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

2019 ◽  
Vol 70 (22) ◽  
pp. 6611-6619
Author(s):  
Ming-He Li ◽  
Ding-Kun Liu ◽  
Guo-Qiang Zhang ◽  
Hua Deng ◽  
Xiong-De Tu ◽  
...  

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.

2002 ◽  
Vol 29 (6) ◽  
pp. 775 ◽  
Author(s):  
Rowan F. Sage

This paper originates from a presentation at the IIIrd International Congress on Crassulacean Acid Metabolism, Cape Tribulation, Queensland, Australia, August 2001. Despite sharing a similar metabolism, crassulacean acid metabolism (CAM) and C4 photosynthesis are not known to occur in identical species, with the exception of Portulaca spp. In Portulaca, C4 and weak CAM photosynthesis occur in distinct regions of the leaf, rather than in the same cells. This is in marked contrast to the situation in most CAM species where C3 and CAM photosynthesis are active in the same cell over the course of a day and growing season. The lack of CAM and C4 photosynthesis in identical cells of a plant indicates these photosynthetic pathways are incompatible. Incompatibilities between CAM and C4 photosynthesis could have a number of biochemical, anatomical and evolutionary explanations. Biochemical incompatibilities could result from the requirement for spatial separation of C3 and C4 phases in C4 plants versus temporal separation in CAM plants. In C4 plants, regulatory systems coordinate mesophyll and bundle sheath metabolism, with light intensity being the major environmental signal. In CAM plants, a circadian oscillator coordinates day and night phases of CAM. The requirement for rapid intercellular transport in C4 plants may be incompatible with the intracellular transport and storage needs of CAM. For example, the large vacuole required for malate storage in CAM could impede metabolite diffusion between mesophyll and bundle sheath cells in C4 plants. Anatomical barriers could also exist because both CAM and the C4 pathway require distinct leaf anatomies for efficient function. Efficient function of the C4 pathway generally requires an outer layer of cells specialized for phosphoenolpyruvate (PEP) carboxylation and regeneration and an inner layer for CO2 accumulation and refixation, while CAM species require enlarged vacuoles and tight cell packing. In evolutionary terms, barriers preventing CAM and C4 photosynthesis in the same species may be the initial steps in the respective evolutionary pathways from C3 ancestors. The first steps in C4 photosynthesis are related to scavenging photorespiratory CO2 via localization of glycine decarboxylase in the bundle sheath cells. The initial steps in CAM evolution are associated with the scavenging of respiratory CO2 at night by PEP carboxylation. In each, simplified versions of the specialized anatomy may need to be present for the evolutionary sequence to begin. For C4 evolution, enhanced bundle sheath size may be required in C3 ancestors; for CAM evolution, succulence may be required. Thus, before CAM or C4 photosynthesis began to evolve, the outcome of the evolutionary experiment may have been predetermined.


2020 ◽  
Vol 7 (1) ◽  
Author(s):  
Li-Yu Chen ◽  
Yinghui Xin ◽  
Ching Man Wai ◽  
Juan Liu ◽  
Ray Ming

AbstractCrassulacean acid metabolism (CAM) photosynthesis is an innovation of carbon concentrating mechanism that is characterized by nocturnal CO2 fixation. Recent progresses in genomics, transcriptomics, proteomics, and metabolomics of CAM species yielded new knowledge and abundant genomic resources. In this review, we will discuss the pattern of cis-elements in stomata movement-related genes and CAM CO2 fixation genes, and analyze the expression dynamic of CAM related genes in green leaf tissues. We propose that CAM photosynthesis evolved through the re-organization of existing enzymes and associated membrane transporters in central metabolism and stomatal movement-related genes, at least in part by selection of existing circadian clock cis-regulatory elements in their promoter regions. Better understanding of CAM evolution will help us to design crops that can thrive in arid or semi-arid regions, which are likely to expand due to global climate change.


2015 ◽  
Vol 156 (1) ◽  
pp. 29-39 ◽  
Author(s):  
Nuno Rainha ◽  
Violante P. Medeiros ◽  
Mariana Câmara ◽  
Hélder Faustino ◽  
João P. Leite ◽  
...  

2005 ◽  
Vol 32 (5) ◽  
pp. 397 ◽  
Author(s):  
Katia Silvera ◽  
Louis S. Santiago ◽  
Klaus Winter

Crassulacean acid metabolism (CAM) is one of three metabolic pathways found in vascular plants for the assimilation of carbon dioxide. In this study, we investigate the occurrence of CAM photosynthesis in 200 native orchid species from Panama and 14 non-native species by carbon isotopic composition (δ13C) and compare these values with nocturnal acid accumulation measured by titration in 173 species. Foliar δ13C showed a bimodal distribution with the majority of species exhibiting values of approximately –28‰ (typically associated with the C3 pathway), or –15‰ (strong CAM). Although thick leaves were related to δ13C values in the CAM range, some thin-leaved orchids were capable of CAM photosynthesis, as demonstrated by acid titration. We also found species with C3 isotopic values and significant acid accumulation at night. Of 128 species with δ13C more negative than –22‰, 42 species showed nocturnal acid accumulation per unit fresh mass characteristic of weakly expressed CAM. These data suggest that among CAM orchids, there may be preferential selection for species to exhibit strong CAM or weak CAM, rather than intermediate metabolism.


1997 ◽  
Vol 24 (6) ◽  
pp. 777 ◽  
Author(s):  
Kate Maxwell ◽  
Susanne von Caemmerer ◽  
John R. Evans

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.


2018 ◽  
Vol 45 (7) ◽  
pp. 681 ◽  
Author(s):  
Jamie Males

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.


1998 ◽  
Vol 25 (3) ◽  
pp. 371 ◽  
Author(s):  
John T. Christopher ◽  
Joseph A. M. Holtum

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.


2013 ◽  
Vol 2013 ◽  
pp. 1-9 ◽  
Author(s):  
Takami Matsuo ◽  
Yusuke Totoki ◽  
Haruo Suemitsu

The mechanism of endogenous circadian photosynthesis oscillations of plants performing crassulacean acid metabolism (CAM) is investigated in terms of a nonlinear theoretical model. Blasius et al. used throughout continuous time differential equations which adequately reflect the CAM dynamics. The model shows regular endogenous limit cycle oscillations that are stable for a wide range of temperatures in a manner that complies well with experimental data. In this paper, we pay attention to the approximation of the fast modes of the CAM dynamics. Using the zero-epsilon approximation of the slow manifold, we derive the critical manifold that is defined by two algebraic nonlinear equations. The critical manifold allows us to give the algebraic estimate of the order of the tonoplast membrane. The dynamic equation of the order of the tonoplast membrane includes the nonlinear function that gives the equilibrium value of the lipid order of tonoplast functions as a hysteresis switch. We identify the nonlinear function with the measurement signals. Using the basis function expansion of the nonlinear and the critical manifold, we propose an adaptive observer to estimate the tonoplast order and the nonlinear function.


2005 ◽  
Vol 32 (5) ◽  
pp. 381 ◽  
Author(s):  
Klaus Winter ◽  
Jorge Aranda ◽  
Joseph A. M. Holtum

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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