Lyu, M.-j. A. | bioRxiv Science

bioRxiv2020

STOMAGEN-like Regulates Stomatal Generation Causing Increased Water Use Efficiency during C4 Evolution

C4 photosynthesis optimizes plants carbon and water relations, allowing high photosynthetic rate with low stomatal conductance. Stomata have long been believed as a part of C4 syndrome. However, it remains unclear how stomata traits evolved along the path from C3 to C4. Stomatal patterning was examined in Flaveria genus, a model for studying C4 evolution. Comparative, transgenic and semi-in-vitro experiments were used to study molecular basis that underlies stomatal traits along C4 evolution. Novel results: the evolution from C3 to C4 species through intermediate species is accompanied by a stepwise rather than an abrupt change in the stomatal traits. The initial change occurs near Type II and dramatic change occurs at the C4-like species. On the road to C4, stomata become less in number but bigger in size and changes in stomatal density dominates changes in maximum stomatal conductance (gsmax). The reduction of FSTOMAGEN expression underlies altered gsmax between Flaveria species with different photosynthetic pathways and likely occurs in other C4 lineages. Our study provides insight into the pattern, mechanism and role of stomatal evolution along the road towards C4. This work highlights the stomatal traits in the current C4 evolutionary model and the co-evolution of photosynthetic pathway and stomata.

plant biology↗

bioRxiv2020

Evolution of co-regulatory network of C4 metabolic genes and TFs in the genus Flaveria: go anear or away in the intermediate species?

C4 photosynthesis evolved from the ancestral C3 photosynthesis by recruiting pre-existing genes to fulfill new functions. The enzymes and transporters required for the C4 photosynthesis have been intensively studied; however, the transcription factors (TFs) regulating these C4 metabolic genes are not well understood. In particular, how the TF regulatory network of C4 metabolic genes was rewired during the evolution is unclear. Here, we constructed TFs co-regulatory networks for core C4 metabolic genes (C4GRN) for four evolutionarily closely related species from the genus Flaveria, which represent four different evolutionary stages of the C4 photosynthesis, namely, C3, type I C3-C4, type II C3-C4 and C4. Our results show that more than half of the co-regulations of TFs and C4 core metabolic genes were species specific. The counterparts of C4 genes in C3 species were already co-regulated with the photosynthesis-related genes; whereas the required TFs for the C4 photosynthesis were recruited later. The type I C3-C4 species recruited 40% of C4 required TFs which co-regulated all core C4 metabolic genes but PEPC; nevertheless, the type II C3-C4 species took on a high divergent C4GRN with C4 species itself. In C4 species, PEPC and PPDK-RP possessed much more co-regulated TFs than other C4 metabolic genes. This study provides for the first time the TFs profiles of the C4 metabolic genes in species with different photosynthetic types and reveal the dynamic of C4 genes-TFs co-regulations along the evolutionary process, providing thereby new insights into the evolution of C4 photosynthesis.

evolutionary biology↗