Next Article in Journal
Oxidative Stress Biomarkers in Fish Exposed to Environmental Concentrations of Pharmaceutical Pollutants: A Review
Previous Article in Journal
Bactericidal Effect and Mechanism of Polyhexamethylene Biguanide (PHMB) on Pathogenic Bacteria in Marine Aquaculture
Previous Article in Special Issue
Effects of Temperature and Salt Stress on Cereus fernambucensis Seed Germination
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Recent Progress in Rice–Xanthomonas oryzae Interactions

1
Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, College of Advanced Agricultural Sciences, Zhejiang A&F University, Hangzhou 311300, China
2
State Key Laboratory of Rice Biology and Breeding, China National Rice Research Institute, Hangzhou 311400, China
*
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
Biology 2025, 14(5), 471; https://doi.org/10.3390/biology14050471
Submission received: 24 March 2025 / Revised: 23 April 2025 / Accepted: 23 April 2025 / Published: 25 April 2025
(This article belongs to the Special Issue Regulatory Mechanisms of Plant Stress Response)

Simple Summary

Rice serves as a staple food crop for billions of people, but bacterial diseases like bacterial blight and bacterial leaf streak, caused by Xanthomonas oryzae, can severely reduce rice yields and threaten food security. This review explores how Xanthomonas oryzae infects rice plants and how rice defends against Xanthomonas oryzae, focusing on the roles of bacterial type III secretion effectors and host resistance genes, as well as the holistic insights into interaction mechanisms between the rice host and Xanthomonas oryzae. Modern genetic technologies, such as gene editing and marker-assisted selection, are discussed for being employed to develop next-generation disease-resistant rice varieties. These advances are crucial for reducing rice losses and ensuring stable food production.

Abstract

Rice bacterial blight (BB) and bacterial leaf streak (BLS), caused by Xanthomonas oryzae pv. oryzae (Xoo) and Xanthomonas oryzae pv. oryzicola (Xoc), respectively, are among the most devastating bacterial diseases threatening global rice production. The interactions between rice and Xanthomonas oryzae are complex and dynamic, involving recognition, attack, defense, and adaptation mechanisms enacted by both the rice host and the pathogens. This review summarizes recent advances in understanding rice–Xanthomonas oryzae interactions, focusing on infection models, pathogenic mechanisms, and immune responses elicited by Xanthomonas oryzae. Special attention is devoted to the roles of transcription activator-like effectors (TALEs) and non-TALE effectors in pathogenicity, the functions of resistance (R) genes in defense, and the interconnected molecular networks of interactions derived from multi-omics approaches. Understanding these interactions is essential for developing effective disease-resistance strategies and creating elite disease-resistant rice varieties.

1. Introduction

Xanthomonas is a genus of Gram-negative bacteria that infects approximately 400 host species, including rice, citrus, tomato, and pepper [1]. Xanthomonas oryzae pv. oryzae (Xoo) and Xanthomonas oryzae pv. oryzicola (Xoc), two closely related pathovars, cause bacterial blight (BB) and bacterial leaf streak (BLS) in rice, respectively [2]. BB is one of the most destructive rice diseases, leading to yield losses of 10–30%, with some cases exceeding 50% [3,4]. Similarly, BLS results in yield reductions of 8–32% [5]. The interactions between rice and Xoo/Xoc are intricate and dynamic, with the pathogens attempting to bypass the host’s defense mechanisms while the rice plant employs immune responses to resist infection. This review provides a comprehensive overview of rice–Xoo/Xoc interactions and summarizes recent advancements regarding the immune responses induced by type III secreted effectors and the application of multi-omics technologies to elucidate the molecular mechanisms of these interactions.

