The origins of C 4 grasslands: integrating evolutionary and ecosystem science. Science , — Biochemistry of C 3 —C 4 intermediates. The biochemistry of plants.
Academic Press : New York , — Single-cell C 4 photosynthesis versus the dual-cell Kranz paradigm. Annual Review of Plant Biology 55 , — The gene for the P-subunit of glycine decarboxylase from the C 4 species Flaveria trinervia : analysis of transcriptional control in transgenic Flaveria bidentis C 4 and Arabidopsis C 3. Distribution and structure of plasmodesmata in mesophyll and bundle-sheath cells of Zea Mays L.
Planta , 77 — Anatomical and ultrastructural changes associated with sink-to-source transition in developing maize leaves. International Journal Of Plant Sciences , — Alteration of organic acid metabolism in Arabidopsis overexpressing the maize C 4 NADP-malic enzyme causes accelerated senescence during extended darkness.
A biochemical-model of photosynthetic CO 2 assimilation in leaves of C 3 species. Planta , 78 — Cracking the Kranz enigma with systems biology. Furbank RT.
Evolution of the C 4 photosynthetic mechanism: are there really three C 4 acid decarboxylation types? Evolution of C 4 photosynthesis in the genus Flaveria : how many and which genes does it take to make C 4? The Plant Cell 23 , — Hatch MD. C 4 Photosynthesis - a unique blend of modified biochemistry, anatomy and ultrastructure.
Biochimica et Biophysica Acta , 81 — Single and double overexpression of C 4 -cycle genes had differential effects on the pattern of endogenous enzymes, attenuation of photorespiration and on contents of UV protectants in transgenic potato and tobacco plants.
Journal of Experimental Botany 52 , — Overexpression of C 4 -cycle enzymes in transgenic C 3 plants: a biotechnological approach to improve C 3 -photosynthesis. Journal of Experimental Botany 53 , — Predicting C 4 photosynthesis evolution: modular, individually adaptive steps on a Mount Fuji fitness landscape. Cell , — Enzymic and photosynthetic characteristics of reciprocal F 1 hybrids of Flaveria pringlei C 3 and Flaveria brownii C 4 -like species.
Plant Physiology 87 , — Glycine decarboxylase is confined to the bundle-sheath cells of leaves of C 3 —C 4 intermediate species. Evolutionary convergence of cell-specific gene expression in independent lineages of C 4 grasses. Plant Physiology , 62 — C 2 photosynthesis generates about 3-fold elevated leaf CO 2 levels in the C 3 —C 4 intermediate species Flaveria pubescens.
Plant species intermediate for C 3 , C 4 photosynthesis. Paradigm shift in plant growth control. Current Opinion in Plant Biology 25 , — Uncouplers of spinach chloroplast photosynthetic phosphorylation. Plant Physiology 34 , — Photosynthetic characteristics of C 3 —C 4 intermediate flaveria species: 1. Leaf anatomy, photosynthetic responses to O 2 and CO 2 , and activities of key enzymes in the C 3 and C 4 pathways. Plant Physiology 71 , — Comparative transcriptome atlases reveal altered gene expression modules between two Cleomaceae C 3 and C 4 plant species.
The Plant Cell 26 , — The developmental dynamics of the maize leaf transcriptome. Nature Genetics 42 , — Deconstructing Kranz anatomy to understand C 4 evolution.
Structural and metabolic transitions of C 4 leaf development and differentiation defined by microscopy and quantitative proteomics in maize. The Plant Cell 22 , — The role of photorespiration during the evolution of C 4 photosynthesis in the genus Flaveria.
Elife 3 , e C 3 —C 4 intermediate photosynthesis in plants. Bioscience 34 , — Monson RK. Oecologia 80 , — The origins of C 4 genes and evolutionary pattern in the C 4 metabolic phenotype.
Coordination of the cell-specific distribution of the four subunits of glycine decarboxylase and of serine hydroxymethyltransferase in leaves of C 3 —C 4 intermediate species from different genera. Characterization of C 3 —C 4 intermediate species in the genus Heliotropium L. Boraginaceae : anatomy, ultrastructure and enzyme activity. Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases, carbon costs and ecological consequences.
