Molecular Plant Advance Access published online on July 31, 2008
Molecular Plant, doi:10.1093/mp/ssn039
Isolation and Manipulation of Quantitative Trait Loci for Disease Resistance in Rice Using a Candidate Gene Approach
National Key Laboratory of Crop Genetic Improvement, National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China
1 To whom correspondence should be addressed. E-mail swang{at}mail.hzau.edu.cn, fax 86-27-8728-7092, tel. 86-27-8728-3009
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Abstract |
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 TOP Abstract INTRODUCTIONRESISTANCE QTLs ARE VALUABLE...DISEASE RESISTANCE QTLs CO...ISOLATION OF MINOR DISEASE...PROSPECTS FOR THE CANDIDATE...FUNDING |
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Bacterial blight caused by Xanthomonas oryzae pv. oryzae and fungal blast caused by Magnaporthe grisea result in heavy production losses in rice, a main staple food for approximately 50% of the world's population. Application of host resistance to these pathogens is the most economical and environment-friendly approach to solve this problem. Quantitative trait loci (QTLs) controlling quantitative resistance are valuable sources for broad-spectrum and durable disease resistance. Although large numbers of QTLs for bacterial blight and blast resistance have been identified, these sources have not been used effectively in rice improvement because of the complex genetic control of quantitative resistance and because the genes underlying resistance QTLs are unknown. To isolate disease resistance QTLs, we established a candidate gene strategy that integrates linkage map, expression profile, and functional complementation analyses. This strategy has proven to be applicable for identifying the genes underlying minor resistance QTLs in rice–Xoo and rice–M. grisea systems and it may also help to shed light on disease resistance QTLs of other cereals. Our results also suggest that a single minor QTL can be used in rice improvement by modulating the expression of the gene underlying the QTL. Pyramiding two or three minor QTL genes, whose expression can be managed and that function in different defense signal transduction pathways, may allow the breeding of rice cultivars that are highly resistant to bacterial blight and blast.
Key Words: bacterial blight • blast • Oryza sativa • quantitative resistance • QTL
Received for publication May 4, 2008. Accepted for publication June 19, 2008.
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INTRODUCTION |
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TOPAbstractINTRODUCTIONRESISTANCE QTLs ARE VALUABLE...DISEASE RESISTANCE QTLs CO...ISOLATION OF MINOR DISEASE...PROSPECTS FOR THE CANDIDATE...FUNDING |
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Approximately 50% of the world's population consumes rice as their main staple food (www.irri.org/). Disease damage is one of the most serious limiting factors for rice production. Bacterial blight caused by Xanthomonas oryzae pv. oryzae (Xoo) and fungal blast caused by Magnaporthe grisea are two of the most devastating diseases of rice worldwide. Chemical controls, biological controls, disease forecasting, and cultivation practices have been applied widely to depress the spread of these diseases (Fravel, 1988; Hokeberg et al., 1997; Bailey et al., 2000; Peters et al., 2003; Mike et al., 2007). Unfortunately, these measures were not very effective. The most economical and environmentally friendly method of disease control is the application of host resistance.
Disease resistance in plants can be classified into two major categories. Various terms have been used to describe the two categories of resistance, such as vertical versus horizontal resistance (Van der Plank, 1968), qualitative versus quantitative resistance (Ou et al., 1975), and complete versus partial resistance (Parlevliet, 1979). In most cases, qualitative resistance is modulated by direct or indirect interaction between the products of a major disease resistance (R) gene and an avirulence gene; this type of resistance is specific to pathogen race and is lifetime limited in a particular cultivar due to the strong selection pressure against and the rapid evolution of the pathogen (McDonald and Linde, 2002). In contrast, quantitative resistance is conferred by quantitative trait loci (QTLs) and is presumably race non-specific and durable (Roumen, 1994).
