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IsoSeq transcriptome assembly of C3 panicoid grasses provides tools to study evolutionary change in the Panicoideae.

ABSTRACT: The number of plant species with genomic and transcriptomic data has been increasing rapidly. The grasses-Poaceae-have been well represented among species with published reference genomes. However, as a result the genomes of wild grasses are less frequently targeted by sequencing efforts. Sequence data from wild relatives of crop species in the grasses can aid the study of domestication, gene discovery for breeding and crop improvement, and improve our understanding of the evolution of C4 photosynthesis. Here, we used long-read sequencing technology to characterize the transcriptomes of three C3 panicoid grass species: Dichanthelium oligosanthes, Chasmanthium laxum, and Hymenachne amplexicaulis. Based on alignments to the sorghum genome, we estimate that assembled consensus transcripts from each species capture between 54.2% and 65.7% of the conserved syntenic gene space in grasses. Genes co-opted into C4 were also well represented in this dataset, despite concerns that because these genes might play roles unrelated to photosynthesis in the target species, they would be expressed at low levels and missed by transcript-based sequencing. A combined analysis using syntenic orthologous genes from grasses with published reference genomes and consensus long-read sequences from these wild species was consistent with previously published phylogenies. It is hoped that these data, targeting underrepresented classes of species within the PACMAD grasses-wild species and species utilizing C3 photosynthesis-will aid in future studies of domestication and C4 evolution by decreasing the evolutionary distance between C4 and C3 species within this clade, enabling more accurate comparisons associated with evolution of the C4 pathway.

SUBMITTER: Carvalho DS

PROVIDER: S-EPMC7047018 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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IsoSeq transcriptome assembly of C<sub>3</sub> panicoid grasses provides tools to study evolutionary change in the Panicoideae.

Carvalho Daniel S DS Nishimwe Aime V AV Schnable James C JC

Plant direct 20200228 2

The number of plant species with genomic and transcriptomic data has been increasing rapidly. The grasses-Poaceae-have been well represented among species with published reference genomes. However, as a result the genomes of wild grasses are less frequently targeted by sequencing efforts. Sequence data from wild relatives of crop species in the grasses can aid the study of domestication, gene discovery for breeding and crop improvement, and improve our understanding of the evolution of C<sub>4</ ...[more]

PMID: 32128472

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Project description:BACKGROUND AND AIMS: The success of C4 plants lies in their ability to attain greater efficiencies of light, water and nitrogen use under high temperature, providing an advantage in arid, hot environments. However, C4 grasses are not necessarily less sensitive to drought than C3 grasses and are proposed to respond with greater metabolic limitations, while the C3 response is predominantly stomatal. The aims of this study were to compare the drought and recovery responses of co-occurring C3 and C4 NADP-ME grasses from the subfamily Panicoideae and to determine stomatal and metabolic contributions to the observed response. METHODS: Six species of locally co-occurring grasses, C3) species Alloteropsis semialata subsp. eckloniana, Panicum aequinerve and Panicum ecklonii, and C4 (NADP-ME) species Heteropogon contortus, Themeda triandra and Tristachya leucothrix, were established in pots then subjected to a controlled drought followed by re-watering. Water potentials, leaf gas exchange and the response of photosynthetic rate to internal CO2 concentrations were determined on selected occasions during the drought and re-watering treatments and compared between species and photosynthetic types. KEY RESULTS: Leaves of C4 species of grasses maintained their photosynthetic advantage until water deficits became severe, but lost their water-use advantage even under conditions of mild drought. Declining C4 photosynthesis with water deficit was mainly a consequence of metabolic limitations to CO2 assimilation, whereas, in the C3 species, stomatal limitations had a prevailing role in the drought-induced decrease in photosynthesis. The drought-sensitive metabolism of the C4 plants could explain the observed slower recovery of photosynthesis on re-watering, in comparison with C3 plants which recovered a greater proportion of photosynthesis through increased stomatal conductance. CONCLUSIONS: Within the Panicoid grasses, C4 (NADP-ME) species are metabolically more sensitive to drought than C3 species and recover more slowly from drought.

