We now have a good understanding of how C 4 photosynthesis responds to environmental variables such as light, temperature and CO 2 Long, These functional models of C 4 which allow the link between leaf biochemistry and gas exchange have become essential tools von Caemmerer and Furbank, ; von Caemmerer, The model comes with an Excel spreadsheet inviting the community to have a go at redesigning C 4 photosynthesis.
The usefulness of a sound mathematical framework is also highlighted in the opinion paper by Li et al. Most C 4 species are characterized by Kranz anatomy, but there are a small number, such as Bienertia cycloptera , that perform C 4 photosynthesis within individual mesophyll cells Voznesenskaya et al. CO 2 diffusion during C 4 photosynthesis also remains an important issue in those species with Kranz anatomy.
Theories developed for the interpretation of stable isotope discrimination during C 4 photosynthesis Farquhar, ; Gillon and Yakir, ; Barbour et al. For example, 13 CO 2 isotope discrimination can be used to quantify bundle sheath leakiness the ratio of CO 2 leak rate out of the bundle sheath over the rate of CO 2 supply and C 18 OO discrimination allows quantification of CO 2 diffusion from intercellular airspace to the mesophyll cytosol in relation to carbonic anhydrase activity there.
Recent technical advances have greatly facilitated the measurements of isotope discrimination concurrently with gas exchange Gong et al. Gong et al. Osborne et al. The techniques of the 14 C pulse chase which were used by Hatch and Slack to unravel the mysteries of C 4 photosynthesis have been replaced by mass spectrometric measurements of 13 CO 2 labelling kinetics, which provide a wealth of information compared to past experiments.
This technique was used for the first time by Arrivault et al. It will provide a welcome tool for establishing C 4 metabolism in C 3 species. Today, major C 4 crops are grown in dense stands where most leaves are shaded compared to their wild progenitors. Pignon et al. The ancestors of maize and miscanthus appear to have existed in very open habitats, where water and nutrient deficiencies would have limited leaf area.
There may therefore have been little evolutionary pressure for maintenance of photosynthetic efficiency in shade conditions. Improving C 4 photosynthesis in a crop environment may be an important next step for increasing genetic yield potential in some of these most important crops Long et al.
Where will C 4 research go next? In 50 years we have seen the expansion of the field from the examination of a rudimentary biochemical pathway in just a few species to the construction of complex evolutionary models and assembly of massive genomic and transcriptomic data sets from a large range of both crop and wild C 4 species, as well as multiple efforts to engineer C 4 traits into C 3 crops and model species.
As gene and transcript sequencing costs plummet with third-generation technologies, what will be the new technological driver of C 4 research? With appropriate rapid kill and cryopreservation, this technique may hold promise for measuring metabolites during photosynthesis in mesophyll and bundle sheath compartments more accurately.
Gene discovery through genomics approaches reveals gene candidates and evidence for the importance of certain genes in evolution or for plant performance, but these must be experimentally validated. Commonly, for C 3 dicots, this is done in model systems like Arabidopsis or tobacco by gene inactivation or overexpression, but only recently have grass transformation systems become sufficiently routine for researchers to approach these experiments in their laboratories.
Alternatives such as producing large panels of mutants by non-targeted mutagenic approaches or by crossing genetic material to develop near-isogenic lines with and without genetic polymorphisms is outside the scope of most small research laboratories. Future development of new and more efficient transformation systems for a range of C 4 plants and the development of genetic stocks which can be ordered routinely for knockout lines and backcrossed mutants, sequenced populations and recombinant in-bred lines would see a rapid development in C 4 research similar to that seen when Arabidopsis genetic resources became widely available.
In the case of the C 4 rice project, the ability to make multiple gene constructs simplifies cloning strategies Simkin et al. There is a vast array of information and new technology now at our fingertips. Nevertheless, we must still marvel at the achievements of researchers 50 years ago in assembling a completely new photosynthetic pathway from a collection of radiolabelling experiments and enzyme assays, and the rapidity with which these researchers brought C 4 anatomical and biochemical data together to underpin the knowledge of the C 4 mechanism we have today.
Metabolite pools and carbon flow during C 4 photosynthesis in maize: 13 CO 2 labeling kinetics and cell type fractionation. Journal of Experimental Botany 68 , — Google Scholar. Deep evolutionary comparison of gene expression identifies parallel recruitment of trans-factors in two independent origins of C4 photosynthesis. PLoS Genetics 10 , e Online CO 2 and H 2 O oxygen isotope fractionation allows estimation of mesophyll conductance in C4 plants, and reveals that mesophyll conductance decreases as leaves age in both C4 and C3 plants.
New Phytologist , — Bellasio C. The CO 2 concentrating function of C 4 Photosynthesis: a biochemical model. The proceedings of the fourth international congress on photosynthesis.
London : Biochemical Society of London , — Google Preview. Christin P-A. Traces of strong selective pressures in the genomes of C 4 grasses. Freeze-quenched maize mesophyll and bundle sheath separation uncovers bias in previous tissue-specific RNA-Seq data.
High-spatial resolution mass spectrometry imaging reveals the genetically programmed, developmental modification of the distribution of thylakoid membrane lipids among individual cells of the maize leaf. The Plant Journal doi: Fankhauser N Aubry S. Post-transcriptional regulation of photosynthetic genes is a key driver of C 4 leaf ontogeny. Farquhar GD. On the nature of carbon isotope discrimination in C 4 species.
Australian Journal of Plant Physiology 10 , — Furbank RT. Walking the C 4 pathway: past, present, and future. Journal of Experimental Botany 67 , — Gillon JS Yakir D. Naturally low carbonic anhydrase activity in C 4 and C 3 plants limits discrimination against COO -O during photosynthesis. Bundle-sheath leakiness and intrinsic water use efficiency of a perennial C 4 grass are increased at high vapour pressure deficit during growth. Evolution of C4 photosynthesis in the genus Flaveria: how many and which genes does it take to make C4?