Considerable progress has been made in rice host resistance for bacterial blight and blast. Approximately 30 R genes for bacterial blight resistance have been identified, and six of them (Xa1, Xa3/Xa26, xa5, xa13, Xa21, and Xa27) have been characterized (Song et al., 1995; Yoshimura et al., 1998; Iyer and McCouch, 2004; Sun et al., 2004; Gu et al., 2005; Chu et al., 2006; Jiang et al., 2006; Xiang et al., 2006). More than 50 R genes for blast resistance have been identified, and eight of them (Pib, Pi-d2, Pi-ta, Pizt, Pi2, Pi9, Pi36, and Pi37) have been characterized (Wang et al., 1999; Bryan et al., 2000; Chen et al., 2006; Qu et al., 2006; Zhou et al., 2006; Lin et al., 2007; Liu et al., 2007). Characterization and analyses of these R genes have provided transgenic tools or tightly linked markers in marker-assisted selection for rice breeding programs. Although numerous QTLs for bacterial blight and blast resistance have been identified (Wang et al., 1994; Li et al., 1999, 2006; Chen, 2001; Chen et al., 2003; Ramalingam et al., 2003), these disease resistance sources have not been effectively used in rice improvement because of the obstacles described in the following sections. In this review, we focus on the work being done to dissect rice quantitative disease resistance and the prospect of using resistance QTLs in breeding programs.
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RESISTANCE QTLs ARE VALUABLE RESOURCES FOR RICE IMPROVEMENT |
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TOPAbstractINTRODUCTIONRESISTANCE QTLs ARE VALUABLE...DISEASE RESISTANCE QTLs CO...ISOLATION OF MINOR DISEASE...PROSPECTS FOR THE CANDIDATE...FUNDING |
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Quantitative resistance, in contrast with qualitative resistance, is generally considered as partial resistance in a particular cultivar (Parlevliet, 1979). This type of disease resistance is controlled by multiple loci, referred to as QTLs, and does not comply with simple Mendelian inheritance. Thus, selecting for these QTLs is difficult. However, several studies have indicated that pyramiding resistance QTLs can achieve the same level or even a higher level of resistance than that conferred by an R gene (Castro et al., 2003a, 2003b; Richardson et al., 2006). A rice population consisting of 241 recombinant inbred lines (RILs) and developed from a cross between susceptible Zhenshan 97 (Oryza sativa ssp. indica) and resistant Minghui 63 (O. sativa ssp. indica) by single-seed descent was used to study quantitative resistance against Xoo and M. grisea (Chen, 2001; Chen et al., 2003). The resistance of Minghui 63 to M. grisea is controlled by the R gene rbr2, which encodes a nucleotide-binding site-leucine-rich repeat type protein, and eight minor QTLs, which accounted for 1.6–6.1% of the phenotypic variation of the resistance (Chen et al., 2003; Yang et al., 2008). In susceptible Zhenshan 97, six resistance QTLs, which explained 2.1–11.7% of the phenotypic variation of the resistance to M. grisea, were identified (Chen et al., 2003). Resistance assessment of each line in this population (Chen et al., 2003) revealed that at least nine lines (R151, R123, R95, R15, R124, R125, R144, R239, and R8), which were free of rbr2 but accumulated most of the QTLs from both the resistant and susceptible parent, showed the same level or even enhanced resistance to M. grisea isolate F1366 as compared to control Minghui 63 (Table 1). Four rice lines (R202, R223, R155, and R218), which carried rbr2 and most of the QTLs from both parents, showed markedly enhanced resistance to F1366 as compared to Minghui 63 (Table 1).
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Chen (2001) examined rice resistance to bacterial blight using the same RIL population mentioned above. Both Minghui 63 and Zhenshan 97 are susceptible to Xoo strain KS-1–21. Though there was no an R gene in this population, six minor QTLs, which explained 4.1–9.2% of the phenotypic variation of resistance to KS-1–21, were identified from Minghui 63 (Chen, 2001); one minor QTL, explaining 4.9% of the phenotypic variation, was identified from Zhenshan 97. Analysis of the data collected by Chen (2001) revealed that three RILs (R96, R117, and R240) that accumulated most of the resistance QTLs from both parents were highly resistant to KS-1–21 (Table 2). Several other RILs (R30, R34, R54, R92, R143, R180, and R209) that carried only one or two of the QTLs showed increased susceptibility to KS-1–21 as compared to their parents, Minghui 63 and Zhenshan 97 (Table 2).
