Characteristics of C-4 photosynthesis in stems and petioles of C-3 flowering plants

Most plants are known as C-3 plants because the first product of photosynthetic CO2 fixation is a three-carbon compound. C-4 plants, which use an alternative pathway in which the first product is a four-carbon compound, have evolved independently many times and are found in at least 18 families. In addition to differences in their biochemistry, photosynthetic organs of C-4 plants show alterations in their anatomy and ultrastructure. Little is known about whether the biochemical or anatomical characteristics of C-4 photosynthesis evolved first. Here we report that tobacco, a typical C-3 plant, shows characteristics of C-4 photosynthesis in cells of stems and petioles that surround the xylem and phloem, and that these cells are supplied with carbon for photosynthesis from the vascular system and not from stomata. These photosynthetic cells possess high activities of enzymes characteristic of C-4 photosynthesis, which allow the decarboxylation of four-carbon organic acids from the xylem and phloem, thus releasing CO2 for photosynthesis. These biochemical characteristics of C-4 photosynthesis in cells around the vascular bundles of stems of C-3 plants might explain why C-4 photosynthesis has evolved independently many times

Phenotypic landscape inference reveals multiple evolutionary paths to C4_4 photosynthesis

C$_4$ photosynthesis has independently evolved from the ancestral C$_3$ pathway in at least 60 plant lineages, but, as with other complex traits, how it evolved is unclear. Here we show that the polyphyletic appearance of C$_4$ photosynthesis is associated with diverse and flexible evolutionary paths that group into four major trajectories. We conducted a meta-analysis of 18 lineages containing species that use C$_3$, C$_4$, or intermediate C$_3$-C$_4$ forms of photosynthesis to parameterise a 16-dimensional phenotypic landscape. We then developed and experimentally verified a novel Bayesian approach based on a hidden Markov model that predicts how the C$_4$ phenotype evolved. The alternative evolutionary histories underlying the appearance of C$_4$ photosynthesis were determined by ancestral lineage and initial phenotypic alterations unrelated to photosynthesis. We conclude that the order of C$_4$ trait acquisition is flexible and driven by non-photosynthetic drivers. This flexibility will have facilitated the convergent evolution of this complex trait

Spectral signatures of photosynthesis II: coevolution with other stars and the atmosphere on extrasolar worlds

As photosynthesis on Earth produces the primary signatures of life that can be detected astronomically at the global scale, a strong focus of the search for extrasolar life will be photosynthesis, particularly photosynthesis that has evolved with a different parent star. We take planetary atmospheric compositions simulated by Segura, et al. (2003, 2005) for Earth-like planets around observed F2V and K2V stars, modeled M1V and M5V stars, and around the active M4.5V star AD Leo; our scenarios use Earth's atmospheric composition as well as very low O2 content in case anoxygenic photosynthesis dominates. We calculate the incident spectral photon flux densities at the surface of the planet and under water. We identify bands of available photosynthetically relevant radiation and find that photosynthetic pigments on planets around F2V stars may peak in absorbance in the blue, K2V in the red-orange, and M stars in the NIR, in bands at 0.93-1.1 microns, 1.1-1.4 microns, 1.5-1.8 microns, and 1.8-2.5 microns. In addition, we calculate wavelength restrictions for underwater organisms and depths of water at which they would be protected from UV flares in the early life of M stars. We estimate the potential productivity for both surface and underwater photosynthesis, for both oxygenic and anoxygenic photosynthesis, and for hypothetical photosynthesis in which longer wavelength, multi-photosystem series are used.Comment: 59 pages, 4 figures, 4 tables, forthcoming in Astrobiology ~March 200

Photosynthetic responses of three common mosses from continental Antarctica

Predicting the effects of climate change on Antarctic terrestrial vegetation requires a better knowledge of the ecophysiology of common moss species. In this paper we provide a comprehensive matrix for photosynthesis and major environmental parameters for three dominant Antarctic moss species (Bryum subrotundifolium, B. pseudotriquetrum and Ceratodon purpureus). Using locations in southern Victoria Land, (Granite Harbour, 77°S) and northern Victoria Land (Cape Hallett, 72°S) we determined the responses of net photosynthesis and dark respiration to thallus water content, thallus temperature, photosynthetic photon flux densities and CO2 concentration over several summer seasons. The studies also included microclimate recordings at all sites where the research was carried out in field laboratories. Plant temperature was influenced predominantly by the water regime at the site with dry mosses being warmer. Optimal temperatures for net photosynthesis were 13.7°C, 12.0°C and 6.6°C for B. subrotundifolium, B. pseudotriquetrum and C. purpureus, respectively and fall within the known range for Antarctic mosses. Maximal net photosynthesis at 10°C ranked as B. subrotundifolium > B. pseudotriquetrum > C. purpureus. Net photosynthesis was strongly depressed at subzero temperatures but was substantial at 0°C. Net photosynthesis of the mosses was not saturated by light at optimal water content and thallus temperature. Response of net photosynthesis to increase in water content was as expected for mosses although B. subrotundifolium showed a large depression (60%) at the highest hydrations. Net photosynthesis of both B. subrotundifolium and B. pseudotriquetrum showed a large response to increase in CO2 concentration and this rose with increase in temperature; saturation was not reached for B. pseudotriquetrum at 20°C. There was a high level of variability for species at the same sites in different years and between different locations. This was substantial enough to make prediction of the effects of climate change very difficult at the moment

