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Host and Pathogen Factors Controlling the Rice-Xanthomonas oryzae Interaction^[C]

Department of Plant Pathology, Kansas State University, Manhattan, Kansas 66506 (F.F.W.); and Department of Genetics, Development, and Cell Biology, Iowa State University, Ames, Iowa 50011 (B.Y.)

Rice (Oryza sativa) cultivation represents a world laboratory for investigation into bacterial diseases of rice, in particular, and host-parasite interactions, in general, at the molecular, genetic, and genomic levels. The crop, in its various forms, has been under intense cultivation for more than 6,000 years, resulting in the selection of a wide variety of traits and germplasm (Khush, 1997). Tremendous molecular and genetic resources have also been developed in recent years. The species can be genetically manipulated by Agrobacterium tumefaciens-mediated transformation (Krishnan et al., 2009). Against this backdrop, bacterial blight is an important disease of rice and present throughout much of the rice-growing regions (Ou, 1985; Mew et al., 1993; Fig. 1 ). Xanthomonas oryzae pv oryzae (Xoo) is the causal agent and a member of the -proteobacteria and, like many other proteobacteria, depends, in part, on a type III secretion system for pathogenicity (Swings et al., 1990; Zhu et al., 2000). The bacterium invades the xylem tissue, either through wounds or water pores, leading to systemic infection. Bacterial streak of rice is caused by the closely related pathovar X. oryzae pv oryzicola (Xoc), which, in contrast to Xoo, is limited to the intervascular regions, giving the disease the characteristic leaf streaking (Niño-Liu et al., 2006). Bacterial streak can also cause severe losses, although the disease tends to be tropical and is more sporadic than blight (Niño-Liu et al., 2006). This review will highlight recent advances in our knowledge of bacterial blight and, to a lesser extent, bacterial streak with regard to the host-bacteria interaction and the peculiar exploitation of a family of type III effectors. We will also provide speculation and thought as to how these findings might relate to classical analyses of disease resistance and susceptibility as well as a discussion of prospects for future research.

View larger version (136K): [in this window] [in a new window] [as a PowerPoint slide]   Figure 1. Bacterial blight and bacterial streak of rice. Left, Bacterial blight in an experimental field plot in Korea, 2006. Right, Bacterial streak from a test inoculation (courtesy of Dr. A. Bogdanove).

	RESISTANCE AND SUSCEPTIBILITY GENES TO XOO

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Xa1 represents the second major class of R genes, the nucleotide-binding site (NBS)-LRR group (Yoshimura et al., 1998). Xa1 expression is elevated upon bacterial infection and, as such, represents one of the cases in which R gene regulation is coordinated with other pathways for defense responses (Yoshimura et al., 1998; Zhang and Gassmann, 2007). Rxo1 from maize (Zea mays) is a member of the NBS-LRR gene family and confers broad resistance to Xoc isolates upon transfer to rice (Zhao et al., 2005). Rxo1-mediated resistance is triggered by strains containing the type III effector gene avrRxo1 from Xoc (Zhao et al., 2004). Although rice has relatively large numbers of NBS-LRR genes, Xa1 remains the only endogenous NBS-LRR gene identified for bacterial resistance (Monosi et al., 2004). Xa1 is effective against some Xoo isolates in Japan but is not effective against most strains from the Philippines. The gene for the elicitor signal from the pathogen has also not been identified for Xa1.

