Dynamic changes of genome sizes and gradual gain of cell‐specific distribution of C₄ enzymes during C₄ evolution in genus Flaveria

Abstract

C 4 plants are believed to have evolved from C 3 plants through various C 3 -C 4 intermediate stages in which a photorespiration-dependent CO 2 concentration system known as C 2 photosynthesis operates. Genes involved in the C 4 cycle were thought to be recruited from orthologs present in C 3 species and developed cell-specific expression during C 4 evolution. To understand the process of establishing C 4 photosynthesis, we performed whole-genome sequencing and investigated expression and mesophyll-or bundle-sheath-cell-specific localization of phosphoenolpyruvate carboxylase (PEPC), NADP-malic enzyme (NADP-ME), pyruvate, orthophosphate dikinase (PPDK) in C 3 , C 3 -C 4 intermediate, C 4 -like, and C 4 Flaveria species. While genome sizes vary greatly, the number of predicted protein-coding genes was similar among C 3 , C 3 -C 4 intermediate, C 4 -like, and C 4 Flaveria species. Cell-specific localization of the PEPC, NADP-ME, and PPDK transcripts was insignificant or weak in C 3 -C 4 intermediate species, whereas these transcripts were expressed celltype specific in C 4 -like species. These results showed that elevation of gene expression and cell-specific control of pre-existing C 4 cycle genes in C 3 species was involved in C 4 evolution. Gene expression was gradually enhanced during C 4 evolution, whereas cell-specific control was gained independently of quantitative transcriptional activation during evolution from C 3 -C 4 intermediate to C 4 photosynthesis in genus Flaveria.

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

“…It clearly outcompetes its parental lineages in terms of C 4 physiology. Taniguchi et al (2021), studying genome size evolution in Flaveria , showed dynamic alteration of genome size in the genus with F. brownii having the largest genome size among the 11 species investigated. Rewiring the parental genomes might have led to the C 4 -like phenotype found in F. brownii and might have facilitated adaptive divergence resulting in colonization of the coastal flats and islands of the lower Texas Gulf Coast.…”

“…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 C 4 pathway rely on the Flaveria model (e.g., Lyu et al, 2021; Taniguchi et al, 2021).…”

Two cyclic electron flows around photosystem I differentially participate in C4photosynthesis

“…1A). The expression of all three PGR5 genes identified in the Flaveria genome (PGR5A, PGR5B, and PGR5C; Taniguchi et al, 2021) was suppressed in the PGR5-RNAi lines. The protein levels of PGR5, PGRL1, and NdhH were undetectable or less than 6% of the WT levels in the PGR5-RNAi, PGRL1-RNAi, and NdhO-RNAi lines, respectively (Fig.…”

Born with intronless ERF transcriptional factors: C4photosynthesis inherits a legacy dating back 450 million years

“…However, due to a lack of genome reference, current knowledge of the regulation of photosynthesis genes in this genus is still very limited. The first version of Flaveria genome references, including four species, were published recently (Taniguchi et al, 2021), and provide valuable resources for protein coding gene predictions for this genus. However, as these genomes were generated using short-read whole genome-sequencing, the assembled genomes are fragmented, which compromises their potential application (Taniguchi et al, 2021).…”

“…The first version of Flaveria genome references, including four species, were published recently (Taniguchi et al, 2021), and provide valuable resources for protein coding gene predictions for this genus. However, as these genomes were generated using short-read whole genome-sequencing, the assembled genomes are fragmented, which compromises their potential application (Taniguchi et al, 2021). Taking advantage of long-read genome sequencing technology, here we reported chromosome-scale genome references of five Flaveria species, with which we conducted a systematic study of CREs and TFs during the evolution of C 4 photosynthesis.…”