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The polygenic control underlying quantitative resistance has been presumed to be much more durable than qualitative resistance, because each gene involved has a small effect on host resistance. The accumulation of such small effects may process longer life span in crop production than the resistance conferred by a single R gene. In addition, quantitative resistance is putatively race non-specific, as indicated by evidence that resistance QTLs for different rice diseases caused by various pathogens are frequently mapped to the same or overlapping loci (Xiong et al., 2002; Ramalingam et al., 2003; Wen et al., 2003; Chu et al., 2004; Zhang et al., 2005; Li et al., 2006). Thus, QTLs are valuable resources for durable and broad-spectrum resistance.
The use of quantitative resistance in breeding programs is generally difficult, however, because of its complex genetic control and a lack of detailed knowledge about the genes underlying QTLs. In addition, the resolution of QTL mapping is frequently very low because of insufficient population size and limited molecular markers for a particular population. Thus, QTLs are often mapped to intervals covering large DNA fragments. Pyramiding resistance QTLs through crosses between different genetic backgrounds may bring undesired traits into an improved cultivar due to linkage drag. Characterization of the genes underlying resistance QTLs will allow these resources to be used for rice improvement.
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DISEASE RESISTANCE QTLs CO-LOCALIZE WITH PATHOGEN-INDUCED DEFENSE-RESPONSIVE GENES |
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TOPAbstractINTRODUCTIONRESISTANCE QTLs ARE VALUABLE...DISEASE RESISTANCE QTLs CO...ISOLATION OF MINOR DISEASE...PROSPECTS FOR THE CANDIDATE...FUNDING |
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Plant disease resistance is regulated by two classes of genes—R genes and pathogen-induced defense-responsive or defense-related genes. Pathogen recognition activates in a plant the signal transduction network composed of products from the two classes of genes. In general, the expression of defense-responsive genes is induced or suppressed upon pathogen infection, which provides researchers a sign to identify genes putatively involved in the interaction of plants and pathogens.
Large numbers of defense-responsive genes have been identified in rice by differential expression analysis (Kim et al., 2001; Zhou et al., 2002; Chu et al., 2004; Lu et al., 2004; Jantasuriyarat et al., 2005; Venu et al., 2007; Vergne et al., 2007). In rice resistance to bacterial blight and fungal blast, defense-responsive genes have been classified into three types (Wen et al., 2003): (1) pathogen non-specific: the expression of these genes was influenced by infection of both Xoo and M. grisea; (2) pathogen specific but race non-specific: the expression was influenced by infection with different races of Xoo or different isolates of M. grisea, but not both; and (3) both pathogen and race specific: the expression was influenced only by the infection of one Xoo race or one M. grisea isolate. Most of the defense-responsive genes belong to the first type, and these may be the sources for broad-spectrum resistance in breeding programs. These results also suggest that bacterial blight and fungal blast resistance share common pathway(s) but are also regulated by unique defense pathways. Mapping of these defense-responsive genes on rice molecular linkage maps has revealed that some of the genes co-localize with disease resistance QTLs (Wang et al., 2001; Xiong et al., 2002; Ramalingam et al., 2003; Wen et al., 2003; Chu et al., 2004; Liu et al., 2004). These findings suggest that some of the defense-responsive genes may be the ones that underlie resistance QTLs, and these can serve as candidates for characterization of QTL genes.
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ISOLATION OF MINOR DISEASE RESISTANCE QTLs |
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TOPAbstractINTRODUCTIONRESISTANCE QTLs ARE VALUABLE...DISEASE RESISTANCE QTLs CO...ISOLATION OF MINOR DISEASE...PROSPECTS FOR THE CANDIDATE...FUNDING |
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Using near-isogenic lines to fine-map a QTL as a single Mendelian factor allows the isolation of the genes underlying some QTLs. Several rice QTLs controlling heading date, salt tolerance, grain shape, and grain weight have been isolated (Yano et al., 2000; Ren et al., 2005; Fan et al., 2006). However, most of the rice QTLs identified have small effect on disease resistance, usually explaining less than 10% of the phenotypic variation. Thus, it appears that near-isogenic lines may not be the best choice to isolate minor QTLs for disease resistance.
