metabolism in the Bromeliaceae

Functional Plant Biology ◽

10.1071/fp17071 ◽

2018 ◽

Vol 45 (7) ◽

pp. 681 ◽

Cited By ~ 10

Author(s):

Jamie Males

Keyword(s):

Crassulacean Acid Metabolism ◽

Acid Metabolism ◽

Leaf Structure ◽

Photosynthetic Pathway ◽

Evolutionary Transitions ◽

Strongly Coupled ◽

Plant Ecophysiology ◽

Evolutionary Changes ◽

Cam Species ◽

Analysis Of Variation

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.

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Shared expression of crassulacean acid metabolism (CAM) genes pre-dates the origin of CAM in the genus Yucca

Journal of Experimental Botany ◽

10.1093/jxb/erz105 ◽

2019 ◽

Vol 70 (22) ◽

pp. 6597-6609 ◽

Cited By ~ 7

Author(s):

Karolina Heyduk ◽

Jeremy N Ray ◽

Saaravanaraj Ayyampalayam ◽

Nida Moledina ◽

Anne Borland ◽

...

Keyword(s):

Crassulacean Acid Metabolism ◽

Acid Metabolism ◽

Expression Patterns ◽

Photosynthetic Pathway ◽

Similar Expression ◽

Cam Species

Although large differences in metabolism exist between C3 and CAM species, we find that many CAM genes have similar expression patterns regardless of photosynthetic pathway, suggesting ancestral propensity for CAM.

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Shared expression of Crassulacean acid metabolism (CAM) genes predates the origin of CAM in the genus Yucca

10.1101/371344 ◽

2018 ◽

Cited By ~ 2

Author(s):

Karolina Heyduk ◽

Jeremy N. Ray ◽

Saaravanaraj Ayyampalayam ◽

Nida Moledina ◽

Anne Borland ◽

...

Keyword(s):

Crassulacean Acid Metabolism ◽

Time Course ◽

Acid Metabolism ◽

Expression Profiles ◽

Expression Patterns ◽

Antioxidant Response ◽

Comparative Approach ◽

Photosynthetic Pathway ◽

Cam Species ◽

And Function

Highlight:Although large differences in metabolism exist between C3 and CAM species, we find that many CAM genes have shared expression patterns regardless of photosynthetic pathway, suggesting ancestral propensity for CAM.Abstract:Crassulacean acid metabolism (CAM) is a carbon-concentrating mechanism that has evolved numerous times across flowering plants and is thought to be an adaptation to water limited environments. CAM has been investigated from physiological and biochemical perspectives, but little is known about how plants evolve from C3 to CAM at the genetic or metabolic level. Here we take a comparative approach in analyzing time-course data of C3, CAM, and C3+CAM intermediate Yucca (Asparagaceae) species. RNA samples were collected over a 24-hour period from both well-watered and drought-stressed plants and were clustered based on time-dependent expression patterns. Metabolomic data reveals differences in carbohydrate metabolism and antioxidant response between the CAM and C3 species, suggesting changes to metabolic pathways are important for CAM evolution and function. However, all three species share expression profiles of canonical CAM pathway genes, regardless of photosynthetic pathway. Despite differences in transcript and metabolite profiles between the C3 and CAM species, shared time-structured expression of CAM genes in both CAM and C3Yucca species suggests ancestral expression patterns required for CAM may have predated its origin in Yucca.

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A perspective on crassulacean acid metabolism photosynthesis evolution of orchids on different continents: Dendrobium as a case study

Journal of Experimental Botany ◽

10.1093/jxb/erz461 ◽

2019 ◽

Vol 70 (22) ◽

pp. 6611-6619

Author(s):

Ming-He Li ◽

Ding-Kun Liu ◽

Guo-Qiang Zhang ◽

Hua Deng ◽

Xiong-De Tu ◽

...