Xa27 confers broad resistance and is representative of an unusual class of dominant R genes in rice (Gu et al., 2004). Upon analysis, Xa27 differed remarkably from other R genes in that specificity is based on differential gene expression (Gu et al., 2005). Identical open reading frames are present in resistant and susceptible cultivars but are only expressed in resistant cultivars upon bacterial infection. No function or conditional expression for the susceptible allele of Xa27 has been determined. The product of Xa27 is unrelated to any other class of R protein and has two related open reading frames on chromosome 6, although whether these related genes are functional is unknown. Xa27 is only expressed upon inoculation with Xoo strains harboring the type III effector gene avrXa27 (Gu et al., 2005). XA27 protein appears to be toxic to rice and initiates a resistant reaction upon expression (Gu et al., 2005; Tian and Yin, 2009). When fused to a pathogen-nonspecific-inducible rice OsPR1 promoter, Xa27 conferred resistance to compatible and incompatible strains of the pathogen alike. Localization studies of XA27 indicate that the protein is secreted into apoplastic space and associated with both the plant membrane and cell walls upon gene induction during resistance (Wu et al., 2008; Fig. 2 ). Two additional, as yet uncharacterized, R genes of rice have similar requirements for the transcription activation domain and nuclear localization signal motifs of the corresponding transcription activation-like (TAL) effectors as required for AvrXa27-mediated induction of Xa27 (Hopkins et al., 1992; Zhu et al., 1998; Yang et al., 2000). Cloning and analysis of these R genes will reveal whether the effectors and R gene expression have similar features to Xa27 (Porter et al., 2003; Chen et al., 2008; Gu et al., 2008).

View larger version (84K): [in this window] [in a new window] [as a PowerPoint slide]   Figure 2. Localization of XA27::GFP. XA27 fused to GFP is found associated with cell plasmalemma and cell wall when cells are plasmolyzed (top). A GFP control is shown at bottom. A complete description of the approach is provided by Wu et al. (2008). P, Plasmolyzed plant cell. Arrows indicate adjoining plant cell wall. Photographs are courtesy of Z. Yin.

TFIIA5

TFIIA1

TFIIA5

Another recessive resistance gene, xa13, has been identified by map-based cloning (Chu et al., 2005, 2006). Like xa5, the recessive allele is not a null mutant and encodes a protein related to MtN3, encoding nodulin 3 (N3) protein of Medicago truncatula. The MtN3 gene was first identified in EST libraries of M. truncatula root nodules (Gamas et al., 1996). The dominant allele Xa13 was also named Os8N3 due to the location on rice chromosome 8 and the similarity to MtN3, and that name is used throughout this review (Yang et al., 2006). Os8N3 is a member of a moderately large gene family consisting of 17 to 20 members in rice. Arabidopsis (Arabidopsis thaliana) also has an 18-member MtN3 family, and the family is also conserved across kingdom boundaries, with related genes in mammals, insects, nematodes, and filamentous fungi, although not to the same degree as TFIIA (Chu et al., 2006; Yang et al., 2006; Guan et al., 2008; B. Yang and F.F. White, unpublished data). The critical difference between resistant (xa13/xa13) and susceptible plants is the elevated expression of Os8N3 during bacterial infection in susceptible plant genotypes and the absence of Os8N3 induction during bacterial infection in the resistant genotypes (Yang et al., 2006; Yuan et al., 2009). Knockdown of Os8N3 expression by inhibitory RNA also results in resistance to some bacterial strains, but, unlike xa13 genotypes, silenced plants have low pollen viability and reduced numbers of viable seeds (Chu et al., 2006; Yang et al., 2006). Thus, xa13 confers resistance due to a lack of elevated Os8N3 expression during bacterial infection. Os8N3, therefore, is a susceptibility (S) gene that is exploited by Xoo, and the xa13 resistance is a naturally occurring allele, actually a series of alleles that "fix" a genetic disease vulnerability in the plant developmental pathways (Yang et al., 2006). Bacterial strains that induce Os8N3 expression are virulent, and those strains that normally induce Os8N3 but not the xa13 allele are incompatible. The xa13 gene appears to have been a valuable allele in rice cultivation, as the resistance has occurred in various forms in a variety of cultivars (Chu et al., 2005). The simplest variant is present in ‘BJ1’, where the difference between the resistant and susceptible alleles is a single nucleotide change in the promoter region of the gene. Other variants have more apparent complex alterations, including multiple base changes and/or insertions in the Os8N3 promoter region (Chu et al., 2006). Further expression analysis of Os8N3 and the various xa13 alleles will provide important insights into the intricacy of host genes that have adapted for disease resistance while maintaining normal developmental processes. Despite the number of alleles, xa13 is not as broad as the resistance provided by Xa21, Xa27, and xa5, and many strains from China, the Philippines, Japan, and Korea are compatible on xa13 lines (Yang et al., 2006).

