Exploring the possible role of hybridization in the evolution of photosynthetic pathways in Flaveria (Asteraceae), the prime model of C₄ photosynthesis evolution

Abstract

Flaveria (Asteraceae) is the prime model for the study of C4 photosynthesis evolution and seems to support a stepwise acquisition of the pathway through C3-C4 intermediate phenotypes, still existing in Flaveria today. Molecular phylogenies of Flaveria based on concatenated data matrices are currently used to reconstruct the complex sequence of trait shifts during C4 evolution. To assess the possible role of hybridization in C4 evolution in Flaveria, we re-analyzed transcriptome data of 17 Flaveria species to infer the extent of gene tree discordance and possible reticulation events. We found massive gene tree discordance as well as reticulation along the backbone and within clades containing C3-C4 intermediate and C4-like species. An early hybridization event between two C3 species might have triggered C4 evolution in the genus. The clade containing all C4 species plus the C4-like species F. vaginata and F. palmeri is robust but of hybrid origin involving F. angustifolia and F. sonorensis (both C3-C4 intermediate) as parental lineages. Hybridization seems to be a driver of C4 evolution in Flaveria and likely promoted the fast acquisition of C4 traits. This new insight can be used in further exploring C4 evolution and can inform C4 bioengineering efforts.

On the hybrid origin of the C2Salsola divaricata agg. (Amaranthaceae) from C3 and C4 parental lineages

“…or antecedent traits from a parental lineage giving them an adaptive advantage that might have influenced their photosynthesis pathway, e.g., adaptations in photosynthesis or photorespiration associated enzymes or Kranz-cells. This is in line with recent findings in the genus Flaveria (Morales-Briones and Kadereit, 2022) where ancient hybridization was found to be a step towards C4 evolution and likely promoted the rapid acquisition of C4 traits. We also found hybridization events in the two clades in the other networks with similar parental lineages, supporting the evidence that these lineages were involved in hybridization events.…”

“…For a few examples, it has been suggested that this might also occur in nature (Dunning et al, 2017) which could mean an immediate adaptive advantage of the hybrid lineage in more stressful environments. A phylogenomic study of Flaveria revealed a major role of hybridization and transgressive segregation in C 4 evolution (Morales-Briones and Kadereit, 2022). In this study we aimed to infer the phylogenetic origin of C 3 -C 4 intermediacy of the Salsola divaricata agg.…”

“…To investigate the possibility of a hybrid origin of a C 3 -C 4 intermediate lineage, detailed phylogenomic studies are needed. For example, evidence of recent and ancient events of reticulate evolution in a phylogenomic study of Flaveria revealed a potential major role of hybridization in the evolution of C 4 photosynthesis in that genus (Morales-Briones and Kadereit, 2022).…”

On the hybrid origin of the C2Salsola divaricata agg. (Amaranthaceae) from C3 and C4 parental lineages

“…For a few examples, it has been suggested that this might also occur in nature (Dunning et al ., 2017); that could mean an immediate adaptive advantage of the hybrid lineage in more stressful environments. A phylogenomic study of Flaveria revealed a major role of hybridisation and transgressive segregation in C 4 evolution (Morales‐Briones & Kadereit, 2022). In this study we aimed to infer the phylogenetic origin of the C 3 –C 4 intermediacy of the Salsola divaricata agg.…”

“…To investigate the possibility of a hybrid origin of a C 3 –C 4 intermediate lineage, detailed phylogenomic studies are needed. For example, evidence of recent and ancient events of reticulate evolution in a phylogenomic study of Flaveria revealed a potential major role of hybridisation in the evolution of C 4 photosynthesis in that genus (Morales‐Briones & Kadereit, 2022).…”