Keyword(s):

Crassulacean Acid Metabolism ◽

Middle Miocene ◽

Acid Metabolism ◽

Flowering Plants ◽

Asian Clade ◽

Wide Range ◽

Cam Species ◽

Climatic Cooling ◽

Cam Photosynthesis

Abstract Members of the Orchidaceae, one of the largest families of flowering plants, evolved the crassulacean acid metabolism (CAM) photosynthesis strategy. It is thought that CAM triggers adaptive radiation into new niche spaces, yet very little is known about its origin and diversification on different continents. Here, we assess the prevalence of CAM in Dendrobium, which is one of the largest genera of flowering plants and found in a wide range of environments, from the high altitudes of the Himalayas to relatively arid habitats in Australia. Based on phylogenetic time trees, we estimated that CAM, as determined by δ 13C values less negative than –20.0‰, evolved independently at least eight times in Dendrobium. The oldest lineage appeared in the Asian clade during the middle Miocene, indicating the origin of CAM was associated with a pronounced climatic cooling that followed a period of aridity. Divergence of the four CAM lineages in the Asian clade appeared to be earlier than divergence of those in the Australasian clade. However, CAM species in the Asian clade are much less diverse (25.6%) than those in the Australasian clade (57.9%). These findings shed new light on CAM evolutionary history and the aridity levels of the paleoclimate on different continents.

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Resistance is useful: diurnal patterns of photosynthesis in C3 and crassulacean acid metabolism epiphytic bromeliads

Functional Plant Biology ◽

10.1071/pp01193 ◽

2002 ◽

Vol 29 (6) ◽

pp. 679 ◽

Cited By ~ 29

Author(s):

Kate Maxwell

Keyword(s):

Crassulacean Acid Metabolism ◽

Acid Metabolism ◽

Photosynthetic Electron Transport ◽

Co2 Assimilation ◽

Enzyme Activation ◽

Photon Flux ◽

Photon Flux Density ◽

Cam Plants ◽

Diurnal Patterns ◽

Rubisco Activation

This paper originates from a presentation at the IIIrd International Congress on Crassulacean Acid Metabolism, Cape Tribulation, Queensland, Australia, August 2001 Diurnal patterns of photosynthesis in response to environmental variables were investigated in an obligate C3 and a facultative C3-crassulacean acid metabolism (CAM) bromeliad species. A midday depression of photosynthesis occurred in both C3 groups, mediated as a decrease in stomatal conductance in response to increased vapour pressure difference. The response was associated with a reduction in Rubisco activation state during the period of maximum photon flux density. In contrast, the switch to CAM resulted in a strong shift in the pattern of Rubisco carbamylation, with full enzyme activation delayed until the midday period. For the first time it is demonstrated that the pattern of Rubisco activation differs between C3 and CAM plants of the same species under identical conditions. Despite large differences in Rubisco content between C3 and CAM plants, neither the amount of Rubisco or enzyme activity is thought to be limiting for photosynthesis, and it is suggested that Rubisco may function as a nitrogen store. Extreme CO2 diffusion limitation resulted in low rates of atmospheric CO2 assimilation that were associated with high rates of photosynthetic electron transport, and it is likely that photorespiration constitutes a significant electron sink over the entire diurnal course. Leaf morphological and physiological adaptations to drought stress are necessary for the epiphytic lifestyle but limit CO2 assimilation and confound the likelihood of high productivity.

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Crassulacean acid metabolism influences D/H ratio of leaf wax in succulent plants

Organic Geochemistry ◽

10.1016/j.orggeochem.2010.09.007 ◽

2010 ◽

Vol 41 (12) ◽

pp. 1269-1276 ◽

Cited By ~ 33

Author(s):

Sarah J. Feakins ◽

Alex L. Sessions

Keyword(s):

Crassulacean Acid Metabolism ◽

Acid Metabolism ◽

Leaf Wax ◽

Succulent Plants

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Carbohydrate partitioning in the leaves of Bromeliaceae performing C3 photosynthesis or Crassulacean acid metabolism