2. Xanthomonas oryzae Infection Models

Xoo typically enters rice leaves through hydathodes at the edges and tips or through wounds. The bacteria multiply in the intercellular spaces of parenchyma cells and spread to the xylem, forming a beaded liquid on the leaf surface after a few days [6]. Xoo interacts with xylem parenchyma cells, moving vertically through the leaf via primary veins and laterally through commissural veins (Figure 1A). In contrast, Xoc penetrates the leaf mainly through stomata, multiplies in the sub-stomatal cavity, and remains confined to the apoplast of the mesophyll tissue without invading the xylem (Figure 1A) [2]. It exudes yellow beads or strands from natural openings, contributing to disease spread [6,7].
Due to their different infection methods, BB and BLS are easily distinguishable in the early stages but may appear similar later. BB symptoms begin as small, green, water-soaked spots at the leaf edges that turn into gray lesions (Figure 1B,C). BLS starts with water-soaked lesions between veins that form into translucent yellow streaks (Figure 1B,C). As both diseases progress, their symptoms can overlap, leading to confusion. Both pathogens often coexist in rice fields, with individual leaves displaying symptoms of both diseases [6,8].

3. Type III Secreted Effectors of Xanthomonas—TALEs

During infection, Xanthomonas secretes effectors into host cells primarily via the type III secretion system (T3SS), which is crucial for pathogenesis [9,10]. Most secreted effectors, known as type III secreted effectors (T3SEs), include transcription activator-like effectors (TALEs). TALEs are notable for inducing the expression of host target genes in the nucleus [11]. TALE proteins exhibit specific structural features: (1) The NH2-terminal region is highly conserved and includes a T3SS signal (T3S) for translocating TALEs to the host cytoplasm; (2) The COOH-terminal region contains nuclear localization signals (NLSs) that transport TALEs to the nucleus and a conserved acidic activation domain (AD) for gene transcription activation (Figure 2). Moreover, TALEs have tandem repeat regions (RR) and repeat variable di-residues (RVDs) at positions 12 and 13 that interact specifically with host DNA, binding to effector-binding elements (EBEs) in gene promoters to activate their expression (Figure 2).
The first TALE to be characterized was AvrBs3 from Xanthomonas campestris pv. Vesicatoria, which triggers Bs3-mediated resistance in peppers [12]. AvrBs3 homologs were subsequently found in Xoo, Xoc, Xanthomonas campestris pv. campestris, and other Xanthomonas species [13,14,15,16]. Some Xanthomonas genomes contain fewer than 6 TALEs, while others, like Xoo and Xoc, can have over 10, with a maximum of 28 [17]. It has been confirmed that PthXo1, PthXo2, PthXo3, and AvrXa7 are significant TALEs of Xoo, accounting for more than 80% of the virulence for rice, as quantified by lesion length, when compared to the full virulence associated with wild-type strains [10,18]. Truncated TALE genes, previously thought to be pseudogenes, have been identified in Xoo/Xoc strains and confirmed as truncated TALEs or interfering TALEs (iTALEs). Unlike typical TALEs, iTALEs have 45 or 129 bp deletions in the N-terminal region and lack C-terminal AD domains [19].

4. Type III Secreted Effectors of Xanthomonas—Non-TALEs

In addition to TALEs, T3SS includes non-TALE effectors. Non-TALEs are found in most Xanthomonas species and are primarily composed of a secretion translocation signal and a functional domain (Figure 2). Eighteen non-TALEs are universally present in Xanthomonas. Genome sequence analysis of Xoo and Xoc strains revealed that non-TALEs are highly conserved, although their numbers vary. Specifically, Xoo strains KACC10331, MAFF311018, and PXO99A contain 19, 24, and 20 non-TALEs, respectively, while Xoc strain BLS256 has 26 [20,21,22].
Some effectors are unique to Xanthomonas oryzae, including XopU, XopW, XopY, and XopAB. Notably, XopT and XopAF are exclusively present in Xoo and Xoc, respectively, while XopO and XopAJ are unique to Xoc and Xanthomonas citri subsp. viticola [18,23,24]. AvrBs2, the first described non-TALE in Xanthomonas campestris pv. vesicatoria, is highly conserved [25,26]. Furthermore, XopN has shown similar pathogenicity to AvrBs2 in the GX01 strain of Xoc. In the PX099A strain, a triple mutant (XopZ, XopN, XopV) exhibited shorter lesion lengths, but virulence was restored by reintroducing these effectors in the Kitaake variety [27].

