Structure and evolution of the r/b chromosomal regions in rice, maize and sorghum

Abstract

The r1 and b1 genes of maize, each derived from the chromosomes of two progenitors that hybridized >4.8 million years ago (MYA), have been a rich source for studying transposition, recombination, genomic imprinting, and paramutation. To provide a phylogenetic context to the genetic studies, we sequenced orthologous regions from maize and sorghum (>600 kb) surrounding these genes and compared them with the rice genome. This comparison showed that the homologous regions underwent complete or partial gene deletions, selective retention of orthologous genes, and insertion of nonorthologous genes. Phylogenetic analyses of the r/b genes revealed that the ancestral gene was amplified independently in different grass lineages, that rice experienced an intragenomic gene movement and parallel duplication, that the maize r1 and b1 genes are descendants of two divergent progenitors, and that the two paralogous r genes of sorghum are almost as old as the sorghum lineage. Such sequence mobility also extends to linked genes. The cisZOG genes are characterized by gene amplification in an ancestral grass, parallel duplications and deletions in different grass lineages, and movement to a nonorthologous position in maize. In addition to gene mobility, both maize and rice regions experienced recent transposition (<3 MYA).

Figure 1.—

Graphical representation of microcollinearity at the r/b loci of rice, sorghum, and maize. Genes and putative genes are numbered by the order of their appearance from the 5′ to 3′ end of a contig (as listed in Table 2). Copies of an amplified gene are marked by the gene number and a letter in alphabetical order corresponding to their appearance on a contig. Red arrows refer to genes (arrows depicting proposed directions of transcription), light blue arrows refer to DNA transposons, dark rectangles show LTR-retrotransposons (hatching shows nested LTR-retrotransposons), and gray arrows refer to polyproteins. The dashed line indicates the partially sequenced Z566K20 BAC. Lines connecting the contigs show conserved genes. Small triangles show the positions of miniature inverted repeat transposable elements. P, partial; F, full-length LTR-retrotransposon.

Figure 2.—

Phylogenetic relationships among the r/b gene homologs. (A) Phylogram resulting from ML analysis with a GTR + I + G model of full-length r and b sequences (2016 nt). Numbers at the internodes refer to the bootstrap proportions from MP (amino acids), MP (nucleotides), ML (nucleotides), and Bayesian-posterior probabilities, respectively. (B) Cladogram resulting from MP analysis of partial sequences (434 nt); numbers show bootstrap values. (C) Proposed history of r/b gene duplication in grasses. The three diagrams located near terminal branches of Oryza, Pennisetum, and Sorghum show the duplication pattern of r/b gene in the corresponding lineage. The wavy line in the Oryza diagram depicts the transfer of one of the r/b homologs to the rice chromosome 1 (the so-called Rb locus). X in the Zea lineage represents the tetraploidization event.

Figure 3.—

Phylogenetic relationship of cis-zeatin O-glucosyltransferase genes and a proposed history of their amplification and removal. (A) An unrooted phylogram of cisZOG homologs from orthologous regions of rice, sorghum, and maize resulting from ML(GTR + G) analysis. Numbers at the internodes show bootstrap values from MP (amino acids), MP (nucleotides), and ML (nucleotides) analyses, respectively. The hexagon on the terminal branch of cisZOG-S5 depicts the position of the root of the gene tree (see text). (B) Schema of a proposed pattern of cisZOG gene duplication and deletion in rice, sorghum, and maize. Squares refer to genes. The dashed line between cisZOG-Z1 and cisZOG-Z2 illustrates that the two copies are not within the single orthologous region of maize.