Tripsacum de novotranscriptome assemblies reveal parallel gene evolution with maize after ancient polyploidy

Abstract

Core Ideas Maize genes with protein evidence have higher expression and GC content Tripsacum homologs of maize genes exhibit the same trends as in maize Maize proteome genes have more highly correlated gene expression with Tripsacum Expression dominance for homeologs occurs similarly between maize and Tripsacum homologs A similar set of genes may be decaying into pseudogenes in maize and Tripsacum Plant genomes reduce in size following a whole‐genome duplication event, and one gene in a duplicate gene pair can lose function in absence of selective pressure to maintain duplicate gene copies. Maize (Zea mays L.) and its sister genus, Tripsacum, share a genome duplication event that occurred 5 to 26 million years ago. Because few genomic resources for Tripsacum exist, it is unknown whether Tripsacum grasses and maize have maintained a similar set of genes that have resisted decay into pseudogenes. Here we present high‐quality de novo transcriptome assemblies for two species: Tripsacum dactyloides (L.) L. and T. floridanum Porter ex Vasey. Genes with experimental protein evidence in maize were good candidates for genes resistant to pseudogenization in both genera because pseudogenes by definition do not produce protein. We tested whether 15,160 maize genes with protein evidence are resisting gene loss and whether their Tripsacum homologs are also resisting gene loss. Protein‐encoding maize transcripts and their Tripsacum homologs have higher guanine–cytosine (GC) content, higher gene expression levels, and more conserved expression levels than putatively untranslated maize transcripts and their Tripsacum homologs. These results suggest that similar genes may be decaying into pseudogenes in both genera after a shared ancient polyploidy event. The Tripsacum transcriptome assemblies provide a high‐quality genomic resource that can provide insight into the evolution of maize, a highly valuable crop worldwide.

Parallels between natural selection in the cold‐adapted crop‐wild relative Tripsacum dactyloides and artificial selection in temperate adapted maize

“…A total of 1259 high quality consensus sequences from T. dactyloides failed to map to maize reference genome, which was generated from the maize inbred B73. This number is roughly consistent with another report of 1737 T. dactyloides transcripts that lack orthologs in the maize genome (Gault et al ., ). Sequences that lacked apparent homologs in the maize reference genome were aligned to NCBI's RefSeq plant database.…”

“…While widely grown in temperate regions over the summer, maize remains sensitive to cold. Maize varieties with the ability to be planted significantly earlier, or in the extreme case to overwinter, have the potential to intercept a greater proportion of total annual solar radiation increasing maximum potential yields (Dohleman and Long, ; Gault et al ., ). It must be acknowledged that there are many other differences in niches, environments, and selective pressures experienced by T. dactyloides and the environments and selective pressures experienced by maize and its wild progenitors.…”

“…Despite their close genetic relationship, some species of the genus Tripsacum are adapted to a much wider range of climates than wild members of the genus Zea (Figure ), particularly T. dactyloides , which is native to much of the current range of domesticated maize cultivation in the western hemisphere (Doebley, ; Forster and Kole, ). T. dactyloides therefore represents a potential source of insight into genetic changes responsible for adaptation to abiotic and biotic stressors found in different parts of that range for traits such as disease and insect resistance, drought and frost tolerance, many of which are targets for maize improvement (Chia et al ., ; Wang et al ., 2013a; Gault et al ., ).…”

“…As part of Hapmap2, 8× short read shotgun data were generated from T. dactyloides (Chia et al ., ). Additional low pass genomic data have been generated for several other species in the Tripsacum genus (Zhu et al ., ), and recently, Illumina transcriptome assemblies of two species in the genus Tripsacum – T. dactyloides and T. floridanum became available (Gault et al ., ). Here we employ PacBio long‐read sequencing to generate a set of full‐length transcript sequences from T. dactyloides .…”

A subfunctionalization epistasis model to evaluate homeologous gene interactions in allopolyploid wheat

“…Whole genome duplication can generate the raw materials for the maintenance of genetic diversity (Wendel, 2000; Adams and Wendel, 2005). Gault et al (2018) demonstrated that similar sets of duplicated genes were preserved in two related genera, Zea and Tripsacum , millions of years after a shared paleopolyploidization event. This conserved pattern in purifying selection suggests that, at least for some genes, there is a clear advantage to maintaining two copies.…”