5. TALEs-Induced Rice Immunity to Xanthomonas oryzae

The plant immune system serves as a barrier against pathogen infection and comprises pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) and effector-triggered immunity (ETI) [28]. In PTI, plant cells employ pattern recognition receptors (PRRs) to recognize PAMPs and initiate basal immune responses. For example, FLAGELLIN SENSITIVE2 (OsFLS2) perceives bacterial flagellins, activating downstream defense signaling pathways [29]. In contrast, ETI involves resistance (R) proteins such as nucleotide-binding leucine-rich repeat (NLR)-type protein Xa1, which specifically recognizes TALEs and triggers stronger immune responses [30]. The presence of functional R proteins leads to ETI, whereas their absence results in effector-triggered susceptibility (ETS) [31]. The interplay between pathogen effectors and their corresponding R proteins reflects a molecular confrontation between the pathogen and the host plant. In Xoo/Xoc–rice interactions, TALEs with targeted R genes are key components determining rice resistance or susceptibility to Xoo/Xoc.
For ETI, rice R genes targeted by TALEs of Xoo have been identified and cloned. Xa1 is the first cloned NLR-type R gene. Xa1 can be recognized by multiple TALEs, such as PthXo1, Tal4, and Tal9d. It was reported that Xa1-mediated resistance triggered by TALEs can be suppressed by iTALEs [30,32]. Xa2/Xa31, Xa14, and Xa45 have also been successfully identified and cloned as alleles of Xa1, exhibiting similar functional properties to Xa1 (Table 1) [19,32,33]. Additionally, executor (E) resistance genes, including Xa7, Xa10, Xa23, and Xa27, are induced by altering the promoter structure, allowing recognition by their corresponding TALEs AvrXa7/PthXo3, AvrXa10, AvrXa23, and AvrXa27, thereby conferring resistance against Xoo (Table 1) [34,35,36,37]. Moreover, some TALEs, such as Tal7, Tal9A, and Tal1C, have been identified, but their molecular mechanisms of interacting proteins in rice remain unclear [38,39].
The genetics of resistance to Xoc are complex, and available resources on resistance are limited, resulting in significantly slower research progress compared to Xoo. Rxo1, the first cloned non-host resistance gene in maize, encodes a NLR protein and confers resistance to Xoc when introduced into rice [56,57]. Xo1, an allele of Xa1, recognizes diverse TALEs from both Xoo and Xoc (Table 1) [58]. However, the resistance mediated by Xo1 can be suppressed by interfering TALEs (iTALEs). Additionally, Xo1 only confers resistance to African Xoc strains and is ineffective against Asian Xoc strains [32,58,59]. Notably, the “truncTALE” Tal2h effector from Xoc strain BLS256 can suppress Xo1-mediated resistance [58,60].
For ETS, rice susceptibility (S) genes are genetically dominant, and their expression is induced upon pathogen infection. The induction of SWEET (Sugar Will Eventually Be Exported Transporter) genes facilitates pathogen nutrient acquisition and promotes disease development. For example, the TALE PthXo1 directly binds to EBE in the promoter of OsSWEET11 (Xa13/Os8N3), inducing its expression and conferring susceptibility to Xoo [39,43,49,61,62]. Similarly, the OsSWEET14 (Xa41/Os11N3) promoter is targeted by multiple TALEs, including AvrXa7, PthXo3, TalC, and Tal5, leading to its activation [50,51,52,63]. Additionally, the susceptibility gene SWEET13 (Xa25/Os12N3) can be activated by PthXo2 and PthXo2-like effectors, which bind to variable EBEs in its promoter (Table 1) [44,64]. In contrast, mutations in the EBEs of their recessive alleles, such as xa13, xa41, and xa25, prevent recognition by the aforementioned TALEs, disrupting pathogen colonization and conferring resistance to Xoo in rice (Table 1) [44,45,65]. OsSWEET12 and OsSWEET15 have also been identified as S genes during Xoo infection, as their expression can be induced by the artificial TAL effectors ArtTAL12 and ArtTAL15 [52].
Many non-SWEET S genes play critical roles during Xoo/Xoc infection. The gamma subunit of the basal transcription factor, TFIIAγ5 (also known as Xa5), binds directly to the TFB region of TALEs, forming a complex that facilitates the transcription of TALE-activated genes (Table 1) [54]. However, the mutant variant xa5, which encodes a naturally occurring V39E variant of TFIIAγ5, cannot interact with TALEs, reducing the expression of TALE-driven S or E genes to enhance rice resistance (Table 1) [66,67]. In the absence of TFIIAγ5, another TFIIAγ gene, OsTFIIAγ1, can be activated by PthXo7, explaining the reason that PthXo7-containing Xoo strains overcome xa5-mediated resistance (Table 1) [66]. Interestingly, qBlsr5a was identified as an allele of xa5, which confers resistance to Xoc [68]. Additionally, OsTFX1, encoding a basic leucine zipper (bZIP) transcription factor, is induced by PthXo6 and TalBMAI1 (Table 1) [46,55]. TalBMAI1 also activates OsERF#123, an AP2/ERF transcription factor gene that contributes to susceptibility to African Xoo strains (Table 1) [55]. In rice–Xoc interactions, the sulfate transporter gene OsSULTR3;6 is targeted by Tal2g and serves as a major S gene for Xoc (Table 1) [69].

