The evolution of TF-regulatory network of core C4 metabolic pathway genes in the genus of Flaveria [ABA]
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ABSTRACT: C4 photosynthesis was evolved from ancestral C3 photosynthesis by recruited pre-existed genes to perform new functions. Enzymes and transporters required for C4 metabolic pathway has been well documented, however, transcriptional factors (TFs) that regulate those C4 metabolic genes is poorly understood, in particular, how the TF regulatory network of C4 metabolic genes was re-wired, and the involved metabolic functions of those TFs along the evolution of C4 photosynthesis remained unknown. Here, by using RNA-Seq data from growth condition that reported to have effect on C4 photosynthesis, we constructed the TF regulatory network for four evolutionarily closely related species in the genus Flaveria, which represent different stages of the evolution of C4 photosynthesis, namely, C3, type I C3-C4, type II C3-C4 and C4. Our results show that four TFs are conserved along the evolution whose function either relate to stress response or light response. TFs regulating C4 core genes in C3 species involved in functions belong to RNA regulation and nitrogen metabolism, and that in both intermediate species and C4 species involved in photosynthesis and light responsiveness. Moreover, the TF-network of C4 core metabolic genes has the highest network density in type I C3-C4 species and C4 species when consider the fragment of TF-regulatory network that up-regulated under low CO2, suggesting that TFs regulating C4 genes were recruited to photosynthesis at type I C3-C4 both in involved functions and network density. Our results provide a valuable resource for studying molecular regulatory mechanisms underlying C4 metabolic process.
Project description:C4 photosynthesis was evolved from ancestral C3 photosynthesis by recruited pre-existed genes to perform new functions. Enzymes and transporters required for C4 metabolic pathway has been well documented, however, transcriptional factors (TFs) that regulate those C4 metabolic genes is poorly understood, in particular, how the TF regulatory network of C4 metabolic genes was re-wired, and the involved metabolic functions of those TFs along the evolution of C4 photosynthesis remained unknown. Here, by using RNA-Seq data from growth condition that reported to have effect on C4 photosynthesis, we constructed the TF regulatory network for four evolutionarily closely related species in the genus Flaveria, which represent different stages of the evolution of C4 photosynthesis, namely, C3, type I C3-C4, type II C3-C4 and C4. Our results show that four TFs are conserved along the evolution whose function either relate to stress response or light response. TFs regulating C4 core genes in C3 species involved in functions belong to RNA regulation and nitrogen metabolism, and that in both intermediate species and C4 species involved in photosynthesis and light responsiveness. Moreover, the TF-network of C4 core metabolic genes has the highest network density in type I C3-C4 species and C4 species when consider the fragment of TF-regulatory network that up-regulated under low CO2, suggesting that TFs regulating C4 genes were recruited to photosynthesis at type I C3-C4 both in involved functions and network density. Our results provide a valuable resource for studying molecular regulatory mechanisms underlying C4 metabolic process.
Project description:C4 photosynthesis was evolved from ancestral C3 photosynthesis by recruited pre-existed genes to perform new functions. Enzymes and transporters required for C4 metabolic pathway has been well documented, however, transcriptional factors (TFs) that regulate those C4 metabolic genes is poorly understood, in particular, how the TF regulatory network of C4 metabolic genes was re-wired, and the involved metabolic functions of those TFs along the evolution of C4 photosynthesis remained unknown. Here, by using RNA-Seq data from growth condition that reported to have effect on C4 photosynthesis, we constructed the TF regulatory network for four evolutionarily closely related species in the genus Flaveria, which represent different stages of the evolution of C4 photosynthesis, namely, C3, type I C3-C4, type II C3-C4 and C4. Our results show that four TFs are conserved along the evolution whose function either relate to stress response or light response. TFs regulating C4 core genes in C3 species involved in functions belong to RNA regulation and nitrogen metabolism, and that in both intermediate species and C4 species involved in photosynthesis and light responsiveness. Moreover, the TF-network of C4 core metabolic genes has the highest network density in type I C3-C4 species and C4 species when consider the fragment of TF-regulatory network that up-regulated under low CO2, suggesting that TFs regulating C4 genes were recruited to photosynthesis at type I C3-C4 both in involved functions and network density. Our results provide a valuable resource for studying molecular regulatory mechanisms underlying C4 metabolic process.
Project description:C4 photosynthesis was evolved from ancestral C3 photosynthesis by recruited pre-existed genes to perform new functions. Enzymes and transporters required for C4 metabolic pathway has been well documented, however, transcriptional factors (TFs) that regulate those C4 metabolic genes is poorly understood, in particular, how the TF regulatory network of C4 metabolic genes was re-wired, and the involved metabolic functions of those TFs along the evolution of C4 photosynthesis remained unknown. Here, by using RNA-Seq data from growth condition that reported to have effect on C4 photosynthesis, we constructed the TF regulatory network for four evolutionarily closely related species in the genus Flaveria, which represent different stages of the evolution of C4 photosynthesis, namely, C3, type I C3-C4, type II C3-C4 and C4. Our results show that four TFs are conserved along the evolution whose function either relate to stress response or light response. TFs regulating C4 core genes in C3 species involved in functions belong to RNA regulation and nitrogen metabolism, and that in both intermediate species and C4 species involved in photosynthesis and light responsiveness. Moreover, the TF-network of C4 core metabolic genes has the highest network density in type I C3-C4 species and C4 species when consider the fragment of TF-regulatory network that up-regulated under low CO2, suggesting that TFs regulating C4 genes were recruited to photosynthesis at type I C3-C4 both in involved functions and network density. Our results provide a valuable resource for studying molecular regulatory mechanisms underlying C4 metabolic process.
