Continued Adaptation of C4 Photosynthesis After an Initial Burst of Changes in the Andropogoneae Grasses

Abstract

C$_{4}$ photosynthesis is a complex trait that sustains fast growth and high productivity in tropical and subtropical conditions and evolved repeatedly in flowering plants. One of the major C$_{4}$ lineages is Andropogoneae, a group of $\sim $1200 grass species that includes some of the world’s most important crops and species dominating tropical and some temperate grasslands. Previous efforts to understand C$_{4}$ evolution in the group have compared a few model C$_{4}$ plants to distantly related C$_{3}$ species so that changes directly responsible for the transition to C$_{4}$ could not be distinguished from those that preceded or followed it. In this study, we analyze the genomes of 66 grass species, capturing the earliest diversification within Andropogoneae as well as their C$_{3}$ relatives. Phylogenomics combined with molecular dating and analyses of protein evolution show that many changes linked to the evolution of C$_{4}$ photosynthesis in Andropogoneae happened in the Early Miocene, between 21 and 18 Ma, after the split from its C$_{3}$ sister lineage, and before the diversification of the group. This initial burst of changes was followed by an extended period of modifications to leaf anatomy and biochemistry during the diversification of Andropogoneae, so that a single C$_{4}$ origin gave birth to a diversity of C$_{4}$ phenotypes during 18 million years of speciation events and migration across geographic and ecological spaces. Our comprehensive approach and broad sampling of the diversity in the group reveals that one key transition can lead to a plethora of phenotypes following sustained adaptation of the ancestral state. [Adaptive evolution; complex traits; herbarium genomics; Jansenelleae; leaf anatomy; Poaceae; phylogenomics.]

Resolving the Phylogeny of the Olive Family (Oleaceae): Confronting Information from Organellar and Nuclear Genomes

“…We assembled full plastomes and the nrDNA cluster following the methods of Bianconi et al [ 56 ]. Sequencing depth in these genomic regions was superior to 100× for all investigated species.…”

“…Each sample was paired-end sequenced (150 bp) on 1/24th of an Illumina HiSeq3000 lane and multiplexed with samples from the same or different projects. We assembled full plastomes and the nrDNA cluster following the methods of Bianconi et al [56]. Sequencing depth in these genomic regions was superior to 100× for all investigated species.…”

Phylogenomics enables biogeographic analysis and a new subtribal classification of Andropogoneae (Poaceae—Panicoideae)

“…Hubb. was used to root the trees, according to GPWG II (2012), Morrone et al (2012), and Bianconi et al (2020).…”

“…In addition to the new plastomes generated for this study, other plastomes were retrieved from previous studies (e.g., Burke et al, 2016;Arthan et al, 2017;McAllister et al, 2018;Lloyd Evans et al, 2019;Bianconi et al, 2020). Voucher specimens, GenBank accession numbers, and original references (when applicable) of the plastome sequences are listed in Table S1. 2.2 DNA extraction, plastome sequencing, and assembly DNA was isolated using a modified CTAB protocol adapted from Doyle & Doyle (1987) from live and silica dried leaves.…”

Reticulate evolution, lateral gene transfer, and innovation in plants

“…The remarkable adaptations that have allowed plants to colonize most environments around the globe did not arise over night. In some cases, protracted evolutionary periods were required to incrementally modify genes either inherited from their ancestors or originating de novo in the genome (Bianconi et al., in press). Reticulation events have the potential to speed up this process and even provide access to new traits that would otherwise have been out of reach of natural selection.…”