6. Non-TALE-Induced Rice Immunity to Xanthomonas oryzae

The targets and molecular mechanisms for most non-TALEs in plant cells remain largely unknown, and a few non-TALEs in Xoo have been characterized (Table 2). It was reported that the interaction between non-TALE XopN and OsVOZ2 promotes rice susceptible to Xoo, while the interaction between XopN and OsXNP is speculated to induce calcium deposition and hydrogen peroxide accumulation against Xoo (Table 2) [27,70,71]. Additionally, XopR of Xoo interacts with OsBIK1, suppressing PAMP-triggered stomatal closure in Arabidopsis (Table 2) [72]. Other non-TALEs, such as XopY (Xoo1488), XopAA (Xop2875), and XopK, interact with OsRLCK185, OsBAK1, and OsSERK1, respectively. OsRLCK185 is involved in chitin-induced immune responses. Xoo1488 suppresses chitin-induced MAPK activation by inhibiting the phosphorylation of OsRLCK185 [73]. OsBAK1 is a key component of both microbe-associated molecular patterns (MAMPs) and brassinosteroid (BR) receptors, suggesting that the virulence activity of Xoo2875 is likely mediated by the inhibition of OsBAK1 [74]. XopK directly ubiquitinates the receptor kinase OsSERK2, leading to its degradation and thereby suppressing the immune response triggered by PAMP [75]. XopP interacts with the rice E3 ubiquitin ligase OsPUB44 to inhibit rice resistance to Xoo (Table 2) [76]. Furthermore, XopL interacts with ferredoxin proteins (NbFd) in non-host plants, promoting reactive oxygen species (ROS) burst and inducing cell death (Table 2) [77]. XopZ was found to interact with ORP1C in Xoo strain PXO99A, but ROS burst and PTI marker gene expression data suggest that ORP1C is not involved in the PTI pathway in rice (Table 2) [78]. These findings highlight the potential for cooperation among multiple non-TALEs and their diverse physiological functions in the host, particularly in modulating innate immune responses.