Project description:BackgroundThe circadian clock drives endogenous 24-h rhythms that allow organisms to adapt and prepare for predictable and repeated changes in their environment throughout the day-night (diurnal) cycle. Many components of the circadian clock in Arabidopsis thaliana have been functionally characterized, but comparatively little is known about circadian clocks in grass species including major crops like maize and sorghum.ResultsComparative research based on protein homology and diurnal gene expression patterns suggests the function of some predicted clock components in grasses is conserved with their Arabidopsis counterparts, while others have diverged in function. Our analysis of diurnal gene expression in three panicoid grasses sorghum, maize, and foxtail millet revealed conserved and divergent evolution of expression for core circadian clock genes and for the overall transcriptome. We find that several classes of core circadian clock genes in these grasses differ in copy number compared to Arabidopsis, but mostly exhibit conservation of both protein sequence and diurnal expression pattern with the notable exception of maize paralogous genes. We predict conserved cis-regulatory motifs shared between maize, sorghum, and foxtail millet through identification of diurnal co-expression clusters for a subset of 27,196 orthologous syntenic genes. In this analysis, a Cochran-Mantel-Haenszel based method to control for background variation identified significant enrichment for both expected and novel 6-8 nucleotide motifs in the promoter regions of genes with shared diurnal regulation predicted to function in common physiological activities.ConclusionsThis study illustrates the divergence and conservation of circadian clocks and diurnal regulatory networks across syntenic orthologous genes in panacoid grass species. Further, conserved local regulatory sequences contribute to the architecture of these diurnal regulatory networks that produce conserved patterns of diurnal gene expression.

Project description:C4 photosynthesis is a carbon-concentrating mechanism that evolved independently more than 60 times in a wide range of angiosperm lineages. Among other alterations, the evolution of C4 from ancestral C3 photosynthesis requires changes in the expression of a vast number of genes. Differential gene expression analyses between closely related C3 and C4 species have significantly increased our understanding of C4 functioning and evolution. In Chenopodiaceae, a family that is rich in C4 origins and photosynthetic types, the anatomy, physiology and phylogeny of C4, C2, and C3 species of Salsoleae has been studied in great detail, which facilitated the choice of six samples of five representative species with different photosynthetic types for transcriptome comparisons. mRNA from assimilating organs of each species was sequenced in triplicates, and sequence reads were de novo assembled. These novel genetic resources were then analyzed to provide a better understanding of differential gene expression between C3, C2 and C4 species. All three analyzed C4 species belong to the NADP-ME type as most genes encoding core enzymes of this C4 cycle are highly expressed. The abundance of photorespiratory transcripts is decreased compared to the C3 and C2 species. Like in other C4 lineages of Caryophyllales, our results suggest that PEPC1 is the C4-specific isoform in Salsoleae. Two recently identified transporters from the PHT4 protein family may not only be related to the C4 syndrome, but also active in C2 photosynthesis in Salsoleae. In the two populations of the C2 species S. divaricata transcript abundance of several C4 genes are slightly increased, however, a C4 cycle is not detectable in the carbon isotope values. Most of the core enzymes of photorespiration are highly increased in the C2 species compared to both C3 and C4 species, confirming a successful establishment of the C2 photosynthetic pathway. Furthermore, a function of PEP-CK in C2 photosynthesis appears likely, since PEP-CK gene expression is not only increased in S. divaricata but also in C2 species of other groups.

Dataset Information

IsoSeq transcriptome assembly of C3 panicoid grasses provides tools to study evolutionary change in the Panicoideae.

Publications

IsoSeq transcriptome assembly of C<sub>3</sub> panicoid grasses provides tools to study evolutionary change in the Panicoideae.

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