Do we underestimate the importance of leaf size in plant economics? Disproportional scaling of support costs within the spectrum of leaf physiognomy. Annals Of Botany , — Functional analysis of corn husk photosynthesis. Systems analysis of a maize leaf developmental gradient redefines the current C 4 model and provides candidates for regulation. Panicum milioides C 3 —C 4 does not have improved water or nitrogen economies relative to C 3 and C 4 congeners exposed to industrial-age climate change.
Late Cretaceous origin of the rice tribe provides evidence for early diversification in Poaceae. Nature Communications 2 , Raines CA. Increasing photosynthetic carbon assimilation in C 3 plants to improve crop yield: current and future strategies. Plant Phy siology , 36 — C 3 —C 4 Intermediate species in Alternanthera Amaranthaceae : leaf anatomy, CO 2 compensation point, net CO 2 exchange and activities of photosynthetic enzymes. Plant Physiology 80 , — Photorespiratory metabolism and immunogold localization of photorespiratory enzymes in leaves of C 3 and C 3 —C 4 intermediate species of Moricandia.
Distribution of photorespiratory enzymes between bundle-sheath and mesophyll cells in leaves of the C 3 —C 4 intermediate species Moricandia arvensis L. Rawsthorne S. C 3 —C 4 intermediate photosynthesis: linking physiology to gene expression.
The Plant Journal 2 , — Evolution and function of leaf venation architecture: a review. Annals of Botany 87 , — Leaf hydraulic architecture correlates with regeneration irradiance in tropical rainforest trees. Sack L Holbrook NM. Leaf hydraulics.
Annual Review of Plant Biology 57 , — Developmentally based scaling of leaf venation architecture explains global ecological patterns. Nature Communications 3 , Sack L Scoffoni C. Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. Sage RF. The evolution of C 4 photosynthesis.
The C 4 plant lineages of planet Earth. Photorespiration and the evolution of C 4 photosynthesis. Annual Review of Plant Biology 63 , 19 — Initial events during the evolution of C 4 photosynthesis in C 3 species of Flaveria. Stage-specific markers define early steps of procambium development in Arabidopsis leaves and correlate termination of vein formation with mesophyll differentiation. Development , — Scarpella E Meijer AH.
Pattern formation in the vascular system of monocot and dicot plant species. Scheres B Xu L. Polar auxin transport and patterning: grow with the flow. Evolution of C 4 photosynthesis in the genus Flaveria : establishment of a photorespiratory CO 2 pump. The Plant Cell 25 , — Tie-dyed2 encodes a callose synthase that functions in vein development and affects symplastic trafficking within the phloem of maize leaves. Slewinski TL. Using evolution as a guide to engineer Kranz-type C 4 photosynthesis.
Frontiers in Plant Science 4 , On the mechanism of C 4 photosynthesis intermediate exchange between Kranz mesophyll and bundle sheath cells in grasses. Journal of Experimental Botany 59 , — On the origin of the theory of mineral nutrition of plants and the law of the minimum.
Soil Science Society of America Journal 63 , — Water-use efficiency and nitrogen-use efficiency of C 3 —C 4 intermediate species of Flaveria Juss. Biochemical models of leaf photosynthesis. Genome-wide transcript analysis of early maize leaf development reveals gene cohorts associated with the differentiation of C 4 Kranz anatomy. The Plant Journa l 75 , — Three distinct biochemical subtypes of C 4 photosynthesis?
A modelling analysis. Quantity and kinetic properties of ribulose 1,5-bisphosphate carboxylase in C 3 , C 4 , and C 3 —C 4 intermediate species of Flaveria Asteraceae. Plant and Cell Physiology 30 , — Westhoff P Gowik U. Evolution of C 4 phosphoenolpyruvate carboxylase. Genes and proteins: a case study with the genus Flaveria. Annals of Botany 93 , 13 — Phenotypic landscape inference reveals multiple evolutionary paths to C 4 photosynthesis.