The number of strains that are compatible on plants containing xa13 illustrates that Xoo can and has adapted to xa13 alleles as well as other R genes in the host. Studies of the basis of compatibility and incompatibility between rice genotypes and strains of the pathogen have been conducted in the hope that insight may be gained into the factors that affect R gene breadth and durability, which here is defined loosely as the time the R gene is effective against extant populations of pathogens.

	TYPE III EFFECTORS IN XOO

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Despite all the resources, only two pathogen genes for elicitors that correspond to cloned R genes for bacterial blight or streak of rice have been cloned: avrXa27 from Xoo as the cognate elicitor gene for Xa27 and, if the heterologous Rxo1 gene from maize is included, avrRxo1 from Xoc (Table II ). Both genes encode substrate proteins that are secreted through the bacterial type III secretion system (T3SS) and are generally known as type III (T3) effectors, which are fully reviewed in this issue. A functioning T3SS is required for pathogenicity of both Xoo and Xoc and serves to secrete multiple T3 effectors into the host cells. Although not all are associated with phenotypic effects for virulence, T3 effectors function, in general, as virulence factors in pathogenicity. A subset of the T3 effectors, including AvrXa27 and AvrRxo1, can serve as the cognate elicitors (avirulence proteins) for specific R genes in many plant systems. Two additional cognate T3 effector (avirulence) genes that have been cloned are avrXa7 and avrXa10, corresponding to the R genes Xa7 and Xa10. Five additional T3 effectors from Xoo have known contributions to virulence under the appropriate conditions (Table II). These genes are pthXo1, pthXo2, pthXo3, pthXo6, and pthXo7. The gene avrXa7, in addition to Xa7-dependent elicitor activity, is also a virulence factor. Four additional T3 effectors were derived under a laboratory setting from avrXa7 (Table II; Yang et al., 2005). Two genes, named pthXo4 and pthXo5, have lost Xa7-dependent elicitor activity while maintaining virulence activity. A third gene, avrXa7-38, retained Xa7-dependent activity without the accompanying virulence activity, and a fourth, avrXa7-sacB50, appears to have lost both avirulence and virulence activity but acquired avirulence activity on the otherwise susceptible rice line IR24. The new incompatible response was not observed on the rice line Nipponbare. Preliminary results indicate that a sixth gene, pthXo8, also contributes to the virulence of Xoo (B. Yang, unpublished data). With the exception of avrRxo1, all of the above T3 effectors are related to avrBs3 and pthA, which were first identified in X. campestris pv vesicatoria and X. campestris pv citri, the causal agents of bacterial spot of pepper (Capsicum annuum) and citrus (Citrus species) canker, respectively (Bonas et al., 1989; Swarup et al., 1991). The AvrBs3/PthA-related T3 effectors have properties of transcription factors and possess eukaryotic nuclear localization signal motifs and a potent acidic transcription activation domain in the C-terminal portion (Van den Ackerveken et al., 1996; Zhu et al., 1998). The proteins have DNA-binding activity, and AvrBs3 can bind specific gene promoter sequences in vivo, as shown by chromatin immunoprecipitation and gel shift assays (Yang et al., 2000; Kay et al., 2007). Here, we refer to the family of T3 effectors as the TAL T3 effectors, and each protein has a series of highly conserved repeated sequence of amino acids (Fig. 3 ). The consensus repeat, in Xoo and Xoc, is 34 amino acid residues, although some repeats have single codon deletions or internal smaller repetitive portions. With some exceptions, the central repetitive region can be switched among the TAL effector family members while retaining the biological activity of the effector from which the repeat region is derived. Thus, some aspect of TAL effector specificity is dictated by the repetitive structure. The repeats may affect domain spacing as well as, perhaps, the maintenance of individual effector identity. The proteins are believed to function as dimeric proteins within the host (Gurlebeck et al., 2005). The closest structural relative of the repeat region is the so-called tetratricopeptide repeat, which is also approximately 34 amino acid residues in length and widespread in proteins of diverse function (Blatch and Lassle, 1999).