Functional Plant Biology ◽

10.1071/pp98005 ◽

1998 ◽

Vol 25 (3) ◽

pp. 371 ◽

Cited By ~ 12

Author(s):

John T. Christopher ◽

Joseph A. M. Holtum

Keyword(s):

Crassulacean Acid Metabolism ◽

Acid Metabolism ◽

Soluble Sugars ◽

Carbohydrate Accumulation ◽

Carbohydrate Partitioning ◽

C3 Species ◽

C3 Photosynthesis ◽

Cam Species

Carbohydrate accumulation was measured in the leaves of 11 speciesrepresenting the three subfamilies of Bromeliaceae. In the Tillandsioideae the C3 species Vriesea carinata Wawra accumulated starch and sucrose while the Crassulacean acid metabolism (CAM)species Tillandsia tricolor Schlechtendal & Chamissoaccumulated mainly starch. In the Pitcairnioideae the C3species Pitcairnia paniculata Ruiz & Pavon and two CAM species Dyckia sp. andFosterella schidosperma Barker accumulated sucrose butnot starch. Of six CAM species in the Bromelioideae, threeCryptanthus zonatus (Visiani) Beer,Neoregalia spectabilis Moore andPortea petropolitana Wawra accumulated starch but notsoluble sugars while three (Ananus comosus Linnaeus,Orthophytum vagans M.B. Foster andNidularium bilbergioides Schultes filius) accumulatedstarch as well as soluble sugars. Carbohydrate accumulation patterns weresimilar for species within each subfamily in that the Pitcairnioideae speciesdid not accumulate starch but accumulated sucrose while species from theTillandsioideae and Bromelioideae all accumulated starch (some alsoaccumulated soluble sugars). Carbohydrate accumulation patterns were notsimilar for C3 species versus CAM species from thedifferent subfamilies. These data suggest that variations in carbohydratebiochemistry resulting from different evolutionary histories have a greaterinfluence on carbohydrate accumulation patterns in CAM bromeliads than theconstraints of the CAM pathway itself.

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Carbon isotope composition and water-use efficiency in plants with crassulacean acid metabolism

Functional Plant Biology ◽

10.1071/fp04123 ◽

2005 ◽

Vol 32 (5) ◽

pp. 381 ◽

Cited By ~ 64

Author(s):

Klaus Winter ◽

Jorge Aranda ◽

Joseph A. M. Holtum

Keyword(s):

Water Use Efficiency ◽

Water Use ◽

Crassulacean Acid Metabolism ◽

Acid Metabolism ◽

Aloe Vera ◽

Dry Mass ◽

Tropical Conditions ◽

Δ13c Value ◽

Use Efficiency ◽

Cam Species

The relationship between water-use efficiency, measured as the transpiration ratio (g H2O transpired g–1 above- plus below-ground dry mass accumulated), and 13C / 12C ratio (expressed as δ13C value) of bulk biomass carbon was compared in 15 plant species growing under tropical conditions at two field sites in the Republic of Panama. The species included five constitutive crassulacean acid metabolism (CAM) species [Aloe vera (L.) Webb & Berth., Ananas comosus (L.) Merr., Euphorbia tirucalli L., Kalanchoë daigremontiana Hamet et Perr., Kalanchoë pinnata (Lam.) Pers.], two species of tropical C3 trees (Tectona grandis Linn. f. and Swietenia macrophylla King), one C4 species (Zea mays L.), and seven arborescent species of the neotropical genus Clusia, of which two exhibited pronounced CAM. The transpiration ratios of the C3 and CAM species, which ranged between 496 g H2O g–1 dry mass in the C3–CAM species Clusia pratensis Seeman to 54 g H2O g–1 dry mass in the constitutive CAM species Aloe vera, correlated strongly with δ13C values and nocturnal CO2 gain suggesting that δ13C value can be used to estimate both water-use efficiency and the proportion of CO2 gained by CAM species during the light and the dark integrated over the lifetime of the tissues.

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