Low dispersal and ploidy differences in a grass maintain photosynthetic diversity despite gene flow and habitat overlap

Olofsson, Jill K.; Curran, Emma V.; Nyirenda, Florence; Bianconi, Matheus E; Dunning, Luke T.; Milenkovic, Vanja; Sotelo, Graciela; Hidalgo, Oriane; Powell, Robyn F.; Lundgren, Marjorie R.; Leitch, Ilia J.; Nosil, Patrik; Osborne, Colin P.; Christin, Pascal‐Antoine

doi:10.1111/mec.15871

Cited by 17 publications

(54 citation statements)

References 104 publications

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“…The C 4 metabolism relies on a biochemical cycle operating within a specialized leaf anatomy, which concentrates CO 2 around Rubisco, suppressing the energetically-costly photorespiratory pathway (Hatch 1987). The C 4 trait is highly polyphyletic, but its multiple origins Southern Africa, genetic analyses have shown that natural hybrids are rare (Olofsson et al 2016;Bianconi et al 2020;Olofsson et al 2021). The lack of a clear hybrid zone has been partially explained by the differences in ploidy levels among photosynthetic types where they are found in sympatry (Olofsson et al 2021).…”

Section: Introductionmentioning

confidence: 99%

“…Alloteropsis semialata has a paleotropical distribution, with C 3 and C 3 +C 4 populations in Southern and Central/Eastern regions of Africa, respectively, and C 4 individuals occurring across Africa, South and Southeast Asia, and Oceania (Lundgren et al 2015; Olofsson et al 2016; Bianconi et al 2020; Olofsson et al 2021). The photosynthetic types in A. semialata are associated with distinct genetic lineages (Lundgren et al 2015; Olofsson et al 2016), which initially diverged around 3 Mya (Bianconi et al 2020).…”

Section: Introductionmentioning

confidence: 99%

“…The photosynthetic types in A. semialata are associated with distinct genetic lineages (Lundgren et al 2015; Olofsson et al 2016), which initially diverged around 3 Mya (Bianconi et al 2020). Although the ranges of C 4 and non-C 4 lineages geographically overlap in some regions of Africa, with C 3 +C 4 and C 4 in Central/Eastern Africa, and C 3 and C 4 in Southern Africa, genetic analyses have shown that natural hybrids are rare (Olofsson et al 2016; Bianconi et al 2020; Olofsson et al 2021). The lack of a clear hybrid zone has been partially explained by the differences in ploidy levels among photosynthetic types where they are found in sympatry (Olofsson et al 2021).…”

Section: Introductionmentioning

confidence: 99%

“…Although the ranges of C 4 and non-C 4 lineages geographically overlap in some regions of Africa, with C 3 +C 4 and C 4 in Central/Eastern Africa, and C 3 and C 4 in Southern Africa, genetic analyses have shown that natural hybrids are rare (Olofsson et al 2016; Bianconi et al 2020; Olofsson et al 2021). The lack of a clear hybrid zone has been partially explained by the differences in ploidy levels among photosynthetic types where they are found in sympatry (Olofsson et al 2021). However, the broad ranges of C 4 and C 3 +C 4 diploids overlap, and they have been coexisting for at least one million years (Lundgren et al 2015; Bianconi et al 2020).…”

Section: Introductionmentioning

confidence: 99%

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Upregulation of C₄ characteristics does not consistently improve photosynthetic performance in intraspecific hybrids of a grass

Bianconi

Sotelo

Curran

et al. 2021

Preprint

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C4 photosynthesis is thought to have evolved via intermediate stages, with changes towards the C4 phenotype gradually enhancing photosynthetic performance. This hypothesis is widely supported by modelling studies, but experimental tests are missing. Mixing of C4 components to generate artificial intermediates can be achieved via crossing, and the grass Alloteropsis semialata represents an outstanding system since it includes C4 and non-C4 populations. Here, we analyse F1 hybrids between C3 and C4, and C3+C4 and C4 genotypes to determine whether the acquisition of C4 characteristics increases photosynthetic performance. The hybrids have leaf anatomical characters and C4 gene expression profiles that are largely intermediate between those of their parents. Carbon isotope ratios are similarly intermediate, which suggests that a partial C4 cycle coexists with C3 carbon fixation in the hybrids. This partial C4 phenotype is associated with C4-like photosynthetic efficiency in C3+C4 x C4, but not in C3 x C4 hybrids, which are overall less efficient than both parents. Our results support the hypothesis that the photosynthetic gains from the upregulation of C4 characteristics depend on coordinated changes in anatomy and biochemistry. The order of acquisition of C4 components is thus constrained, with C3+C4 species providing an essential step for C4 evolution.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Upregulation of C₄ characteristics does not consistently improve photosynthetic performance in intraspecific hybrids of a grass