View larger version (5K): [in this window] [in a new window] [as a PowerPoint slide]   Figure 3. Prototypic TAL effector. Each TAL effector contains a central repetitive region of varying numbers of 34 amino acid repeat units (white boxes). The C-terminal region contains three nuclear localization signal motifs (NLS [A, B, and C]) and an acidic activation domain (AD).

	IMPLICATION OF INTERACTION BETWEEN T3 EFFECTORS AND THE CORRESPONDING HOST GENES

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Xa27 and xa13 have provided insight into the diversity of resistance mechanisms in rice. The apparent reason for the broad activity of Xa27 is the presence of avrXa27 in a large number of strains from southeast Asia, including many strains from Korea, China, Japan, and the Philippines (Gu et al., 2004). At the same time, two lines of evidence indicate that strains of Xoo could defeat Xa27. First, avrXa27 is present in a single copy, at least in the two strains that have been examined; therefore, simple loss or mutation of the gene converts incompatible strains to compatible strains on plants with Xa27 (Gu et al., 2005; Ochiai et al., 2005). Second, mutation of avrXa27 in the strain PXO99^A converts PXO99^A to compatibility on plants containing Xa27 and does not lead to any detectible loss of virulence. Thus, the loss of avrXa27 does not appear to have a fitness cost to the pathogen, and populations of Xoo without avrXa27 could be expected to appear relatively rapidly should Xa27 be deployed. avrXa7, unlike avrXa27, is an important virulence factor for some strains of Xoo, and loss of avrXa7 can result in strains that are only weakly virulent (Bai et al., 2000; Yang et al., 2000). Several factors mitigate the argument that Xa7, by itself, would provide durable resistance due to the fitness cost for loss of avrXa7 in the pathogen. One factor is that a variety of other TAL T3 effector genes are present in Xoo populations that do not have Xa7-mediated elicitor activity but can restore full virulence to strains missing avrXa7 (Yang and White, 2004). We refer to interchangeable TAL effectors with regard to virulence activity as major TAL effectors. In addition to avrXa7, the major TAL effector genes in Xoo are pthXo1, pthXo2, and pthXo3 (Yang and White, 2004). Loss of Xa7-dependent elicitor activity from avrXa7 and concomitant retention of virulence activity has also been observed (Yang et al., 2005). Thus, evasion of Xa7-mediated resistance should, at least theoretically, be possible by deletion of the central repeats, as observed for pthXo4, by recombination among different TAL effector genes, as observed with pthXo5, or by horizontal transfer of alternate virulence factors (Yang et al., 2005). At the same time, field studies in the Philippines indicated that deployment of Xa7 was durable in test plots for more than 10 years (Vera Cruz et al., 2000). Regardless of the possibility of race changes in the pathogen population, pyramiding R genes with cognate T3 effectors that are widespread in the pathogen populations should provide a degree of broad durable resistance.