Elife 2 , e Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide. Sign In or Create an Account. Sign In. Advanced Search. Search Menu. Article Navigation. Close mobile search navigation Article Navigation.
In this type of photosynthesis, organisms absorb sunlight energy during the day then use the energy to fix carbon dioxide molecules during the night.
During the day, the organism's stomata close up to resist dehydration while the carbon dioxide from the previous night undergoes the Calvin cycle. CAM photosynthesis allows plants to survive in arid climates and therefore is the type of photosynthesis used by cacti and other desert plants.
However, non-desert plants like pineapples and epiphyte plants such as orchids also use CAM photosynthesis. Alexander Eliot has been a professional writer since He holds a B. His academic background allows him to write articles in all fields of education, as well as science and philosophy. Eliot once worked for a performance auto center, an experience he draws from to write informative articles in automotive theory, maintenance and customization.
What Is the Role of Pigments in Photosynthesis? Leaf Cell Structure. The Three Stages of Photosynthesis. This is achieved by restricting the Gly decarboxylation reaction to the bundle sheath mitochondria, thus all Gly produced by photorespiration in the mesophyll has to be transferred to the bundle sheath cells for further processing.
The Gly shuttle affects photosynthetic CO 2 fixation in two ways. All photorespiratory CO 2 is set free inside the leaf far apart from the outer surface. Therefore it has to diffuse through several cell layers, before it could escape from the leaf. In some C 3 -C 4 intermediate species this refixation capacity is supported by the spatial distribution of the organelles within the bundle sheath cell, since the mitochondria concentrate adjacent to the vascular bundles Rawsthorne et al.
Additionally, the Gly shuttle enhances the CO 2 concentration within the bundle sheath cells. As a consequence, the carboxylation activity of Rubisco in the bundle sheath cells increases, while its oxygenase reaction is outcompeted Bauwe, It is assumed that the establishment of such a photorespiratory CO 2 pump is an important intermediate step on the way toward C 4 photosynthesis.
A photorespiratory CO 2 pump can easily be accomplished at the molecular level. The expression of only one gene, encoding a subunit of the Gly decarboxylase multienzyme complex, had to be restricted to the bundle sheath cells. This might have been achieved through relatively subtle changes in the cis-regulatory elements that control the expression of these genes compare with Akyildiz et al.
In cases where several isogenes with different leaf expression specificities existed already in the respective C 3 ancestral species this process might also have included the pseudogenization of those isogenes that are not bundle sheath specific. In the C 3 -C 4 intermediate species Moricandia arvensis , for example, only the P subunit of Gly decarboxylase is restricted to the bundle sheath.
Since the enzyme is inactive without this subunit, Gly cannot be decarboxylated in the mesophyll Rawsthorne et al. For other C 3 -C 4 intermediates from the genera Flaveria and Panicum , it was found that also the other subunit genes were expressed specifically or at least preferentially in the bundle sheath cells Morgan et al.
It follows that once Kranz anatomy and enlarged bundle sheath cells with increased amounts of organelles were established, a photorespiratory CO 2 pump could be easily achieved in genetic terms.
The photorespiratory CO 2 pump and the resulting elevated CO 2 content in the bundle sheath cells might have led to a further increase in organelle numbers in these cells Sage, The next step toward true C 4 photosynthesis might have been an increase in the levels of carbonic anhydrase and PEPC in the cytosol of the mesophyll cells.
This would have aided in recapturing the photorespiratory CO 2 that escaped from the bundle sheath into the mesophyll cells. Also this evolutionary step is reflected by C 3 -C 4 intermediate species of the genus Flaveria , which contain significantly higher levels in PEPC transcript and protein amounts as compared to C 3 Flaveria species but do not exhibit C 4 cycle activity yet Ku et al. To establish a limited C 4 cycle activity the remaining C 4 cycle enzymes must have been elevated at this point.
Thus the expression of the related genes must have been shifted to the bundle sheath cells. To complete the C 4 cycle the expression of chloroplastic pyruvate orthophosphate dikinase must have been enhanced to allow an efficient PEP regeneration.
