The Coordination and Jumps along C4 Photosynthesis Evolution in the Genus Flaveria

Abstract

C4 photosynthesis is a remarkable complex trait, elucidations of the evolutionary trajectory of C4 photosynthesis from its ancestral C3 pathway can help us better understand the generic principles of the evolution of complex trait and guide the engineering of C3 crops for higher yields. Here, we used the genus Flaveria that contains C3, C3-C4, C4-like and C4 species as a system to study the evolution of C4 photosynthesis. We first mapped transcript abundance, protein sequence, and morphological features to the phylogenetic tree of the genus Flaveria, and calculated the evolutionary correlation of different features; we then predicted the relative changes of ancestral nodes of those features to illustrate the key stages during the evolution of C4 photosynthesis. We found that gene expression and protein sequence showed consistent modification pattern along the phylogenetic tree. High correlation coefficients ranging from 0.46 to 0.9 among gene expression, protein sequence and morphology were observed, and the greatest modification of those different features consistently occurred at the transition between C3-C4 species and C4-like species. Our results show highly coordinated changes in gene expression, protein sequence and morphological features, which support an obviously evolutionary jump during the evolution of C4 metabolism.

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

“…Our analyses recovered F. brownii (C4-like) + F. sonorensis (C3-C4) as sister to the remaining species in Clade B. The remaining species, all C3-C4, had similar relationships as inLyu et al (2015) with F. anomala as sister to the clade F. pubescens, F. chlorifolia + F. floridana.…”

“…Test significance was assessed with a Bonferroni correction (α= 0.05) for the number of hypothesis tests conducted with estimates of γ between 0 and 1 (Blischak et al, 2018). We carried out HyDe hybridization test using all species and without F. pringlei (C3), as it has been identified as a potential artificial hybrid (Lyu et al, 2015).…”

“…Therefore, a phylogenetic study exploring the occurrence and location of past reticulation events is needed. Comprehensive molecular phylogenetic studies of Flaveria published so far were either based on few molecular markers only (McKown et al, 2005), or on concatenated data matrices and inference methods unable to reveal tree discordance, possible reticulation, or incomplete lineage sorting (Lyu et al, 2015). Irrespective of this, numerous current studies of evolutionary change during the establishment of the C4 pathway rely on the Flaveria model (e.g., Lyu et al, 2021;Taniguchi et al, 2021).…”

“…Flaveria cronquistii (C3), F. robusta (C3) and F. pringlei (C3) + F. angustifolia (C3-C4) formed a grade which is sister to Clade A + Clade B (clades names followedMcKown et al, 2005). Clade A from IQ-TREE comprised the same species and relationships as inLyu et al (2015). Flaveria ramosissima (C3-C4) and F. palmeri (C4-like) were successive sisters to F. kochiana (C4) + F. vaginata (C4-like) and the C4 clade [(F. bidentis, F. trinervia + F australasica); BS = 83].…”

“…The ASTRAL tree recovered F. bidentis (C4) sister to F. kochiana (C4) + F. vaginata (C4-like; LLP = 0.96; Fig.S1). Clade B included the same species as inLyu et al (2015) but also included F. sonorensis (C3-C4). Our analyses recovered F. brownii (C4-like) + F. sonorensis (C3-C4) as sister to the remaining species in Clade B.…”