Because some defense-responsive genes co-localize with resistance QTLs (Wang et al., 2001; Xiong et al., 2002; Ramalingam et al., 2003; Wen et al., 2003; Chu et al., 2004; Liu et al., 2004), we established a candidate gene strategy to isolate disease resistance QTLs in rice. This strategy has four steps. First, pathogen-induced defense-responsive genes are identified by differential expression analysis. Next, the genes are mapped onto a molecular linkage map to identify those showing chromosomal locations corresponding to known disease resistance QTLs by bioinformatics analysis. The expression patterns of genes co-localized with QTLs are examined in different rice–pathogen interactions to identify those whose expression is influenced by a wide range of pathogens. Finally, the function of the genes in disease resistance is confirmed by complementary analyses via overexpressing or suppressing the target gene or using the rice mutant of the target gene identified from a rice mutant library. Using this strategy, we have characterized four candidate genes and shown that they can influence the rice phenotype in the interaction with Xoo or M. grisea. Segregation analysis allowed us to map the genes using the RIL population developed from a cross between susceptible Zhenshan 97 and resistant Minghui 63, which had been used to study the quantitative disease resistance for bacterial blight and fungal blast (Chen, 2001; Chen et al., 2003). This mapping confirmed that they were the genes underlying the resistance QTLs. The following are the four examples of isolating resistance QTLs using the candidate gene strategy.
OsWRKY13
This gene encodes a WRKY-type transcription factor (Qiu et al., 2007). Our previous study showed that a cDNA clone EI12I1, corresponding to OsWRKY13, increased expression in the resistance reaction (Zhou et al., 2002). Further analysis showed that OsWRKY13 (EI12I1) expression was induced in different incompatible (resistant) rice–Xoo interactions and rice–M. grisea interactions (Wen et al., 2003). In addition, OsWRKY13 (EI12I1) localized in a region of chromosome 1 covered by a resistance QTL against blast disease identified by two independent groups (Wang et al., 1994; Chen et al., 2003; Wen et al., 2003). Overexpression of OsWRKY13 in a susceptible rice line enhanced rice resistance to Xoo, with the lesion area ranging from 24 to 49% compared to 62% for the susceptible wild-type; OsWRKY13-overexpressing plants also showed enhanced resistance to M. grisea, with the lesion degree ranging from 0 to 3 compared to 4 to 5 for the susceptible wild-type (Qiu et al., 2007). The enhanced resistance was accompanied by the activation of a salicylic acid-dependent pathway and suppression of a jasmonic acid-dependent pathway (Qiu et al., 2007). Mapping of OsWRKY13 using a simple sequence repeat (SSR) marker (Table 3) in the RIL population (Chen, 2001; Chen et al., 2003) showed that OsWRKY13 co-localized with the peaks of resistance QTLs against M. grisea isolate F1814 and Xoo strain KS-1–21, respectively (Figure 1). The QTLs explained only 3.3 and 4.5% of the phenotypic variation of resistance to F1814 and KS-1–21 in the RIL population, respectively.
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OsDR8
This gene encodes an enzyme-like protein involved in thiamine biosynthesis (Wang et al., 2006). The expression of OsDR8 (cDNA EI35I3) was induced in resistance reactions against different Xoo strains and M. grisea isolates (Zhou et al., 2002; Wen et al., 2003). OsDR8 (EI35I3) was mapped to a similar location as a resistance QTL against blast disease on chromosome 7 (Wen et al., 2003). OsDR8-suppressing plants showed reduced resistance or susceptibility to Xoo and M. grisea (Wang et al., 2006). Exogenous application of thiamine complemented the compromised defense of the OsDR8-suppressing plants, suggesting that accumulation of thiamine regulated by OsDR8 may be essential for bacterial blight resistance and blast resistance. Mapping of OsDR8 using an SSR marker (Table 3) in the same RIL population (Chen, 2001; Chen et al., 2003) showed that OsDR8 co-localized with the peak of a resistance QTL that accounted for 2.1% of the phenotypic variation against M. grisea isolate F1366 (Figure 1). OsDR8 also co-localizeed with the peak of a resistance QTL that explained 3.0% of the phenotypic variation against Xoo strain PXO339 in the RIL population.
GH3-8
This gene encodes indole-3-acetic acid-amido synthetase (Ding et al., 2008). The expression of a cDNA EI5P11 (GH3-8) was induced in different resistance reactions for bacterial blight and blast diseases (Zhou et al., 2002; Wen et al., 2003). GH3-8 (EI5P11) was mapped to the same genomic region as a QTL for blast resistance on rice chromosome 7 (Wen et al., 2003). GH3-8-overexpressing plants showed enhanced resistance to Xoo, with the lesion area ranging from 24 to 54% compared with 78% in susceptible wild-type (Ding et al., 2008). This gene activates basal resistance by preventing the accumulation of auxin, which functions as a virulence factor in pathogen infection. Mapping of GH3-8 using an SSR marker (Table 3) in the RIL population (Chen, 2001) showed that GH3-8 co-localized with the peak of a resistance QTL that explained 2.1% phenotypic variation against Xoo strain PXO61 (Figure 1).
