Spatial resolution of an integrated C+CAM photosynthetic metabolism.

C and CAM photosynthesis have repeatedly evolved in plants over the past 30 million years. Because both repurpose the same set of enzymes but differ in their spatial and temporal deployment, they have long been considered as distinct and incompatible adaptations. contains multiple C species that perform CAM when droughted.

Gene co-expression reveals the modularity and integration of C4 and CAM in Portulaca.

C4 photosynthesis and Crassulacean acid metabolism (CAM) have been considered as largely independent adaptations despite sharing key biochemical modules. Portulaca is a geographically widespread clade of over 100 annual and perennial angiosperm species that primarily use C4 but facultatively exhibit CAM when drought stressed, a photosynthetic system known as C4 + CAM. It has been hypothesized that C4 + CAM is rare because of pleiotropic constraints, but these have not been deeply explored.

C and crassulacean acid metabolism within a single leaf: deciphering key components behind a rare photosynthetic adaptation.

Although biochemically related, C and crassulacean acid metabolism (CAM) systems are expected to be incompatible. However, Portulaca species, including P. oleracea, operate C and CAM within a single leaf, and the mechanisms behind this unique photosynthetic arrangement remain largely unknown.

Key changes in gene expression identified for different stages of C4 evolution in Alloteropsis semialata.

C4 photosynthesis is a complex trait that boosts productivity in tropical conditions. Compared with C3 species, the C4 state seems to require numerous novelties, but species comparisons can be confounded by long divergence times. Here, we exploit the photosynthetic diversity that exists within a single species, the grass Alloteropsis semialata, to detect changes in gene expression associated with different photosynthetic phenotypes.

The genetics of convergent evolution: insights from plant photosynthesis.

The tree of life is resplendent with examples of convergent evolution, whereby distinct species evolve the same trait independently. Many highly convergent adaptations are also complex, which makes their repeated emergence surprising. In plants, the evolutionary history of two carbon concentrating mechanisms (CCMs) - C and crassulacean acid metabolism (CAM) photosynthesis - presents such a paradox.

Lateral transfers of large DNA fragments spread functional genes among grasses.

A fundamental tenet of multicellular eukaryotic evolution is that vertical inheritance is paramount, with natural selection acting on genetic variants transferred from parents to offspring. This lineal process means that an organism's adaptive potential can be restricted by its evolutionary history, the amount of standing genetic variation, and its mutation rate. Lateral gene transfer (LGT) theoretically provides a mechanism to bypass many of these limitations, but the evolutionary importance and frequency of this process in multicellular eukaryotes, such as plants, remains debated.

C anatomy can evolve via a single developmental change.

C photosynthesis is a complex trait that boosts productivity in warm environments. Paradoxically, it evolved independently in numerous plant lineages, despite requiring specialised leaf anatomy. The anatomical modifications underlying C evolution have previously been evaluated through interspecific comparisons, which capture numerous changes besides those needed for C functionality.

Gene duplication and dosage effects during the early emergence of C4 photosynthesis in the grass genus Alloteropsis.

The importance of gene duplication for evolutionary diversification has been mainly discussed in terms of genetic redundancy allowing neofunctionalization. In the case of C4 photosynthesis, which evolved via the co-option of multiple enzymes to boost carbon fixation in tropical conditions, the importance of genetic redundancy has not been consistently supported by genomic studies. Here, we test for a different role for gene duplication in the early evolution of C4 photosynthesis, via dosage effects creating rapid step changes in expression levels.

Highly Expressed Genes Are Preferentially Co-Opted for C4 Photosynthesis.

Novel adaptations are generally assembled by co-opting pre-existing genetic components, but the factors dictating the suitability of genes for new functions remain poorly known. In this work, we used comparative transcriptomics to determine the attributes that increased the likelihood of some genes being co-opted for C4 photosynthesis, a convergent complex trait that boosts productivity in tropical conditions. We show that independent lineages of grasses repeatedly co-opted the gene lineages that were the most highly expressed in non-C4 ancestors to produce their C4 pathway.

Introgression and repeated co-option facilitated the recurrent emergence of C photosynthesis among close relatives.

The origins of novel traits are often studied using species trees and modeling phenotypes as different states of the same character, an approach that cannot always distinguish multiple origins from fewer origins followed by reversals. We address this issue by studying the origins of C photosynthesis, an adaptation to warm and dry conditions, in the grass Alloteropsis. We dissect the C trait into its components, and show two independent origins of the C phenotype via different anatomical modifications, and the use of distinct sets of genes.