The Plant Cell 23 , — A MEM1-like motif directs mesophyll cell-specific expression of the gene encoding the C 4 carbonic anhydrase in Flaveria. Hatch MD. C 4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta , 81 — C 4 photosynthesis—an unlikely process full of surprises. Plant and Cell Physiology 33 , — Photosynthesis by sugar-cane leaves. A new carboxylation reaction and the pathway of sugar formation. The Biochemical journal , — Predicting C 4 photosynthesis evolution: modular, individually adaptive steps on a Mount Fuji fitness landscape.
After reactions interconverting the C 4 acids, oxaloacetate, malate and aspartate, the 4-carboxyl of one of these acids is transferred to become the carboxyl group of 3-PGA and they speculated that the remaining 3-carbons of the dicarboxylic acid might serve as a precursor to regenerate pyruvate or PEP.
Soon after, they named this process the C 4 dicarboxylic acid pathway of photosynthesis which was later abbreviated to the C 4 pathway or C 4 photosynthesis see Figure 3. Figure 3. C 4 photosynthesis is an evolutionary development where specialised mesophyll cells initially fix CO 2 from the air into 4-carbon acids which are transported to the site of the Calvin PCR cycle in the bundle sheath. The bundle sheath cells are relatively impermeable to CO 2 , so that when the CO 2 is released here from the 4-carbon acids, it builds up to high levels.
The C 4 photosynthetic mechanism is a biochemical CO 2 pump. C 4 photosynthesis is an evolutionary pathway shown here overlayed on a micrograph of a C 4 leaf, showing bundle sheath and mesophyll cells.
Rubisco and the other PCR enzymes are in the bundle sheath cells while phosphoenolpyruvate PEP carboxylase is part of the CO 2 pump in the mesophyll cells. Original drawings courtesy M. Then followed a series of studies where predictions based on existing information led to discoveries about the enzymes involved which in turn allowed further predictions.
For instance, radiotracer studies predicted a primary carboxylation reaction involving either PEP or pyruvate. A search for such an enzyme revealed that sugarcane and other plants showing this unconventional C 4 -type labelling contained very high levels of PEP carboxylase, with up to 50 times the activities seen in leaves of non-C 4 -type plants.
You can imagine the difficulties this caused in the early stages of our studies on these enzymes, with activities varying widely from day to day depending on how fast one got from the glasshouse to the laboratory. By , work on photosynthesis in the Colonial Sugar Refining Company laboratory in Brisbane had been terminated and the group broke up.
In December , an international meeting on Photosynthesis and Photorespiration was held in Canberra, and provided the first opportunity for the growing number of people with an interest in C 4 photosynthesis to get together. The proceedings of this meeting were published in and helped to cement together into some kind of cohesive story, the various strands of the overall C 4 photosynthetic phenomenon- the unique biochemistry with the special Kranz anatomy and ultrastructural features, the special physiological and performance characteristics, and the emerging taxonomic patterns distinguishing C 3 and C 4 plants.
At this meeting, Olle Bjorkman from the Carnegie Institute, Stanford and Marshall Hatch, proposed what was to become a very important element of C 4 philosophy — that the function of the process was to concentrate CO 2 for fixation by the Calvin cycle.
The following five years saw the delineation of two alternatives to NADP malic enzyme for the decarboxylation of C 4 acids in bundle sheath cells. The fact that evolving C 4 plants came up with three separate mechanisms for decarboxylating C4 acids in bundle sheath cells was one of the many surprising features of this process. Other surprises included the involvement of mitochondria in C 4 acid decarboxylation in two of these three sub-groups and the operation of unique chloroplasts with no Rubisco and sometimes no Photosystem II activity.
For instance, we spent many years trying to understand the nature of the decarboxylation process in PEP carboxykinase-type species. Understanding the unique mechanism of dark-light regulation of pyruvate, Pi dikinase was a long and slow process extending over nearly twenty years. In recent times we have also been able to directly and quantitatively demonstrate what was suspected for some time — that the mesophyll-bundle sheath cell interface in C 4 leaves is remarkably permeable to metabolites, thus facilitating the essential rapid flux of metabolites between mesophyll and bundle sheath cells, but remarkably impermeable to CO 2 , thus permitting the concentrating of CO 2 in bundle sheath cells with acceptable efficiency.
We are also slowly getting more quantitative information about the bundle sheath inorganic carbon pool and the likely concentration of CO 2 , as such, in these cells. The studies on pyruvate, Pi dikinase were plagued by an array of unusual circumstances and experimental problems that mitigated against its discovery and the elucidation of its mechanism of action and regulation.
Early studies on the enzyme were difficult because of its ephemeral activity. Aust J Plant Physiol — Hatch MD C4 photosynthesis: a historical overview. Academic Press, New York. Hatch MD and Slack CR Photosynthesis in sugarcane leaves: a new carboxylation reaction and the pathway of sugar formation. Biochem J — Biochem Biophys Res Commun — World Scientific Publishing, Singapore.
Karpilov YS The distribution of radioactive carbon 14 amongst the products of photosynthesis of maize. Trudy Kazansk Sel'shokoz Institute 15— Plant Physiol — Photosynth Res — Slack CR and Hatch MD Comparative studies on the activity of carboxylases and other enzymes in relation to the new pathway of photosynthetic carbon dioxide fixation in tropical grasses.
Download references. You can also search for this author in PubMed Google Scholar. Reprints and Permissions. Hatch, M. C 4 photosynthesis: discovery and resolution.
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