Project description:C4 photosynthesis was evolved from ancestral C3 photosynthesis by recruited pre-existed genes to perform new functions. Enzymes and transporters required for C4 metabolic pathway has been well documented, however, transcriptional factors (TFs) that regulate those C4 metabolic genes is poorly understood, in particular, how the TF regulatory network of C4 metabolic genes was re-wired, and the involved metabolic functions of those TFs along the evolution of C4 photosynthesis remained unknown. Here, by using RNA-Seq data from growth condition that reported to have effect on C4 photosynthesis, we constructed the TF regulatory network for four evolutionarily closely related species in the genus Flaveria, which represent different stages of the evolution of C4 photosynthesis, namely, C3, type I C3-C4, type II C3-C4 and C4. Our results show that four TFs are conserved along the evolution whose function either relate to stress response or light response. TFs regulating C4 core genes in C3 species involved in functions belong to RNA regulation and nitrogen metabolism, and that in both intermediate species and C4 species involved in photosynthesis and light responsiveness. Moreover, the TF-network of C4 core metabolic genes has the highest network density in type I C3-C4 species and C4 species when consider the fragment of TF-regulatory network that up-regulated under low CO2, suggesting that TFs regulating C4 genes were recruited to photosynthesis at type I C3-C4 both in involved functions and network density. Our results provide a valuable resource for studying molecular regulatory mechanisms underlying C4 metabolic process.
Project description:C4 photosynthesis overpasses C3 by a higher photosynthetic rate, along with a higher water and nitrogen use efficiency. The establishment of C4 photosynthesis requires modification of ancestral C3 in both anatomical and metabolic aspects, both are involved in many functional pathways which have not been fully demonstrated. This study aims to illustrate overall functional changes along the evolution of C4 photosynthesis, with a purpose to gain an overall view of what are required for C4 photosynthesis. To achieve this, this study assembled chromosome scale of genome sequencing of five Flaveria species, representing gradual evolutionary stages of C4 photosynthesis from C3 to C3-C4 and to C4. Here, result showed that the genome size gradually increases from C3 to intermediate to C4 species, which ranges from 0.5 G to 1.87 G. The enlarged genomes are mainly from transposable elements, with the number of protein coding gene are comparable along evolution. The copy of C4 version CA1 and PEPC1, as well as PEPC-k gained extra one, two and five copies in C4 species F. trinervia as a result of tandem duplication, which plays a positive role for the emergency of C4 photosynthesis. Besides, the evolutionary pattern of C4 gene on transcript abundance are consistent with that on protein abundance, suggesting transcriptional regulation is a key factor for establishing C4 photosynthesis.
Project description:In multicellular systems changes to the patterning of gene expression drive modifications in cell function and trait evolution. One striking example is found in more than sixty plant lineages where compartmentation of photosynthesis between cell types allowed evolution of the efficient C4 pathway from the ancestral C3 state. The molecular events enabling this transition are unclear. We used single nuclei sequencing to generate a cell level expression atlas for C3 rice and C4 sorghum during photomorphogenesis. In both species a conserved cistrome was identified for each cell type and initiation of photosynthesis gene expression was conditioned by cell identity. Photosynthesis genes switching expression from mesophyll in rice to bundle sheath in sorghum acquire hallmarks of bundle sheath identity. The sorghum bundle sheath has also acquired gene networks associated with C3 guard cells. We conclude C4 photosynthesis is based on rewiring in cis that exapts cell identity networks of C3 plants.
Project description:Photosynthesis supports life on Earth but the regulatory architecture associated with photosynthesis gene expression is poorly understood. Most crops use either C3 or C4 photosynthesis with the latter allowing significantly higher efficiencies as well as improved water and nitrogen use. Here we use DNAse-SEQ to define >1 million transcription factor binding sites in leaves of grasses that either operate C3 or C4 photosynthesis and that are consistent with significant differences in the modes of gene regulation between the kingdoms of life. Leaf samples were collected from seedlings to allow for comparison of regulatory interactions between species from the same (Zea mays and Sorghum bicolor) and different (Setaria italica) C4 lineages, as well as a C3 grass (Brachypodium distachyon) in order to investigate evolution of C4 photosynthetic gene expression. Additionally bundle sheath tissues were mechanically isolated from C4 species and analysed by DNAse-SEQ to identify DNA regulatory elements controlling cell-specific gene expression patterns.
Project description:Maize and rice are the two most economically important grass crops and utilize distinct forms of photosynthesis to fix carbon: C4 and C3 respectively. Relative to C3 photosynthesis, C4 photosynthesis reduces photorespiration and affords higher water and nitrogen use efficiencies under hot arid conditions. To define key innovations in C4 photosynthesis, we profiled metabolites and gene expression along a developing leaf gradient. A novel statistical method was implemented to compare transcriptomes from these two species along a unified leaf developmental gradient and define candidate cis-regulatory elements and transcription factors driving photosynthetic gene expression. We also present comparative primary and secondary metabolic profiles along the gradients that provide new insight into nitrogen and carbon metabolism in C3 and C4 grasses. These resources, including community viewers to access and mine these datasets, will enable the elucidation and engineering of C4 photosynthetic networks to improve the photosynthetic capacity of C3 and C4 grasses.
Project description:Transcriptome profiling in response to water stress and rewatering of Moricandia species with C3 and C3-C4 intermediate photosynthesis.