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Lyu, M.-J. A.

Publications and source records attributed to Lyu, M.-J. A..

5 recordsLinked to original sources

Comparative spatiotemporal single cell transcriptomes reveal rewiring of pre-existing regulations during emergence of Kranz anatomy in C4 grasses

Many of the worlds most productive food and bioenergy crops use C4 photosynthesis, which have high photosynthetic efficiency due to a Kranz anatomy-based CO2 concentrating mechanism. Here, we took a comparative transcriptomics approach using single cell spatial transcriptomes of leaf primordia for maize (Zea mays) and single cell RNA-seq (scRNA-seq) atlases of corresponding leaf tissues for three C4 species (Zea mays, Sorghum bicolor, Setaria viridis) and one C3 rice (Oryza sativa) to study regulatory networks involved in the development and evolution of Kranz anatomy. We show that the formation of Kranz anatomy involves extensive recruitment and modification of pre-existing regulatory modules, especially the SHR-SCR module and the auxin signaling pathway. Members of the INDETERMINATE DOMAIN (IDD) family transcription factors, including IDD7 and IDDP1, contribute to the modification of the involved modules. These extensive recruitment and modification of existing genetic regulatory programs underlie the repeated emergence of C4 photosynthesis during evolution.

plant biology↗

Regulatory preconditioning for the evolution of C4 photosynthesis revealed by low CO2 treatment of Arabidopsis thaliana

Low CO2 condition was considered a preconditioning or selection pressure for C4 evolution. However, it remains elucidated how low CO2 condition contribute to the evolutionary assembly of the C4 pathway. We conducted a systematic transcriptomics and metabolomics analysis under short-term low CO2 condition and found that Arabidopsis grown under this condition showed increased expression of most genes encoding C4- related enzymes and transporters. Low CO2 condition increased NH4+ content in leaves; as expected, photorespiratory and ammonia refixing pathways were enhanced. Furthermore, we found that compared to low CO2 condition, in vitro treatment with NH4+ induced a similar pattern of changes in C4 related genes and genes involved in ammonia refixation. This supports that increased expression of C4 genes induced by low CO2 condition can supply carbon skeleton for ammonia recycling. This study provides new insight into the regulatory preconditioning which may have facilitated the evolution of C4 photosynthesis under low atmospheric CO2 environments.

evolutionary biology↗

Increased α-ketoglutarate as a missing link from the C3-C4 intermediate state to C4 photosynthesis in the genus Flaveria

As a complex trait, C4 photosynthesis has multiple independent origins in evolution. Phylogenetic evidence and theoretical analysis suggest that C2 photosynthesis, which is driven by glycine decarboxylation in the bundle sheath cell, may function as a bridge from C3 towards C4 photosynthesis. However, the exact molecular mechanism underlying the transition between C2 photosynthesis towards C4 photosynthesis remains elusive. Here, we provide multiple evidence suggesting a role of higher -ketoglutarate (AKG) concentration during this transition. Metabolomic data of 12 Flaveria species, including multiple photosynthetic types, show that AKG concentration initially increases in the C3-C4 intermediate with a further increase in C4 species. Petiole feeding of AKG increased the concentrations of C4 related metabolites in C3-C4 and C4 species but not the activity of C4 related enzymes. Sequence analysis shows that glutamate synthase (Fd-GOGAT), which catalyzes the generation of glutamate using AKG, was under strong positive selection during the evolution of C4 photosynthesis. Simulations with a constraint-based model for C3-C4 intermediate further show that decreasing the activity of Fd-GOGAT facilitates the transition from a C2-dominant to a C4-dominant CO2 concentrating mechanisms. All these provide an insight into the mechanistic switch from C3-C4 intermediate to C4 photosynthesis.

plant biology↗

Evolutionary changes of phosphoenolpyruvate transporter (PPT) during the emergence of C4 photosynthesis

C4 photosynthesis is a complex trait, which evolved from its ancestral C3 photosynthesis by recruiting pre-existing genes. The evolutionary history of enzymes involved in the C4 shuttle has been extensively studied. Here we analyze the evolutionary changes of phosphoenolpyruvate (PEP) transporter (PPT) during its recruitment from C3 to C4 photosynthesis. Our analysis shows that 1) among the two PPT paralogs, i.e. PPT1 and PPT2, PPT1 is an ancestral copy while PPT2 is a derived copy; 2) during C4 evolution, PPT1 shifted its expression from predominantly in root to in leaf, and from bundle sheath cell to mesophyll cell, supporting that PPT1 was recruited into C4 photosynthesis; 3) PPT1 gained increased transcript abundance, gained more rapid and long-lasting responses to light during C3 to C4 evolution, while PPT2 lost its responsiveness to light; 4) PPT1 gained a number of new cis-elements during C4 evolution; 5) C4 PPT1 can complement the phenotype of Arabidopsis PPT1 loss-of-function mutant, suggesting that it is a bidirectional transporter and its transport direction did not alter during C4 evolution. We finally discuss mechanistic linkages between these observed changes in PPT1 and C4 photosynthesis evolution.\n\nHigh lightDuring the process of C4 photosynthesis evolution, PPT not only experienced changes in its expression location and transcript abundance, but also acquired new cis-elements in its promoter region and accumulated protein variations.

evolutionary biology↗

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

BackgroundC4 photosynthesis is a remarkable complex trait, elucidations of the evolutionary trajectory of C4 photosynthesis from its ancestral C3 pathway can help us to better understand the generic principles of complex trait evolution and guide engineering of C3 crops for higher yields. 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.\n\nResultsWe mapped transcript abundance, protein sequence, and morphological features to the phylogenetic tree of the genus Flaveria, and calculated the evolutionary correlation of different features. Besides, we predicted the relative changes of ancestral nodes of those features to illustrate the key stages during the evolution of C4 photosynthesis. 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.\n\nConclusionsOur data shows highly coordinated changes in gene expression, protein sequence and morphological features. Besides, our results support an obviously evolutionary jump during the evolution of C4 metabolism.

evolutionary biology↗