Clustering of disease resistance loci in the maize genome
--Michael D. McMullen and Kevin D. Simcox

Prior to the advent of RFLP mapping, there was a surprising lack of disease resistance genes that had been placed onto the maize genetic linkage map. A substantial number of resistance genes and QTLs to different plant pathogens and pests have been mapped in the last five years. When the various resistance genes and QTLs are placed onto the linkage map it is evident that resistance genes are clustered in the genome. These clusters of disease resistance loci include not only genes conferring resistance to a single pathogen or pest, but also genes for resistance to unrelated organisms. The bin locations of resistance genes and QTLs reported in the literature are shown in Table 1. There are six different regions that contain resistance genes or QTLs for more than one organism.

The region around bin 1.04, near the centromere on chromosome 1, contains loci for resistance to maize streak virus (msv1) and Cochliobolus carbonum race 1 (hm1). QTLs for northern corn leaf blight (NCLB), Erwinia stewartii, gray leaf spot (GLS), Gibberella zeae, and 2nd brood European corn borer (ECB) also map in or near this region.

The cluster on chromosome 3 includes loci for resistance to maize mosaic virus (mv1), WSMV (wsm2), and Puccinia sorghi (rp3). These genes map near umc10 in the centromeric region of chromosome 3. QTL loci for resistance to G. zeae and ECB map to bins just distal to this region.

The short arm of chromosome 4 contains a single gene for resistance to P. sorghi (rp4) and QTLs for resistance to NCLB, GLS, G. zeae, and 1st brood ECB. This region is particularly

Table 1. Chromosomal bin location of disease resistance loci and QTLs affecting plant response to pathogens and pests. An asterisk (*) is used to designate a bin containing a QTL.1
 
  MDMV SCLB WSMV MMV P.s. P.p. E.s.
1S             1.04-1.06*
1L              
2S              
2L              
3     3.04 3.04 3.04    
4S         4.01*    
4L              
5              
6 6.01 6.01 6.01        
7              
8              
9S              
9L              
10S         10.01 10.01  
10L     10.05        
               
  GLS G.z. ECB NCLB MSV C.c.  
1S 1.04*   1.01* 1.02-1.05* 1.04    
1L   1.07* 1.07*     1.06  
2S 2.04*   2.02*        
2L     2.08* 2.08      
3   3.06* 3.05* 3.08*      
4S 4.02* 4.01-          
4.04*   4.01*          
4L 4.07*            
5   5.04*   5.01*      
6              
7     7.04* 7.03*      
8 8.06*   8.04* 8.04*      
8.06              
9S     9.01*        
9L           9.04*  
10S              
10L 10.05* 10.05* 10.04*        

1MDMV = Maize Dwarf Mosaic Virus (McMullen and Louie, Mol. Plant-Microbe Interact. 2:309, 1989); SCLB = Southern Corn Leaf Blight (Zaitlin et al., Genome 36:555, 1993); WSMV = Wheat Streak Mosaic Virus (McMullen et al., Mol. Plant-Microbe Interact. 7:708, 1994); MMV = Maize Mosaic Virus (Ming et al., MNL this issue); P.s. = Puccina sorghi (MNL 68:177); P.p. = Puccina polysora (MNL 68:177); E.s. = Erwinia stewartii (Ming et al., MNL this issue); MSV = Maize Streak Virus (Kyetere et al., MNL this issue); NCLB = Northern Corn Leaf Blight (Freymark et al., 87:537, 1993); GLS = Gray Leaf Spot (Bubeck et al., Crop Sci 33:838, 1993); G.z. = Gibberella zeae (Pe et al., MGG 241:11, 1993); ECB = European Corn Borer (Beavis et al.,Crop Sci 34:882, 1994; Schön et al., Heredity 70:648, 1993); C.c. = Cochliobolus carbonum race 1 (MNL 68:167).

interesting since bx1 maps to this region. The bx1 locus is involved in the accumulation of DIMBOA, a pre-formed anti-microbial com-pound. The presence of DIMBOA has been shown to be correlated with reduced NCLB lesion size (Couture et al., Physiol. Plant Path. 1:515, 1971; Freymark et al., Theor. Appl. Genet. 87:537, 1993). The NCLB, GLS, G. zeae, and ECB QTLs mapping to this region might be associated with regulation of DIMBOA accumulation.

On chromosome 6, three resistance genes map to bin 6.01; maize dwarf mosaic virus (mdm1), WSMV (wsm1), and resistance to southern corn leaf blight (rhm1). This region on chromosome 6 also contains the NOR, which has been shown to co-segregate with mdm1 (Simcox et al., MNL 67:117, 1993; Simcox et al., Theor. Appl. Genet. 90:341-346, 1995).

A cluster on the long arm of chromosome 8 includes Ht2 and Htn1 (bin 8.06), and QTLs for resistance to NCLB and GLS. The QTL for NCLB located on the long arm of chromosome 3 (3.08) might be related to the NCLB QTL on chromosome 8. Chromosomes 3 and 8 share extensive duplicated sequences, especially in the region of bins 3.08 and 8.06 (Simcox and Bennetzen, Phytopathology 83:1326, 1993).

The other significant cluster is on the long arm of chromosome 10. Resistance to WSMV (wsm3) and QTLs for resistance to GLS, G. zeae, and ECB have been mapped near umc44.

It is interesting to speculate if there is a functional significance underlying clustering of disease resistance genes or if clustering is a consequence of genome organization. It is possible that these clusters represent gene families involved in signal transduction, or some other step in the cascade of events leading to an incompatible interaction between the host and the pathogen or pest. On the other hand, the clusters of disease resistance genes might represent ancestral arrangements of either disease resistance genes or genes which were recruited during the evolution of the pathosystem. It is interesting to note that the clusters present on chromosomes 1 and 3 are in the centromere region, and that the cluster on chromosome 6 is tightly linked to the NOR, which suppresses recombination. Over the evolution of maize, sequences mapping to regions of reduced recombination potential might be maintained as a linkage block. It will be interesting to determine if disease resistance genes map to syntenic regions of other grass species.
 


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