, Volume 114, Issue 7, pp 1289-1302

Introgressed and endogenous Mi-1 gene clusters in tomato differ by complex rearrangements in flanking sequences and show sequence exchange and diversifying selection among homologues

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Abstract

Many plant disease resistance genes (R-genes) encode proteins characterized by the presence of a nucleotide-binding site (NBS) and a leucine-rich repeat (LRR) region and occur in clusters of related genes in plant genomes. One such gene, Mi-1, confers isolate-specific resistance against root-knot nematodes, aphids and whiteflies in cultivated tomato, Solanum lycopersicon. The DNA region carrying Mi-1 and six closely related sequences was introgressed into tomato from Solanum peruvianum in the 1940s. For both susceptible and resistant tomato, Mi-1 homologues are present in two clusters with 3 and 4 copies each on the short arm of chromosome 6. Two homologues from each source are pseudogenes, and one homologue from each source encodes a truncated product. DNA sequence identity among the homologues including the truncated genes, but excluding the pseudogenes, ranges from 92.9 to 96.7%. All the non-pseudogene homologues are transcribed. Comparison of homologues suggests that extensive sequence exchange has occurred. Regions of diversifying selection are present in the ARC2 domain of the NBS region and dispersed throughout the LRR region, suggesting that these regions are possible locations of specificity determinants. Other sequences in the introgressed region have similarity to the Arabidopsis auxin-receptor protein TIR1, a jumonji-like transcription factor and a Na+/H+ antiporter. Analysis of sequences flanking the Mi-1-homologues reveals blocks of homology, but complex differences in arrangement of these blocks when susceptible and resistant genotypes are compared indicating that the region has undergone considerable rearrangement during evolution, perhaps contributing to evolution of specificity.

Communicated by M. Xu.