Plants in this phase of C 4 evolution exhibit high activities of C 4 cycle enzymes, but still high Rubisco activity in the mesophyll cells. Consequently, CO 2 is only partially fixed through the C 4 pathway. The key step in establishing true C 4 photosynthesis and to integrate the C 4 pathway and the Calvin-Benson cycle was the spatial separation of the two carboxylation reactions. PEPC was restricted to the mesophyll and Rubisco to the bundle sheath cells.
Now the vast majority of the photoassimilated CO 2 passed initially through the C 4 cycle before it was fixed by Rubisco. The evolving C 4 pathway was further optimized by compartmentalizing other enzymes of both the C 4 and Calvin-Benson cycles, by adapting the light reaction of photosynthesis and by strongly increasing carbonic anhydrase activity in the cytosol of mesophyll cells. The C 4 photosynthetic pathway is characterized by the extensive shuffling of metabolites between the organelles and the cytosol within mesophyll and bundle sheath cells, respectively.
The evolution of this pathway, therefore, required also the establishment of the necessary transport capacity. In plants of the NADP-ME type, for example, for every molecule of CO 2 fixed, one molecule of pyruvate and oxaloacetate each have to be transported into the mesophyll chloroplasts and in a countermove PEP and malate have to be translocated to the cytosol.
In bundle sheath cells, on the other hand, malate has to enter and pyruvate has to leave the chloroplast matching the rate of CO 2 assimilation. This was most likely necessary due to differences in the supply of energy and reduction equivalents in the different tissues and to optimize the overall integration of the various metabolic pathways. The evolution of C 4 photosynthesis was accompanied by massive changes in gene expression.
About 2. As to be expected the expression levels of genes involved in the C 4 cycle, the photorespiratory pathway, and the photosynthetic light reactions changed. However, several other pathways showed explicit alterations in their corresponding transcript levels, too.
Most interestingly, genes encoding components of the cytosolic and plastidic protein synthesis machinery are down-regulated in the C 4 species. Besides quantitative alterations C 4 evolution required changes in the spatial gene expression patterns. Sawers et al. This comparison indicates that the establishment of C 4 photosynthesis involved a dramatic redesign and restructuring of leaf functions.
Most of the evolutionary alterations, leading to the quantitative and qualitative changes in gene expression, are not yet understood at the molecular level and only a few have been analyzed in great detail.
These cases demonstrate that nature appeared to have been quite flexible in achieving the desired goal, i. Cell-specific gene expression can be achieved by transcriptional control. A very similar element was also found in the promoters of the orthologous ppcA genes from C 3 Flaverias ; however, these elements lack the ability to direct mesophyll specificity. Accordingly, slight modifications within a cis-regulatory element were sufficient to convert a gene with no apparent expression specificity into a mesophyll-specific gene Akyildiz et al.
In contrast, the bundle sheath-specific expression of one of the genes encoding the small subunit of Rubisco in the C 4 plant Flaveria bidentis , FbRbcS1, was reported to be regulated mainly at the posttranscriptional level Patel et al. Most likely, the FbRcS1 transcripts are differentially stable in mesophyll and bundle sheath cells. The massive changes in gene expression during the transition from C 3 to C 4 photosynthesis combined with the fact that C 4 evolution must have been easy in genetic terms implies that preexisting gene regulatory networks in C 3 plants were probably the foundation for multiple evolutionary changes toward C 4 photosynthesis compare with Matsuoka, In C 3 plants gene regulatory networks exist that assure a coordinated response of genes involved in photosynthesis and related metabolic pathways Mentzen and Wurtele, Promoters driving mesophyll- or bundle sheath-specific gene expression in C 4 species partly maintain their cell preference of expression in C 3 species Matsuoka et al.
Consequently, networks for regulating developmental and metabolic processes operated already in C 3 ancestral angiosperms and could serve as a platform for the establishment of C 4 leaf anatomy and metabolism. Unfortunately, our understanding of gene regulatory networks controlling the development and anatomy of a typical leaf of a C 3 angiosperm is rather rudimentary.