OsMPK6
This gene encodes a mitogen-activated protein kinase (Yuan et al., 2007). OsMPK6 is the homologue of Arabidopsis AtMPK4, which is involved in the regulation of pathogen-induced defense response (Yuan et al., 2007). Rice–pathogen interaction influenced OsMPK6 expression. Sequence analysis showed that OsMPK6 localized close to a minor QTL for blast resistance in chromosome 10 (Chen, 2001). These results led us to consider OsMPK6 as a candidate resistance QTL. Suppressing or knocking out OsMPK6 enhanced rice resistance to different races of Xoo, with the lesion area ranging from 5 to 37% compared to 71% measured for the susceptible wild-type (Yuan et al., 2007). Overexpressing OsMPK6 enhanced rice resistance to M. grisea (X. Shen and S. Wang, unpublished data). Mapping OsMPK6 using a cleaved amplification polymorphism sequence marker (Table 3) in the RIL population (Chen et al., 2003) showed that OsMPK6 co-localized with the peak of a resistance QTL that explained 4.2% of the phenotypic variation of resistance against M. grisea isolate F1366 (Figure 1).
Characterization of the genes OsWRKY13, OsDR8, GH3-8, and OsMPK6 indicates that their products do not directly interact with pathogen effectors in disease resistance. Thus, their roles in defense responses will not be changed due to the mutation of pathogens. Modulation of the expression of OsWRKY13, OsDR8, and OsMPK6 can enhance rice resistance to both bacterial blight and blast, suggesting that resistance mediated by these genes is race non-specific. These results provide direct evidence that at least some resistance QTLs are durable and have broad-spectrum resistance.
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PROSPECTS FOR THE CANDIDATE GENE STRATEGY |
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TOPAbstractINTRODUCTIONRESISTANCE QTLs ARE VALUABLE...DISEASE RESISTANCE QTLs CO...ISOLATION OF MINOR DISEASE...PROSPECTS FOR THE CANDIDATE...FUNDING |
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The candidate gene strategy has proven to be a rapid and efficient approach to isolate minor disease resistance QTLs. Characterization of the genes underlying resistance QTLs will facilitate pyramiding these genes via marker-assisted selection in breeding programs. Comparative genomic analyses have revealed extensive colinearity in gene orders in distantly related taxa of grasses (Keller and Feuillet, 2000; Schmidt, 2000; Bennetzen and Ma, 2003). This syntenic relationship has also been observed in resistance QTLs against M. grisea between rice and barley (Chen et al., 2003). Thus, characterization of rice QTLs for disease resistance will help to identify candidate genes underlying resistance QTLs for other cereals as well. Plant disease resistance is regulated via multiple signal transduction pathways, which form a network composed of synergistic or antagonistic cross-talk among these pathways (Hammond-Kosack and Parker, 2003; Durrant and Dong, 2004; Pieterse and Van Loon, 2004; Qiu et al., 2007). A resistance QTL may only function in a branch of a pathway, which would result in a minor contribution to quantitative disease resistance. Our findings suggest that a single minor resistance QTL can be used in breeding resistant cultivars by managing the expression of the gene underlying the QTL. Although the resistance achieved by overexpression or suppression of a QTL gene is frequently less efficient than that conferred by an R gene, pyramiding two or three minor QTLs genes, whose expression is managed and that function in different defense signal transduction pathways, may allow for the breeding of rice cultivars that are highly resistant to bacterial blight and fungal blast.
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FUNDING |
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TOPAbstractINTRODUCTIONRESISTANCE QTLs ARE VALUABLE...DISEASE RESISTANCE QTLs CO...ISOLATION OF MINOR DISEASE...PROSPECTS FOR THE CANDIDATE...FUNDING |
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This work was supported by grants from the National Program on the Development of Basic Research in China and the National Natural Science Foundation of China. No conflict of interest declared.
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