7. Whole Picture of Rice–Xanthomonas oryzae Interaction Mechanisms from Multi-Omics View

Although many bacterial virulence factors and rice resistance genes have been identified or cloned in rice–Xanthomonas oryzae interactions as described above, the molecular mechanisms behind these interactions remain fragmented, with most studies focusing on individual components rather than systemic networks. Over the past two decades, genome-derived multi-omics studies have gradually evolved and expanded. Numerous plant functional genomics studies, which integrate the generation of transgenic and mutant plants with parallel analyses of mRNA expression, protein levels, and metabolic profiles, have been applied to uncover the complex molecular basis underlying rice immunity against Xanthomonas oryzae [79,80,81,82]. The systems-level understandings derived from integrated multi-omics reveal interconnected molecular networks and lay the groundwork for the breeding of Xoo/Xoc-resistant rice varieties, as well as broad-spectrum disease-resistant cultivars. Furthermore, they offer valuable data to develop novel organic pesticides.
Genome re-sequencing of diverse rice varieties can be conducted to comprehensively reveal genomic variations and interactions, facilitating the discovery of novel genes associated with disease resistance. Genome-wide association study (GWAS) analysis can validate the known resistance genes and identify novel sites to expand the current resistance gene pool. A total of 77 and 7 loci associated with Xoo and Xoc resistance, respectively, were identified with the GWAS analysis of 895 accessions from the 3000 Rice Genomes Project (3K RGP) (Table 3). Among the loci, seven for Xoo resistance were co-localized with known Xoo resistance genes, and one locus for Xoc resistance overlapped with a previously reported Xoc resistance QTL. The remaining novel loci encompass several defense-related genes potentially involved in Xoo and Xoc resistance [83]. Through another GWAS involving 340 accessions from the 3K RGP, a total of 11 QTLs associated with Xoo resistance were identified (Table 3). Eight of these resistance loci were mapped to relatively small genomic intervals, consistent with previously reported QTLs or resistance genes. Linear regression analysis revealed a significant correlation between bacterial blight lesion length and the number of favorable resistance alleles [84]. Furthermore, whole genome sequences can provide insights into phylogenetic relationships and help predict genes associated with strain-specific virulence factors and behaviors. A GWAS of 172 global indica rice germplasm infected by representative strains from six Xoo races (China and the Philippines) highlighted the importance of chromosomes 11 and 12 in the evolution of rice disease resistance (Table 3). The hotspot region on chromosome 11 contained 89.6% of significant SNPs associated with resistance to race P1, while the chromosome 12 hotspot encompassed 85.3% of SNPs linked to race P9a resistance [85].
Proteomic analyses of resistant and susceptible rice cultivars during pathogen infection have revealed key proteins associated with defense mechanisms [93]. Time-course proteomic profiling of susceptible rice (RLX) leaves at 3, 6, and 12 h post-inoculation identified critical virulence-related proteins in Xoo, including carbohydrate metabolism enzymes (hexose phosphate mutase, inositol monophosphatase), arginase, and septum site-determining protein (Table 3) [86]. Comparative proteomics between wild-type Xoc and its rpfF mutant (encoding diffusible signal factor synthase) demonstrated DSF’s regulatory role in virulence through nitrogen transfer, protein folding, ROS scavenging, and flagellum formation (Table 3) [87]. In another study comparing incompatible (H471-PXO99A) and compatible (HHZ-PXO99A) interactions, 374 host and 117 pathogen differentially abundant proteins (DAPs) were identified, predominantly involved in secondary metabolism and virulence, respectively. Further, it was demonstrated that phytoalexin and salicylic acid (SA) signaling pathways were activated faster in the incompatible interaction than in the compatible interaction (Table 3) [88].
Transcriptomic profiling serves as a powerful tool for the systematic identification of defense response (DR) genes involved in rice–Xoo interactions. RNA-sequencing analysis of susceptible rice inoculated with two Xoc strains (hypervirulent HGA4 and hypovirulent RS105) revealed distinct temporal patterns of differentially expressed genes (DEGs) at 12 h (PTI phase) and at 3 days post-inoculation (ETI/ETS phase) (Table 3) [89]. The early PTI stage was characterized by conserved DEGs mediating broad-spectrum basal defense, while the late stage showed the predominant regulation of TALE and DR genes. Parallel investigations in Xoo–rice interactions demonstrated that mutants of host-induced virulence factors (ΔxanA and Δimp) similarly disrupted photosynthetic efficiency, redox homeostasis, and secondary metabolite biosynthesis pathways (Table 3) [86]. Furthermore, temperature-dependent transcriptomic analysis demonstrated that WRKY and ERF transcription factor families mediate a temperature-sensitive defense-growth trade-off in rice. Under low-temperature condition, plants sustained the robust activation of defense pathways against Xoo infection. Conversely, elevating temperature induced a physiological shift where resources were preferentially allocated to growth and reproductive processes, resulting in attenuated pathogen responses (Table 3) [90].
When plants are infected by pathogens, they synthesize specialized metabolites. These metabolites generally fall into three categories: primary metabolites, secondary metabolites, and plant hormones [94]. Among these, secondary metabolites such as terpenoids, phenolics, nitrogen-containing compounds, sulfur-containing compounds, and others play a critical role in plant interactions with biotic and abiotic environments and act as modulators of plant defense [95,96,97]. By analyzing and comparing the metabolic characteristics of three rice varieties—resistant (IRBB27), susceptible (IR24), and wild-type (CG154)—in response to bacterial leaf blight, various defense-related metabolites were identified, including amino acids, flavonoids, alkaloids, terpenes, nucleotide derivatives, organic acids, inorganic compounds, fatty acids, and lipid derivatives. Among these, key metabolites such as flavonoids, terpenes, and phenolic compounds showed significantly higher levels in resistant varieties [91]. Rice variety CBB23, which carries the Xa23 resistance gene, was inoculated with Xoo strains AH28 and PXO99A. Metabolomics analysis showed that a large amount of alkaloid and terpenoid metabolite content decreased significantly after inoculation with AH28 compared to inoculation with PXO99A, while the content of amino acids and their derivatives significantly increased [92].
Generally, metabolomics provides a comprehensive analysis of all small molecules within an organism, positioned at the phenotypic endpoint of the omics cascade. It captures the results of an informative sequence starting from the genome and extending through the transcriptome and proteome, offering critical insights into the biochemical basis of plant–pathogen interactions.