With the exceptions discussed above we know little about the molecular nature of cis-and trans-regulatory factors that regulate gene expression in the mesophyll and bundle sheath cells of both C 3 and C 4 plants. This pair of transcription factors occurs in all land plants. In Arabidopsis the GLK proteins are largely redundant and control the expression of more than genes that are mainly connected with photosynthesis. In the mesophyll and bundle sheath of the C 4 species maize, however, the two GLK genes are expressed differentially with GOLDEN2 specifically affecting only chloroplast development in the bundle sheath cells Waters and Langdale, All C 4 cycle enzymes evolved from nonphotosynthetic isoforms.
To ensure high fluxes through the C 4 pathway, the concentration of substrates and effector metabolites is elevated as compared to the original metabolic environment in the ancestral C 3 species. Accordingly, the evolution of the C 4 isoforms involved changes in their kinetic and regulatory properties. The C 4 isoform of PEPC is perhaps the best-documented example for these evolutionary processes for review, see Gowik and Westhoff, These differences in enzymatic properties were achieved by relatively small changes in primary enzyme structure.
Although C 4 PEPCs evolved at least eight times independently within the grass family the resulting enzymes show a surprisingly high degree of similarity. A strong positive selection was found for 21 amino acid positions Christin et al.
Alternatively, this might also reflect the fact that most of the dicot C 4 lineages are very young compared to the first origins of C 4 photosynthesis within the grasses Ehleringer et al. One may infer therefore, that the C 4 PEPCs of the grass family are much more optimized for their role in C 4 photosynthesis than their dicot counterparts.
This might explain the higher degree of convergence within the photosynthetic PEPCs of the grasses. Distinct enzyme regions could be identified that are involved in an altered pH-dependent inhibition by malate and differences in tetramerization of the enzyme Detarsio et al. Adaptation of C 4 enzymes to the new metabolic context of the C 4 pathway could also involve a change in the cellular location of the enzyme. The photosynthetic carbonic anhydrase gene of F.
The gene is highly expressed in the mesophyll cells Tetu et al. Due to a mutation in the chloroplast transit peptide of the ancestral enzyme, the C 4 isoform became a cytosolic enzyme Tanz et al. Interestingly, this ancestral carbonic anhydrase gene was already highly expressed in leaves, suggesting that the intracellular localization of the protein was of minor importance and altered during evolution. It is not clear so far to which extent other enzymes, which are not directly related to the C 4 pathway, were modified during C 4 evolution.
The world of the 21st century will face massive problems in feeding the growing human population. Green energy from plant biomass is being developed to help cover energy demands, and might compete with food production for terrain and resources in the future. It will be a challenge to increase crop production adequately in a sustainable manner both in terms of harvestable yield and total biomass.
C 4 plants exhibit high photosynthetic capacity and efficient use of nitrogen and water resources. They have received an increasing interest in recent years and the transfer of C 4 photosynthesis into current C 3 crops is being considered Sheehy et al.
Knowledge about the genetic architecture of C 4 photosynthesis and the underlying gene regulatory networks is a prerequisite to be successful in this endeavor. To elucidate these networks different approaches are needed. Large forward-genetic screens with mutagenized rice and Sorghum bicolor as well as reverse-genetic approaches are being carried out to identify genes that are related to C 4 subtraits like a reduced CO 2 compensation point, high vein density, or enlarged bundle sheath cells.
The analysis of the transcriptomes, proteomes, and metabolomes of different developmental stages of C 4 leaves will help to understand how C 4 leaf differentiation and the establishment of Kranz anatomy are regulated. The successful integration of these different data, the identification of the key regulators of C 4 traits, and the generation of a strategy of how the C 3 plant rice must be genetically altered to introduce the C 4 pathway should become a milestone in the relatively young field of synthetic biology.
We are thankful to an anonymous reviewer who helped to improve this text significantly. Plant Cell 19 : — Google Scholar. Anderson LE Chloroplast and cytoplasmic enzymes. Pea leaf triose phosphate isomerases. Biochim Biophys Acta : —
0コメント