THE R1 RESISTANCE CLUSTER CONTAINS THREE GROUPS OF INDEPENDENTLY EVOLVING, TYPE I R1 HOMOLOGUES AND SHOWS SUBSTANTIAL STRUCTURAL VARIATION AMONG HAPLOTYPES OF SOLANUM DEMISSUM

Authors: KUANG, HANHUI - ARS-UCB PLNT GENE EXP CTR; WEI, FUSHENG - ARS-UCB PLNT GENE EXP CTR; MARANO, MARIA ROSA - ARS-UCB PLNT GENE EXP CTR; WIRTZ, UWE - ARS-UCB PLNT GENE EXP CTR; WANG, XIAOXUE - ARS-UCB PLNT GENE EXP CTR; LIU, JAI - TIGR ROCKVILLE MD; SHUM, WAI PUN - ARS-UCB PLNT GENE EXP CTR; ZABORSKY, JENNIFER - TIGR ROCKVILLE MD; TALLON, LUKE - TIGR ROCKVILLE MD; RENSINK, WILLEM - TIGR ROCKVILLE MD; LOBST, STACEY - TIGR ROCKVILLE MD; ZHANG, PEIFEN - ARS-UCB PLNT GENE EXP CTR; TORNQVIST, CARL-ERIK - ARS-UCB PLNT GENE EXP CTR; TEK, AHMET - HORTICLT U WI MADISON WI; Bamberg, John; HELGESON, JOHN - 3655-05-00 ARS (RETIRED); FRY, WILLIAM - PLNT PATH CORNELL ITHACA; YOU, FRANK - PLNT SCI, UC DAVIS, CA; LUO, MING-CHENG - PLNT SCI, UC DAVIS, CA; JIANG, JIMING - HORTICLT U WI MADISON WI; BUELL, C. ROBIN - TIGR, ROCKVILLE MD; Baker, Barbara

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/28/2005
Publication Date: 10/1/2005
Citation: Kuang, H., Wei, F., Marano, M., Wirtz, U., Wang, X., Liu, J., Shum, W., Zaborsky, J., Tallon, L.J., Rensink, W., Lobst, S., Zhang, P., Tornqvist, C., Tek, A., Bamberg, J., Helgeson, J.P., Fry, W., You, F., Luo, M., Jiang, J., Buell, C., Baker, B.J. 2005. The R1 resistance cluster contains three groups of independently evolving, type I R1 homologues and shows substantial structural variation among haplotypes of Solanum demissum. Plant Journal. 44(1):37-51.

Interpretive Summary: To explore the functional and evolutionary significance of disease resistance gene clustering in the generation of novel resistance genes, we constructed physical maps of the R1 resistance gene cluster in each of the three haplotypes of wild potato species Solanum demissum. Three distinct resistance gene families were identified, one homologous to the potato R1 gene and two others homologous to either the Prf or the Bs4 R-gene of tomato. We determined that the R1 homologues form three independent groups of fast-evolving Type I resistance genes, providing the first report of differentiation of Type I. This is the first report of groups among Type I resistance genes. Such genes were first identified among clustered RGC2 genes in lettuce, where they were distinguished from slow-evolving Type II R-genes. Our findings suggest that a common or similar mechanism underlies differentiation of Type I and Type II R-genes and differentiation of Type I R-genes into distinct groups.

Technical Abstract: Cultivated and wild potatoes contain a major disease resistance cluster on the short arm of chromosome V, including the R1 resistance (R) gene against potato late blight. To explore the functional and evolutionary significance of the clustering in the generation of novel disease resistance genes, we constructed three ~1 Mb physical maps in the R1 gene region, one for each of the three genomes (haplotypes) of allohexaploid Solanum demissum, the wild potato progenitor of the R1 locus. A total of 691 kb, 919 kb and 559 kb was sequenced for each haplotype and three distinct resistance gene families were identified, one homologous to the potato R1 gene and two others homologous to either the Prf or the Bs4 R-gene of tomato. The regions with R1 homologues are highly divergent among the three haplotypes, in contrast to the conserved flanking non-resistance gene regions. The R1 locus shows dramatic variation in overall length and R1 homologue number among the three haplotypes. Sequence comparisons of the R1 homologues show that they form three distinct clades in a distance tree. Frequent sequence exchanges were detected among R1 homologues within each clade, but not among those in different clades. These frequent sequence exchanges homogenized the intron sequences of homologues within each clade, but did not homogenize the coding sequences. Our results suggest that the R1 homologues represent three independent groups of fast-evolving Type I resistance genes, characterized by chimeric structures resulting from frequent sequence exchanges among group members. Such genes were first identified among clustered RGC2 genes in lettuce, where they were distinguished from slow-evolving Type II R-genes. Our findings at the RI locus in S. demissum may indicate that a common or similar mechanism underlies the previously reported differentiation of Type I and Type II R-genes and the differentiation of Type I R-genes into distinct groups, identified here.