A Segmental Gene Duplication Generated Differentially Expressed myb-Homologous Genes in Maize

Abstract

The myb -homologous p1 gene regulates the synthesis of flavonoid pigments in maize kernel pericarp and cob; these floral organs are greatly modified in size and shape compared with their counterparts in teosinte, the progenitor of maize. To elucidate the molecular evolution of the p1 gene in relation to its expression and possible functions in maize and teosinte, we have isolated a second maize gene ( p2 ) that is highly homologous with the p1 gene, and a related gene ( p2-t ) from Zea mays subsp parviglumis . We present evidence that the maize p1 and p2 genes were generated by duplication of an ancestral p gene ( p pre ) and its downstream sequences; the duplicated 3 Ј flanking sequences were inserted upstream of the p pre gene, thereby changing its transcription pattern. This model accounts for the structural organization and the observed differential expression of the p1 and p2 genes: p1 transcripts accumulate in kernel pericarp, cob, tassel glumes, and silk, whereas p2 transcripts are found in developing anther and silk. The duplication is estimated to have occurred 2.75 million years ago; subsequently, multiple retroelements have been inserted between the p1 and p2 genes. Our results demonstrate the evolution of a single gene into a compound locus containing two component genes with different tissue specificities. Expression of the p1 gene in the kernel pericarp may have provided a selective advantage during the evolution of maize kernel morphology. INTRODUCTIONEukaryotic genomes have been shaped to a large extent by gene duplications. Changes in ploidy are common in plants and give rise to immediate whole-genome duplications. Local gene duplications are commonly observed in genomic sequence analysis; for example, a 1.9-Mb stretch of Arabidopsis genomic sequence contains eight pairs of related genes, located adjacent to each other and in the same orientation (Bevan et al., 1998). These local sequence repeats apparently are produced by segmental duplications of discreet chromosome intervals. By whatever mechanism they occur, duplications can have a fundamentally important role in evolution. A complete gene duplication produces two identical copies, which then may undergo one of several alternative fates. Both gene copies may retain their original function, enabling the organism to produce a greater quantity of RNA or proteins. Or one of the copies may retain the original function, whereas the other copy may mutate to a functionless state (pseudogene) or acquire mutations that generate a new function (neomorph) (Li and Graur, 1991). Finally, one copy may retain the same coding sequence function but acquire new regulatory elements that specify a different pattern of expression. The latter process is best exemplified in the evolution of genes that regulate biosynthesis of flavonoid pigments in plants. In maize, anthocyanin biosynthesis is controlled by the combined function of two groups of regulatory genes: the c1/pl genes, which encode Myb-homologous transcriptional activators, and the r/b gene family, which ...

Clustered Transcription Factor Genes Regulate Nicotine Biosynthesis in Tobacco

“…Since most duplicated Arabidopsis regulatory genes show evidence of divergent expression (Duarte et al, 2006), many plant regulatory genes may experience subfunctionalization and/or neofunctionalization. A clear example is found in a P1-rr locus of maize (Zea mays), containing genes encoding two tandemly duplicated Myb-like transcriptional activators (Zhang et al, 2000). One MYB-like gene is expressed in the kernel pericarp, cob, tassel glumes, and silk and is responsible for pigmentation in these tissues, whereas the other gene functions in the developing anther and silk.…”

Nearly Identical Paralogs: Implications for Maize (Zea mays L.) Genome Evolution

“…These include the genetically unlinked ciszog1 and ciszog2 genes (Swigonova et al 2005), the tightly linked p1 and p2 genes (Zhang et al 2000), and the locally duplicated zein seed storage protein gene families that exhibit 98% identity (Song et al 2001). This study demonstrates that most NIPs are expressed and that individual members of many NIP families exhibit differential expression patterns.…”

A Segmental Deletion Series Generated by Sister-Chromatid Transposition of Ac Transposable Elements in Maize

“…Maysin accumulation is correlated with a phenotype termed silk browning, in which the cut ends of silks turn brown due to the oxidation of flavones (Byrne et al 1996;Lee et al 1998;McMullen et al 1998;Guo et al 2001;Rector et al 2003). Both p1 and p2 genes are expressed in maize silk (Zhang et al 2000), and both encode highly similar R2R3-Myb proteins with a similar potential to activate flavonoid biosynthesis in transgenic cell lines (P. . Previous studies have shown that a stock that contains both p1 and p2 genes has high maysin levels and strong silk browning.…”

“…Identification of deletions extending to the p2 gene and beyond: The p1 gene is linked with a second, highly similar gene termed p2; the p1 and p2 genes were proposed to have been generated by a segmental duplication followed by retroelement insertions to separate the two paralogs (Zhang et al 2000). If the p2 gene is located 59 of p1, then some of the SCT-generated deletions would be expected to have deletions that include p2.…”

“…The negative result in the P1-wr lane would suggest that P1-wr alleles also lack (or are polymorphic for) the sequence upstream of p1 in p1-vv. The p1-ww1112 allele contains a deletion of p1 and retains the p2 gene (Zhang et al 2000). (C) Screening for deletions of the 59-end of the p2 gene using primer pair p1-3 1 p1-4, which gives a 420-bp product from the p2 gene and a 500-bp product from the p1 gene.…”