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. Phylogenetically informed comparative transcriptomics show that intermediates with a weak C4 cycle are separated from the C3 phenotype by increases in the expression of 58 genes (0.22% of genes expressed in the leaves), including those encoding just three core C4 enzymes: aspartate aminotransferase, phosphoenolpyruvate carboxykinase, and phosphoenolpyruvate carboxylase. The subsequent transition to full C4 physiology was accompanied by increases in another 15 genes (0.06%), including only the core C4 enzyme pyruvate orthophosphate dikinase. These changes probably created a rudimentary C4 physiology, and isolated populations subsequently improved this emerging C4 physiology, resulting in a patchwork of expression for some C4 accessory genes. Our work shows how C4 assembly in A. semialata happened in incremental steps, each requiring few alterations over the previous step. These create short bridges across adaptive landscapes that probably facilitated the recurrent origins of C4 photosynthesis through a gradual process of evolution.
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Genetic exchanges between closely related groups of organisms with different adaptations have well-documented beneficial and detrimental consequences. In plants, pollen-mediated exchanges affect the sorting of alleles across physical landscapes and influence rates of hybridization. How these dynamics affect the emergence and spread of novel phenotypes remains only partially understood. Here, we use phylogenomics and population genomics to retrace the origin and spread of two geographically overlapping ecotypes of the African grass
Alloteropsis angusta
. In addition to an ecotype inhabiting wetlands, we report the existence of a previously undescribed ecotype inhabiting Miombo woodlands and grasslands. The two ecotypes are consistently associated with different nuclear groups, which represent an advanced stage of divergence with secondary low-level gene flow. However, the seed-transported chloroplast genomes are consistently shared by distinct ecotypes inhabiting the same region. These patterns suggest that the nuclear genome of one ecotype can enter the seeds of the other via occasional pollen movements with sorting of nuclear groups in subsequent generations. The contrasting ecotypes of
A. angusta
can thus use each other as a gateway to new locations across a large part of Africa, showing that hybridization can facilitate the geographical dispersal of distinct ecotypes of the same grass species.
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