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C 4 photosynthesis evolved multiple times independently from ancestral C 3 photosynthesis in a broad range of flowering land plant families and in both monocots and dicots. The evolution of C 4 photosynthesis entails the recruitment of enzyme activities that are not involved in photosynthetic carbon fixation in C 3 plants to photosynthesis. This requires a different regulation of gene expression as well as a different regulation of enzyme activities in comparison to the C 3 context. Further, C 4 photosynthesis relies on a distinct leaf anatomy that differs from that of C 3 , requiring a differential regulation of leaf development in C 4 . We summarize recent progress in the understanding of C 4 -specific features in evolution and metabolic regulation in the context of C 4 photosynthesis.

Harnessing natural variation in photosynthetic capacity is a promising route toward yield increases, but physiological phenotyping is still too laborious for large-scale genetic screens. Here, we evaluate the potential of leaf reflectance spectroscopy to predict parameters of photosynthetic capacity in Brassica oleracea and Zea mays, a C 3 and a C 4 crop, respectively. To this end, we systematically evaluated properties of reflectance spectra and found that they are surprisingly similar over a wide range of species. We assessed the performance of a wide range of machine learning methods and selected recursive feature elimination on untransformed spectra followed by partial least squares regression as the preferred algorithm that yielded the highest predictive power. Learning curves of this algorithm suggest optimal species-specific sample sizes. Using the Brassica relative Moricandia, we evaluated the model transferability between species and found that cross-species performance cannot be predicted from phylogenetic proximity. The final intra-species models predict crop photosynthetic capacity with high accuracy. Based on the estimated model accuracy, we simulated the use of the models in selective breeding experiments, and showed that high-throughput photosynthetic phenotyping using our method has the potential to greatly improve breeding success. Our results indicate that leaf reflectance phenotyping is an efficient method for improving crop photosynthetic capacity., (Copyright © 2017 The Author. Published by Elsevier Inc. All rights reserved.)

Evolution of C 4 photosynthesis is not distributed evenly in the plant kingdom. Particularly interesting is the situation in the Brassicaceae, because the family contains no C 4 species, but several C 3 -C 4 intermediates, mainly in the genus Moricandia Investigation of leaf anatomy, gas exchange parameters, the metabolome, and the transcriptome of two C 3 -C 4 intermediate Moricandia species, M. arvensis and M. suffruticosa, and their close C 3 relative M. moricandioides enabled us to unravel the specific C 3 -C 4 characteristics in these Moricandia lines. Reduced CO 2 compensation points in these lines were accompanied by anatomical adjustments, such as centripetal concentration of organelles in the bundle sheath, and metabolic adjustments, such as the balancing of C and N metabolism between mesophyll and bundle sheath cells by multiple pathways. Evolution from C 3 to C 3 -C 4 intermediacy was probably facilitated first by loss of one copy of the glycine decarboxylase P-protein, followed by dominant activity of a bundle sheath-specific element in its promoter. In contrast to recent models, installation of the C 3 -C 4 pathway was not accompanied by enhanced activity of the C 4 cycle. Our results indicate that metabolic limitations connected to N metabolism or anatomical limitations connected to vein density could have constrained evolution of C 4 in Moricandia., (© The Author 2016. Published by Oxford University Press on behalf of the Society for Experimental Biology.)

Background: Abiotic stress causes disturbances in the cellular homeostasis. Re-adjustment of balance in carbon, nitrogen and phosphorus metabolism therefore plays a central role in stress adaptation. However, it is currently unknown which parts of the primary cell metabolism follow common patterns under different stress conditions and which represent specific responses., Results: To address these questions, changes in transcriptome, metabolome and ionome were analyzed in maize source leaves from plants suffering low temperature, low nitrogen (N) and low phosphorus (P) stress. The selection of maize as study object provided data directly from an important crop species and the so far underexplored C4 metabolism. Growth retardation was comparable under all tested stress conditions. The only primary metabolic pathway responding similar to all stresses was nitrate assimilation, which was down-regulated. The largest group of commonly regulated transcripts followed the expression pattern: down under low temperature and low N, but up under low P. Several members of this transcript cluster could be connected to P metabolism and correlated negatively to different phosphate concentration in the leaf tissue. Accumulation of starch under low temperature and low N stress, but decrease in starch levels under low P conditions indicated that only low P treated leaves suffered carbon starvation., Conclusions: Maize employs very different strategies to manage N and P metabolism under stress. While nitrate assimilation was regulated depending on demand by growth processes, phosphate concentrations changed depending on availability, thus building up reserves under excess conditions. Carbon and energy metabolism of the C4 maize leaves were particularly sensitive to P starvation.

We systematically analyzed a developmental gradient of the third maize (Zea mays) leaf from the point of emergence into the light to the tip in 10 continuous leaf slices to study organ development and physiological and biochemical functions. Transcriptome analysis, oxygen sensitivity of photosynthesis, and photosynthetic rate measurements showed that the maize leaf undergoes a sink-to-source transition without an intermediate phase of C(3) photosynthesis or operation of a photorespiratory carbon pump. Metabolome and transcriptome analysis, chlorophyll and protein measurements, as well as dry weight determination, showed continuous gradients for all analyzed items. The absence of binary on-off switches and regulons pointed to a morphogradient along the leaf as the determining factor of developmental stage. Analysis of transcription factors for differential expression along the leaf gradient defined a list of putative regulators orchestrating the sink-to-source transition and establishment of C(4) photosynthesis. Finally, transcriptome and metabolome analysis, as well as enzyme activity measurements, and absolute quantification of selected metabolites revised the current model of maize C(4) photosynthesis. All data sets are included within the publication to serve as a resource for maize leaf systems biology.

In the Arabidopsis mutant sdd1-1, a point mutation in a single gene (SDD1) causes specific alterations in stomatal density and distribution. In comparison to the wild type (C24), abaxial surfaces of sdd1-1 rosette leaves have about 2.5-fold higher stomatal densities. This mutant was used to study the consequence of stomatal density on photosynthesis under various light regimes. The increased stomatal density in the mutant had no significant influence on the leaf CO(2) assimilation rate (A) under constant light conditions. Mutant and wild-type plants contained similar amounts of carbohydrates under these conditions. However, exposure of plants to increasing photon flux densities resulted in differences in gas exchange and the carbohydrate metabolism of the wild type and mutant. Increased stomatal densities in sdd1-1 enabled low-light-adapted plants to have 30% higher CO(2) assimilation rates compared to the wild type when exposed to high light intensities. After 2 d under high light conditions leaves of sdd1-1 accumulated 30% higher levels of starch and hexoses than wild-type plants.