Oxygen Requirement and Inhibition of C4 Photosynthesis . An Analysis of C4 Plants Deficient in the C3 and C4 Cycles

The basis for O2 sensitivity of C4 photosynthesis was evaluated using a C4-cycle-limited mutant of Amaranthus edulis (a phosphoenolpyruvate carboxylase-deficient mutant), and a C3-cycle-limited transformant of Flaveria bidentis (an antisense ribulose-1,5-bisphosphate carboxylase/oxygenase [Rubisco] small subunit transformant). Data obtained with the C4-cycle-limited mutant showed that atmospheric levels of O2 (20 kPa) caused increased inhibition of photosynthesis as a result of higher levels of photorespiration. The optimal O2 partial pressure for photosynthesis was reduced from approximately 5 kPa O2 to 1 to 2 kPa O2, becoming similar to that of C3 plants. Therefore, the higher O2 requirement for optimal C4 photosynthesis is specifically associated with the C4 function. With the Rubisco-limited F. bidentis, there was less inhibition of photosynthesis by supraoptimal levels of O2 than in the wild type. When CO2 fixation by Rubisco is limited, an increase in the CO2 concentration in bundle-sheath cells via the C4 cycle may further reduce the oxygenase activity of Rubisco and decrease the inhibition of photosynthesis by high partial pressures of O2 while increasing CO2 leakage and overcycling of the C4 pathway. These results indicate that in C4 plants the investment in the C3 and C4 cycles must be balanced for maximum efficiency

What limits photosynthesis? Identifying the thermodynamic constraints of the biosphere within the Earth system

Photosynthesis converts sunlight into the chemical free energy that feeds the Earth's biosphere, yet at levels much lower than what thermodynamics would allow for. I propose here that photosynthesis is nevertheless thermodynamically limited, but this limit acts indirectly on the material exchange of water and carbon dioxide. I substantiate this interpretation using global observation-based datasets of radiation, photosynthesis, precipitation and evaporation. I first calculate the conversion efficiency of photosynthesis in terrestrial ecosystems and its climatological variation, with a median efficiency of 0.78% (n = 13445). The rates tightly correlate with evaporation (r2 = 0.89), which demonstrates the importance of the coupling of photosynthesis to material exchange. I then infer evaporation from the maximum material exchange between the surface and the atmosphere that is thermodynamically possible using datasets of solar radiation and precipitation. This inferred rate closely correlates with the observation-based evaporation dataset (r2 = 0.85). When this rate is converted back into photosynthetic activity, the resulting patterns correlate highly with the observation-based dataset (r2 = 0.56). This supports the interpretation that it is not energy directly that limits terrestrial photosynthesis, but rather the material exchange that is driven by sunlight. This interpretation can explain the very low, observed conversion efficiency of photosynthesis in terrestrial ecosystems as well as its spatial variations. More generally, this implies that one needs to take the necessary material flows and exchanges associated with life into account to understand the thermodynamics of life. This, ultimately, requires a perspective that links the activity of the biosphere to the thermodynamic constraints of transport processes in the Earth system.Comment: accepted for publication in Special Issue "21st European Bioenergetics Conference", Biochimica et Biophysica Acta - Bioenergetic

Palisade cell shape affects the light-induced chloroplast movements and leaf photosynthesis

Leaf photosynthesis is regulated by multiple factors that help the plant to adapt to fluctuating light conditions. Leaves of sun-light-grown plants are thicker and contain more columnar palisade cells than those of shade-grown plants. Light-induced chloroplast movements are also essential for efficient leaf photosynthesis and facilitate efficient light utilization in leaf cells. Previous studies have demonstrated that leaves of most of the sun-grown plants exhibited no or very weak chloroplast movements and could accomplish efficient photosynthesis under strong light. To examine the relationship between palisade cell shape, chloroplast movement and distribution, and leaf photosynthesis, we used an Arabidopsis thaliana mutant, angustifolia (an), which has thick leaves that contain columnar palisade cells similar to those in the sun-grown plants. In the highly columnar cells of an mutant leaves, chloroplast movements were restricted. Nevertheless, under white light condition (at 120 µmol m-2 s-1), the an mutant plants showed higher chlorophyll content per unit leaf area and, thus, higher light absorption by the leaves than the wild type, which resulted in enhanced photosynthesis per unit leaf area. Our findings indicate that coordinated regulation of leaf cell shape and chloroplast movement according to the light conditions is pivotal for efficient leaf photosynthesis