TAL T3 effectors also are involved in recessive resistance. In the case of xa13, induction of the dominant allele Os8N3 is mediated by the TAL effector PthXo1 (Yang et al., 2006). The gene pthXo1 was first identified in Xoo strain PXO99^A, which coincidentally is also a strain that is incompatible on plants that are homozygous for xa13 (Yang and White, 2004). PXO99^A cannot induce the xa13 allele of Os8N3 and does not grow as well in xa13 plants in comparison with normal plants (Chu et al., 2005; Yang et al., 2006). The introduction of avrXa7, pthXo2, or pthXo3 into PXO99^A restores virulence regardless of the presence of pthXo1 (Yang et al., 2006). Thus, xa13-dependent resistance is only effective against strains that rely on pthXo1 and is mimicked phenotypically by mutations in pthXo1 of PXO99^A (Yang et al., 2006). The recessive resistance provided by xa13 is phenotypically and qualitatively different from resistance provided by the dominant R gene Xa7, for example (Chu et al., 2004; Yang et al., 2006). Quantitatively, in terms of bacterial growth and lesion length, resistance mediated by xa13 and Xa7 are approximately equal (Bai et al., 2000; Yang et al., 2000, 2006). However, Xa7 resistance is the result of the presence of the appropriate elicitor gene in the pathogen, while xa13 is dependent on the absence of an effective virulence factor (Fig. 4 ). The xa13 alleles are natural cases of mutations in loss of function for susceptibility, hence the classification of the dominant allele Os8N3 as a S gene of the host and the target of the virulence factor PthXo1. The defeat of xa13-mediated resistance could theoretically involve induction of the xa13 allele or targeting of alternative host genes that provide the same effect as Os8N3. Some variants of xa13 are weakly inducible in young plants and concomitantly have greater susceptibility to PXO99^A as young plants (B. Yang, unpublished data). No strains have been identified that induced the xa13 allele similar to PthXo1-mediated induction of Os8N3, nor have strains with alternate virulence TAL effectors been found that induce Os8N3 in normal plants (Yang et al., 2006). The three aforementioned TAL effectors that restore virulence to PXO99^A compensate for PthXo1 by targeting alternative S genes (B. Yang and F.F. White, unpublished data).

View larger version (95K): [in this window] [in a new window] [as a PowerPoint slide]   Figure 4. Diverse host responses to Xoo challenge in rice. Leaves were inoculated with water or Xoo by needleless syringe. Leaf 1, Mock inoculation; leaf 2, response to T3SS nonpathogenic mutant of PXO99A; leaf 3, recessive R gene response (note the lack of streaking up and down the leaf blade); leaf 4, fully susceptible response (wild-type strain); leaf 5, PXO99A (avrXa7; response to dominant R gene Xa7). Photographs were taken with back lighting, and yellow zones are indicative of water soaking.

The genomic sequences are available for three strains of Xoo and one strain of Xoc (Lee et al., 2005; Ochiai et al., 2005; Lu et al., 2008; Salzberg et al., 2008). The full complement of TAL T3 effectors are now known for two strains of Xoo and one strain of Xoc, and both pathogens are unusual due to the high number of TAL effector genes within their individual genomes. Xoo strains PXO99^A and MAFF311018 (also named T7174) have 19 and 17 genes, respectively, organized in nine and eight regions of their respective genomes (Ochiai et al., 2005; Salzberg et al., 2008; Fig. 5 ). The individual genes are distinguishable on the basis of the number of repeats in the central repetitive region and by polymorphisms within each repeat sequence, particularly at the 12th and 13th codons. A comparison of the repetitive regions of PXO99^A and MAFF311018 indicates a high degree of rearrangements and shuffling of the genes at all of the loci, to the point where only three genes of 17 in MAFF311018 are identical (Salzberg et al., 2008). The large numbers of TAL effector genes in these species may reflect the evolutionary "investment" the strains have in utilizing the TAL effectors for virulence. The major contribution to virulence by pthXo1, for example, corroborates the view that the genes, as a class of T3 effectors, are important, maybe essential, to the ecological niche these bacteria occupy. Yang and Gabriel (1995) proposed that maintenance of a large repertoire of TAL effector genes may increase the frequency of recombination between genes and, as a consequence, increase the diversity of TAL effectors within the pathogen population. Populations with greater diversity of effector genes may then adapt faster to changing host genotypes. The maintenance of high gene numbers may even be exacerbated by rice breeding and R gene deployment by farmers over the millennia. The gene pthXo5, for example, gained virulence function by recombination of the original avrXa7 and a chromosomal gene of PXO99^A, now known to be pthXo6 (Yang et al., 2005; Sugio et al., 2007). Some of the genes are apparent pseudogenes, in the sense that a number of the genes are truncated in comparison with known functional genes (Salzberg et al., 2008). Pseudogenes could still serve as recombination substrates for generating new effector genes. Remarkably, Xoc strain BLS256 has 28 TAL effector genes, and the evidence also indicates that none are identical and most are unique with respect to repetitive region sequence. The profiles of changes in host gene expression upon infection by Xoc also appear different (A. Bogdanove, unpublished data). Differences in TAL effector gene effects have been observed between Xoo and Xoc, indicating possible differences in TAL effector utilization for host adaptation (Makino et al., 2006).

