Ordered origin of the typical two- and three-repeat Myb genes
Introduction
The Myb gene super-family comprises a group of related genes found in plant, animal, and fungal genomes. The archetype is the v-myb oncogene from Avian Myeloblastosis Virus (Klempnauer et al., 1982). Subsequently, members of the Myb gene family were identified in diverse plants and animals (Rosinski and Atchley, 1998). Myb genes encode proteins with DNA-binding domains composed of one, two or three semi-conserved motifs of approximately 50 amino acids each. Each motif is capable of forming 3 α-helices; the 3rd α-helix is thought to play a recognition role in binding to a short DNA sequence (Rabinowicz et al., 1999). Many Myb proteins contain two or three tandem repeats of the motif (referred to as R1, R2, and R3 repeat, respectively) within a single protein (Lipsick, 1996). A 4-repeat Myb gene was reported in Arabidopsis (Stracke et al., 2001).
Vertebrate genomes are reported to contain relatively few Myb genes (Rosinski and Atchley, 1998); these are classified on a functional basis into three general forms, A-Myb, B-Myb and C-Myb (Lipsick, 1996). In contrast to animals, flowering plants contain large numbers of Myb genes. For example, 125 R2R3 Myb genes have been identified in Arabidopsis (Stracke et al., 2001). Surveys based on expressed sequences have detected more than 80 Myb genes in maize (Rabinowicz et al., 1999), approximately 30 in Petunia hybrida (Avila et al., 1993), and approximately 200 Myb genes in cotton (Cedroni et al., 2003). Moreover, plant Myb genes are structurally and functionally very diverse. The functions of most plant Myb genes are unknown, although analysis of some well-studied examples indicates three well-defined roles for plant Myb transcription factors to date: (1) controlling secondary metabolism, particularly in flavonoid biosynthesis (Grotewold et al., 1994); (2) regulating cellular morphogenesis (Oppenheimer et al., 1991); (3) mediating signal transduction pathways, such as in response to abiotic stress (Urao et al., 1993) and pathogen attack (Yang and Klessig, 1996). In addition, some plant Myb proteins may serve structural roles as in the case of RTBP1, a Myb-domain protein implicated in plant telomere function (Yu et al., 2000).
It should be noted that a group of Myb proteins containing only one or a partial Myb repeat was found in Drosophila (England et al., 1992) and in plants (Baranowskij et al., 1994). Additionally, some Myb proteins with two or three repeats in fungi and plants lack the typical constantly spaced Trp residues. These proteins with atypical Trp spacing or partial Myb domains are non-typical Myb proteins.
In this article, we focus on the typical R2R3 and R1R2R3 Myb proteins, which have sufficient sequence divergence to investigate molecular evolution of the Myb gene family. Recently, Dias et al. (2003) provided evidence for expansion of the maize R2R3 Myb gene family through genome duplication, tandem gene duplication, and a more ancient duplication. Additionally, Myb homologous genes in cotton appear to evolve independently in the allopolyploid nucleus, rather than via concerted evolution (Cedroni et al., 2003). However, the general evolutionary scenario of the Myb gene family still remains unclear; specifically, the ancient origin of the plant R2R3 Myb gene family is subject to controversy. Here, we analyzed new sorghum and maize Myb gene sequences obtained in our laboratory and available Myb sequence data to explore Myb gene evolutionary history, and to study the relationship of Myb gene sequences and their functional diversity.
Section snippets
Isolation and sequencing of Myb genes from sorghum and maize
Maize and sorghum Myb genes were isolated from Bacterial Artificial Chromosome (BAC) clones obtained from Clemson University Genomics Institute (CUGI), Clemson, South Carolina; www.genome.clemson.edu. Membrane filters containing arrayed clones of sorghum (SB_BBa) and maize (ZMMBBb) genomic libraries were hybridized with a radiolabeled fragment of a maize p1-wr gene cDNA containing a typical R2R3 Myb domain. Radiolabeled probes were prepared using an oligo-labeling kit (Amersham Pharmacia
Identification of Myb domains, conserved coding sequences and variant non-coding sequences in Myb genes
Currently there are relatively few complete Myb gene sequences available from cereal grain species. To increase the representation of Myb genes from these important crop plants, we isolated and sequenced maize and sorghum genes encoding Myb-homologous proteins. First, we isolated BAC clones that hybridized with a typical R2R3 Myb probe; second, we used a degenerate oligonucleotide primer complementary to a highly conserved region of Myb genes to sequence directly from each BAC clone. The
Expansion of Myb gene family in monocot
Previous reports have described the expansion of Myb-homologous genes in various plants including maize and Arabidopsis (e.g., Rabinowicz et al., 1999). For example, 125 R2R3 Myb genes have been identified in Arabidopsis (Stracke et al., 2001). Our results confirm and extend those studies, with new sequence data from 64 sorghum and 31 maize Myb genomic clones (accession numbers: F474125–AF474126AF474127AF474128AF474129AF474130AF474131AF474132AF474133AF470058–AF470059AF470060AF470061AF470062AF470063
Acknowledgements
We thank Terry Olson for the technical assistance in the isolation and sequencing of Myb genes. We acknowledge Monsanto/Pharmacia rice-research.org (www.rice-research.org) for providing the O. sativa genomic sequences. This work was supported by a grant from the USDA-NRICGP to T.P. and S.C, and an NIH grant to X. G. X.G is the Dupont young faculty. This is Journal Paper No. J-19751 of the Iowa Agriculture and Home Economics Experiment Station, Ames, IO, Project No. 3297, and supported by Hatch
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Present address: Department of Crop and Soil Science, Pennsylvania State University, University Park, PA 16802, USA.