Genome-wide mapping of NBS-LRR genes and their association with disease resistance in soybean

Abstract

Background: R genes are a key component of genetic interactions between plants and biotrophic bacteria and are known to regulate resistance against bacterial invasion. The most common R proteins contain a nucleotide-binding site and a leucine-rich repeat (NBS-LRR) domain. Some NBS-LRR genes in the soybean genome have also been reported to function in disease resistance. In this study, the number of NBS-LRR genes was found to correlate with the number of disease resistance quantitative trait loci (QTL) that flank these genes in each chromosome. NBS-LRR genes co-localized with disease resistance QTL. The study also addressed the functional redundancy of disease resistance on recently duplicated regions that harbor NBS-LRR genes and NBS-LRR gene expression in the bacterial leaf pustule (BLP)-induced soybean transcriptome.

Results: A total of 319 genes were determined to be putative NBS-LRR genes in the soybean genome. The number of NBS-LRR genes on each chromosome was highly correlated with the number of disease resistance QTL in the 2-Mb flanking regions of NBS-LRR genes. In addition, the recently duplicated regions contained duplicated NBS-LRR genes and duplicated disease resistance QTL, and possessed either an uneven or even number of NBS-LRR genes on each side. The significant difference in NBS-LRR gene expression between a resistant near-isogenic line (NIL) and a susceptible NIL after inoculation of Xanthomonas axonopodis pv. glycines supports the conjecture that NBS-LRR genes have disease resistance functions in the soybean genome.

Conclusions: The number of NBS-LRR genes and disease resistance QTL in the 2-Mb flanking regions of each chromosome was significantly correlated, and several recently duplicated regions that contain NBS-LRR genes harbored disease resistance QTL for both sides. In addition, NBS-LRR gene expression was significantly different between the BLP-resistant NIL and the BLP-susceptible NIL in response to bacterial infection. From these observations, NBS-LRR genes are suggested to contribute to disease resistance in soybean. Moreover, we propose models for how NBS-LRR genes were duplicated, and apply Ks values for each NBS-LRR gene cluster.

Figure 1

The circular map showing the locations of recently duplicated regions, locations of NBS-LRR genes, transcription levels of NBS-LRR genes after BLP treatment, locations of disease resistance QTL, and locations of significantly expressed NBS-LRR genes. For the QTL layer, the dot colors are defined in the legend. On the transcriptome layer, the heatmap shows the expression level of susceptible NIL 0, 6, and 12 hai and resistant NIL 0, 6, and 12 hai from the inner side to the outer side, and the colors were chosen according to the expression level. Minimum values to maximum values of expression are represented with black, grey, red, orange, yellow, lime, green, blue and purple.

Figure 2

Models explaining the duplication process of NBS-LRR genes. In Model 1, the tandem duplication occurred prior to the recent duplication. In Model 2, the ancient duplication event occurred first, the recent duplication event copied a gene or region to another chromosome, and the tandem duplication occurred independently. In the Mixed Model, the tandem duplication occurred prior to the recent duplication and the independent tandem duplication occurred again after the recent duplication. A bar graph of Ks values between recent duplication regions is shown in the right column of the figure. ID 10176678 was matched with Model 1, where tandem duplication occurred prior to the recent duplication. ID 18934088 was matched with Model 2, where an ancient duplication occurred first, followed by a recent duplication and then tandem duplication. ID 18159398 was matched with the Mixed Model; the tandem duplication of Group 3 on chromosome 13 occurred first and the recent duplication followed prior to the independent tandem duplication of Groups 1 and 2, which occurred on chromosomes 13 and 15.