Comparative Sequence Analysis of the Sorghum RphRegion and the Maize Rp1 Resistance Gene Complex

Abstract

A 268-kb chromosomal segment containing sorghum (Sorghum bicolor) genes that are orthologous to the maize (Zea mays) Rp1 disease resistance (R) gene complex was sequenced. A region of approximately 27 kb in sorghum was found to contain five Rp1 homologs, but most have structures indicating that they are not functional. In contrast, maize inbred B73 has 15 Rp1 homologs in two nearby clusters of 250 and 300 kb. As at maize Rp1, the cluster of R gene homologs is interrupted by the presence of several genes that appear to have no resistance role, but these genes were different from the ones found within the maize Rp1 complex. More than 200 kb of DNA downstream from the sorghum Rp1-orthologous R gene cluster was sequenced and found to contain many duplicated and/or truncated genes. None of the duplications currently exist as simple tandem events, suggesting that numerous rearrangements were required to generate the current genomic structure. Four truncated genes were observed, including one gene that appears to have both 5Ј and 3Ј deletions. The maize Rp1 region is also unusually enriched in truncated genes. Hence, the orthologous maize and sorghum regions share numerous structural features, but all involve events that occurred independently in each species. The data suggest that complex R gene clusters are unusually prone to frequent internal and adjacent chromosomal rearrangements of several types.Disease resistance (R) genes in plants provide a major mode of defense against a wide variety of pathogens and pests. The most abundant class of R genes encodes proteins with a nucleotide-binding site (NBS) and a Leu-rich repeat (LRR) region. The genome of the model plant, Arabidopsis, contains more than 120 NBS-LRR genes (Arabidopsis Genome Initiative, 2000), but the possible R specificities of these candidate R genes are only known for a handful of loci. From the few NBS-LRR genes that have received functional analysis, it appears that the LRR region provides the specificity for recognition of a pathogen gene product (Ellis et al., 2000a), thereby leading to the initiation of a signal transduction cascade that activates several defense pathways.Most of the R gene loci in plants are highly complex, containing numerous nearby R genes (Ellis et al., 2000b). Unequal recombination within an R gene cluster can result in variation in the size and organization of a complex locus. New R genes with novel pathogen-recognition specificities can be generated by this unequal recombination process (Richter et al., 1995). Some R genes appear to be the obvious products of unequal crossing over and/or conversion between R genes in the same tandem array, thereby providing a new "chimeric" locus with a possible new recognition specificity. Hence, complex R gene loci can undergo rapid internal reorganization. In addition, R gene loci often show a lack of synteny in closely related species (Leister et al., 1998), suggesting that they are also unstable in their gross chromosomal locations. For instance, neither the Lr1 R gene of wheat (Triti...

Conserved Noncoding Sequences among Cultivated Cereal Genomes Identify Candidate Regulatory Sequence Elements and Patterns of Promoter Evolution[W]

“…This finding largely reflects difficulties in distinguishing among different members of gene families or between duplicated genes. The best evidence for orthology is obtained by sequencing and comparative analysis of orthologous BAC clones from multiple grass species; however, few such comparisons have been performed to date (Chen et al, 1998;Tikhonov et al, 1999;Tarchini et al, 2000;Morishige et al, 2002;Ramakrishna et al, 2002aRamakrishna et al, , 2002bSong et al, 2002). As demonstrated in our surveys for conserved sequence blocks among both maize-rice and maizesorghum gene pairs, blocks of Ͼ70% identity over a window of 20 bp are likely to be found only among orthologous genes.…”

“…This observation suggests that A1-b is more likely to be orthologous with the maize a1 gene than with sorghum A1-a. Similarly, VISTA comparisons of the maize Rp1-D gene with the different duplicated sorghum rph1 genes characterized by Ramakrishna et al (2002b) found that maize Rp1-D showed CNS only with the sorghum rph1-1 gene promoter region (data not shown), despite the fact that the rph1-1 coding region is truncated. This finding suggests that maize Rp1-D and sorghum rph1-1 may be orthologous genes that subsequently underwent independent duplication and diversification in the maize and sorghum lineages.…”

Dynamic Evolution ofOryzaGenomes Is Revealed by Comparative Genomic Analysis of a Genus-Wide Vertical Data Set

“…In general, large multigene families, such as disease resistance genes and genes involved in reproduction or morphological complexity, evolve rapidly (Leister et al, 1998;Meyers et al, 1999;Song et al, 2001;Ramakrishna et al, 2002aRamakrishna et al, , 2002bSong and Messing, 2002;Fiebig et al, 2004;Schein et al, 2004). The frequent gain and loss of gene family members observed in this region follows the birth-and-death model of gene evolution (Ohno, 1970;Nei et al, 1997;Michelmore and Meyers, 1998;Nei and Rooney, 2005).…”

Target Site Specificity of the Tos17 Retrotransposon Shows a Preference for Insertion within Genes and against Insertion in Retrotransposon-Rich Regions of the Genome

“…Comparative sequence analysis of a resistance gene complex in sorghum and maize shows that disease resistance gene clusters are unusually prone to frequent internal and adjacent chromosomal rearrangements (Ramakrishna et al, 2002). Such rearrangements may facilitate the rapid evolution of these genes and, in turn, help plants develop novel resistance mechanisms.…”