TY - JOUR

T1 - Contrasted histories of organelle and nuclear genomes underlying physiological diversification in a grass species

T2 - Intraspecific dispersal of C4 physiology

AU - Bianconi, M.E.

AU - Dunning, L.T.

AU - Curran, E.V.

AU - Hidalgo, O.

AU - Powell, R.F.

AU - Mian, S.

AU - Leitch, I.J.

AU - Lundgren, M.R.

AU - Manzi, S.

AU - Vorontsova, M.S.

AU - Besnard, G.

AU - Osborne, C.P.

AU - Olofsson, J.K.

AU - Christin, P.-A.

PY - 2020/11/11

Y1 - 2020/11/11

N2 - C 4 photosynthesis evolved multiple times independently in angiosperms, but most origins are relatively old so that the early events linked to photosynthetic diversification are blurred. The grass Alloteropsis semialata is an exception, as this species encompasses C 4 and non-C 4 populations. Using phylogenomics and population genomics, we infer the history of dispersal and secondary gene flow before, during and after photosynthetic divergence in A. semialata. We further analyse the genome composition of individuals with varied ploidy levels to establish the origins of polyploids in this species. Detailed organelle phylogenies indicate limited seed dispersal within the mountainous region of origin and the emergence of a C 4 lineage after dispersal to warmer areas of lower elevation. Nuclear genome analyses highlight repeated secondary gene flow. In particular, the nuclear genome associated with the C 4 phenotype was swept into a distantly related maternal lineage probably via unidirectional pollen flow. Multiple intraspecific allopolyploidy events mediated additional secondary genetic exchanges between photosynthetic types. Overall, our results show that limited dispersal and isolation allowed lineage divergence, with photosynthetic innovation happening after migration to new environments, and pollen-mediated gene flow led to the rapid spread of the derived C 4 physiology away from its region of origin.

AB - C 4 photosynthesis evolved multiple times independently in angiosperms, but most origins are relatively old so that the early events linked to photosynthetic diversification are blurred. The grass Alloteropsis semialata is an exception, as this species encompasses C 4 and non-C 4 populations. Using phylogenomics and population genomics, we infer the history of dispersal and secondary gene flow before, during and after photosynthetic divergence in A. semialata. We further analyse the genome composition of individuals with varied ploidy levels to establish the origins of polyploids in this species. Detailed organelle phylogenies indicate limited seed dispersal within the mountainous region of origin and the emergence of a C 4 lineage after dispersal to warmer areas of lower elevation. Nuclear genome analyses highlight repeated secondary gene flow. In particular, the nuclear genome associated with the C 4 phenotype was swept into a distantly related maternal lineage probably via unidirectional pollen flow. Multiple intraspecific allopolyploidy events mediated additional secondary genetic exchanges between photosynthetic types. Overall, our results show that limited dispersal and isolation allowed lineage divergence, with photosynthetic innovation happening after migration to new environments, and pollen-mediated gene flow led to the rapid spread of the derived C 4 physiology away from its region of origin.

KW - admixture

KW - C 4 photosynthesis

KW - miombo woodlands

KW - phylogenomics

KW - phylogeography

KW - polyploidy

KW - C4 plant

KW - cell organelle

KW - dispersal

KW - genome

KW - grass

KW - physiology

KW - Alloteropsis semialata

KW - Magnoliophyta

U2 - 10.1098/rspb.2020.1960rspb20201960

DO - 10.1098/rspb.2020.1960rspb20201960

M3 - Journal article

VL - 287

JO - Proceedings of the Royal Society B: Biological Sciences

JF - Proceedings of the Royal Society B: Biological Sciences

SN - 0962-8452

IS - 1938

M1 - 20201960

ER -