Bianconi

Sotelo

Curran

et al. 2021

Preprint

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“…The copyright holder for this preprint this version posted April 18, 2021. ; https://doi.org/10.1101/2021.04.16.440116 doi: bioRxiv preprint angusta individuals, and 15 newly sequenced A. semialata, which were combined with 49 previously sequenced A. semialata (Olofsson et al, 2021;Table S1).…”

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confidence: 99%

Hybridisation boosts dispersal of two contrasted ecotypes in a grass species

et al. 2021

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In the absence of strong reproductive barriers, 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 hybridisation. How these dynamics affect the emergence and spread of novel ecological strategies remains only partially understood. We use phylogenomics and population genomics to retrace the origin of two geographically overlapping ecotypes of the African grass Alloteropsis angusta. We report the existence of a previously undescribed ecotype inhabiting miombo woodlands and grasslands. The two ecotypes have divergent nuclear genomes. 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 reach the seeds of the other via pollen movements, with strong selection subsequently sorting nuclear alleles by habitat. The contrasting ecotypes of A. angusta can use each other as a gateway to new locations across a large part of Africa. Coupled with newly discovered hybridisation with the sister species A. semialata, our results show that hybridisation can facilitate the geographical dispersal of distinct ecotypes of the same grass species.

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Interspecific transfer of genetic information through polyploid bridges

Kauai,

Bafort,

Mortier

et al. 2024

Proc. Natl. Acad. Sci. U.S.A.

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Hybridization blurs species boundaries and leads to intertwined lineages resulting in reticulate evolution. Polyploidy, the outcome of whole genome duplication (WGD), has more recently been implicated in promoting and facilitating hybridization between polyploid species, potentially leading to adaptive introgression. However, because polyploid lineages are usually ephemeral states in the evolutionary history of life it is unclear whether WGD-potentiated hybridization has any appreciable effect on their diploid counterparts. Here, we develop a model of cytotype dynamics within mixed-ploidy populations to demonstrate that polyploidy can in fact serve as a bridge for gene flow between diploid lineages, where introgression is fully or partially hampered by the species barrier. Polyploid bridges emerge in the presence of triploid organisms, which despite critically low levels of fitness, can still allow the transfer of alleles between diploid states of independently evolving mixed-ploidy species. Notably, while marked genetic divergence prevents polyploid-mediated interspecific gene flow, we show that increased recombination rates can offset these evolutionary constraints, allowing a more efficient sorting of alleles at higher-ploidy levels before introgression into diploid gene pools. Additionally, we derive an analytical approximation for the rate of gene flow at the tetraploid level necessary to supersede introgression between diploids with nonzero introgression rates, which is especially relevant for plant species complexes, where interspecific gene flow is ubiquitous. Altogether, our results illustrate the potential impact of polyploid bridges on the (re)distribution of genetic material across ecological communities during evolution, representing a potential force behind reticulation.

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Low dispersal and ploidy differences in a grass maintain photosynthetic diversity despite gene flow and habitat overlap

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 17 publications

References 104 publications

Upregulation of C₄ characteristics does not consistently improve photosynthetic performance in intraspecific hybrids of a grass

Upregulation of C₄ characteristics does not consistently improve photosynthetic performance in intraspecific hybrids of a grass

Hybridisation boosts dispersal of two contrasted ecotypes in a grass species

Interspecific transfer of genetic information through polyploid bridges

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Low dispersal and ploidy differences in a grass maintain photosynthetic diversity despite gene flow and habitat overlap

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 17 publications

References 104 publications

Upregulation of C4 characteristics does not consistently improve photosynthetic performance in intraspecific hybrids of a grass

Upregulation of C4 characteristics does not consistently improve photosynthetic performance in intraspecific hybrids of a grass

Hybridisation boosts dispersal of two contrasted ecotypes in a grass species

Interspecific transfer of genetic information through polyploid bridges

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Upregulation of C₄ characteristics does not consistently improve photosynthetic performance in intraspecific hybrids of a grass

Upregulation of C₄ characteristics does not consistently improve photosynthetic performance in intraspecific hybrids of a grass