View larger version (10K): [in this window] [in a new window] [as a PowerPoint slide]   Figure 5. Genomic positions of TAL effector genes in two strains of Xoo. Genes are labeled and identified by biological function and name, where assigned (adapted from Salzberg et al. [2008] and Ochiai et al. [2005]). The dashed line indicates the location of the PXO99A TAL effector gene 9e in MAFF3113018. Apostrophes after gene letters indicate truncated genes. Colored boxes indicate gene clusters. [See online article for color version of this figure.]

OsTFIIA1

TFIIA5

Research into the molecular basis of Xoo and Xoc interaction with the host promises to provide exciting new insights in the near future into the adaptations between pathogen and host. The full complement of host effects due to the T3 TAL effectors wait to be discovered as more genes, strains, and host genotypes are examined. More recently, the characterization of strains from West Africa has revealed new genotypes of both Xoo and Xoc and indicates that an ability to cause bacterial blight of rice may have arisen in at least three lineages of related bacteria (Gonzalez et al., 2007). The research has also uncovered a variety of novel R genes, and a further understanding of their function in host susceptibility and resistance will be forthcoming. As in other bacterial pathogen-host systems, the features of a host strategy to turn the mechanism of the virulence factors against the pathogen are beginning to emerge. Curiously, in the rice system, the pathogen gains advantage by expropriating the developmental control of host genes and subsequent induction of a membrane protein, in the case of Os8N3. The host, on the other hand, can foil the process by production of a separate membrane protein (XA27) that triggers a rapid defense response. The differential effects of the proteins and the components of the two consequences on host cell physiology await further investigations. XA27, on the basis of sequence relatedness, is unique to rice and, possibly, some relatives (Gu et al., 2004), and it is one of a number of genes that may have been "invented" through the evolutionary process for specific purposes (Xiao et al., 2009).

Our understanding of Xoo and Xoc virulence is far from complete. For example, a third TAL effector gene, named pthXo8, has been identified in PXO99^A with quantitative effects similar to pthXo6, and the host gene expression associated with pthXo8 is under investigation. Preliminary evidence indicates that the effector is involved in manipulation of the small RNA pathways of the host. The curious and novel nature of the TAL T3 effectors sometimes distracts attention from the presence of multiple other T3 effectors in Xoo and Xoc genomes. Recent characterization of the genomic data from MAFF311018 indicates that at least 19 candidate T3 effector genes, in addition to the 17 TAL effector genes, are present in the genome (Furutani et al., 2009; Table III ). Three of the T3 effector genes are novel to Xoo (Furutani et al., 2009). The value of RLK-type resistance in rice is evident through the investigations of Xa21 and Xa26 (Lee et al., 2006; Cao et al., 2007). At the same time, some Xoo strains are virulent in Xa21 or Xa26 plants (Lee et al., 1999, 2003; Jeung et al., 2006), and evidence from the case of FLS2 and related proteins indicates that PTI is also vulnerable to T3 effector interference (Gohre et al., 2008; Xiang et al., 2008; reviewed in more detail in this issue). Xoo and possibly Xoc appear to have built a lifestyle that is dependent on a single family of T3 effector genes. This strategy, while providing interesting insight to the vulnerabilities and driving forces of rice genome evolution, may also prove the Achilles' heel in future strategies for durable and broad resistance to bacterial blight and streak in rice.

	ACKNOWLEDGMENTS

Received April 1, 2009; accepted May 17, 2009; published May 20, 2009.

	FOOTNOTES

 
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Frank F. White (fwhite{at}ksu.edu).

^[C] Some figures in this article are displayed in color online but in black and white in the print edition.

www.plantphysiol.org/cgi/doi/10.1104/pp.109.139360

^* Corresponding author; e-mail fwhite{at}ksu.edu.

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