Comparative transcriptomics of three Poaceae species reveals patterns of gene expression evolution

Abstract

SUMMARYThe Poaceae family, also known as the grasses, includes agronomically important cereal crops such as rice, maize, sorghum, and wheat. Previous comparative studies have shown that much of the gene content is shared among the grasses; however, functional conservation of orthologous genes has yet to be explored. To gain an understanding of the genome-wide patterns of evolution of gene expression across reproductive tissues, we employed a sequence-based approach to compare analogous transcriptomes in species representing three Poaceae subgroups including the Pooideae (Brachypodium distachyon), the Panicoideae (sorghum), and the Ehrhartoideae (rice). Our transcriptome analyses reveal that only a fraction of orthologous genes exhibit conserved expression patterns. A high proportion of conserved orthologs include genes that are upregulated in physiologically similar tissues such as leaves, anther, pistil, and embryo, while orthologs that are highly expressed in seeds show the most diverged expression patterns. More generally, we show that evolution of gene expression profiles and coding sequences in the grasses may be linked. Genes that are highly and broadly expressed tend to be conserved at the coding sequence level while genes with narrow expression patterns show accelerated rates of sequence evolution. We further show that orthologs in syntenic genomic blocks are more likely to share correlated expression patterns compared with non-syntenic orthologs. These findings are important for agricultural improvement because sequence information is transferred from model species, such as Brachypodium, rice, and sorghum to crop plants without sequenced genomes.

Differentially Regulated Orthologs in Sorghum and the Subgenomes of Maize

“…This observation is consistent with previous reports about the analysis of expression across reproductive tissues in three grass species (Davidson et al, 2012). However, it should be noted that these correlations were significantly lower than those observed between biological replicates (see Methods for a detailed explanation of what constituted a biological replicate in this study) of the same species (Spearman's rho = 0.88-0.98, Pearson r = 0.89-0.99, Kendall rank correlation 0.78-0.91), and many individual genes have large divergence in baseline (A) The overlap between syntenic orthologous gene pairs conserved between maize1/sorghum and maize2/sorghum.…”

“…However, this approach is limited to identifying changes in baselines expression in the same treatment rather than examining patterns of regulation across multiple treatments. Within the grasses, several research groups have employed clustering-based methods to identify genes with conserved patterns of regulation during either reproductive or photosynthetic development (Davidson et al, 2012;Wang et al, 2014). Among other results, one of these studies concluded that orthologous genes conserved at syntenic locations are more likely to share correlated expression patterns across multiple species than genes classified as orthologs based on phylogenetic analysis but located at nonsyntenic locations (Davidson et al, 2012).…”

“…Within the grasses, several research groups have employed clustering-based methods to identify genes with conserved patterns of regulation during either reproductive or photosynthetic development (Davidson et al, 2012;Wang et al, 2014). Among other results, one of these studies concluded that orthologous genes conserved at syntenic locations are more likely to share correlated expression patterns across multiple species than genes classified as orthologs based on phylogenetic analysis but located at nonsyntenic locations (Davidson et al, 2012). Clustering-based methods can identify genes with conserved patterns of regulation across multiple species, but they have high false positive rates when used to identify genes with changes in regulatory pattern.…”

nana plant2 Encodes a Maize Ortholog of the Arabidopsis Brassinosteroid Biosynthesis Gene DWARF1, Identifying Developmental Interactions between Brassinosteroids and Gibberellins

“…FPKM values and histograms were obtained from qteller.com for selected maize and sorghum (Sorghum bicolor) genes (Wang et al, 2009;Li et al, 2010;Davidson et al, 2011Davidson et al, , 2012Dugas et al, 2011;Schnable and Freeling, 2011;Waters et al, 2011;Bolduc et al, 2012;Chang et al, 2012;Kakumanu et al, 2012;Mizuno et al, 2012). Recreation of these histograms could be obtained at http://www.qteller.com.…”

Gene duplication, silencing and expression alteration govern the molecular evolution of PRC2 genes in plants

“…Expression data analyses Previously, Davidson et al (2012) performed a transcriptome analysis of reproductive and vegetative tissue of three Gramineae species, Brachypodium distachyon, O. sativa and Sorghum bicolor, using the RNA-sequencing method. These gene expression data were used in the present study.…”