8. Concluding Remarks and Future Perspectives

Significant progress has been made in understanding the interaction between rice and Xoo, particularly in identifying and cloning pathogenic effectors and the corresponding rice R genes. However, there exists a notable gap in knowledge concerning the effectors of Xoc and their targeted R genes. Therefore, it is imperative to explore new effectors and their interactions with rice for Xoc infection.
To date, a total of 44 R loci conferring resistance to BB have been identified, with 15 of these R genes having been successfully cloned [98]. Among the 15 R genes, Xa4, xa5, Xa7, xa13, Xa21, and Xa23 have demonstrated strong and broad-spectrum resistance and been widely used in disease-resistant breeding. However, in recent years, due to the evolution of Xoo, many previously resistant rice varieties have lost their effectiveness, highlighting the urgent need to identify new resistance genes and develop new disease-resistant rice varieties adapted to the emerging Xoo strain [99].
To address this challenge, gene editing strategies and molecular marker-assisted selection (MAS) have been employed to create broad-spectrum disease-resistant rice varieties (Figure 3). The disruption of the binding elements for PthXo3, AvrXa7, and PthXo2 within the promoter regions of the OsSWEET14 and OsSWEET13 genes through TALEN technology has demonstrated significant resistance to BB [44,100]. The application of CRISPR/Cas9 technology to target and mutate EBEs of OsSWEET11 and OsSWEET14 in the rice cultivar Kitaake has successfully generated novel rice cultivars. These cultivars, exhibiting mutations in PthXo2-EBE, along with mutations in PthXo1-EBE and PthXo3-EBE, have been shown to confer a broad spectrum of resistance to Xoo infection [53]. Prime Editor (PE) technology addresses the limitations of low homology-directed repair (HDR) efficiency and significantly enhances gene editing precision. Gupta et al. successfully employed the PE5max system to introduce EBE from OsSWEET14 into the promoter of the dysfunctional R gene xa23, creating a functional R gene, Xa23SW14. This modification led to dominant resistance, effectively protecting rice against all Xoo strains carrying pthXo3/avrXa7. Additionally, they converted TFIIAγ5 to xa5, which offers protection against all Asian Xoo strains except those carrying pthXo1 [101]. Further, the double-mutant lines obtained by converting TFIIAγ5 to xa5 and xa23 to Xa23 using the duplex PE system exhibited robust broad-spectrum resistance against multiple Xoo strains [102]. These studies demonstrate the potential of PE technology for precise genetic modifications to enhance disease resistance in crops.
Similarly, several modified disease resistance genes targeting Xoc have been identified in rice. EBEs of OsSWEET11, OsSWEET14, and OsSULTR3;6 in the rice cultivars Guihong 1 and Zhonghua 11 were precisely edited using CRISPR/Cas9 technology. This resulted in the development of the GT0105 (derived from Guihong 1) and ZT0918 (derived from Zhonghua 11) rice varieties, which exhibited significantly enhanced resistance to both Xoo and Xoc strains while maintaining agronomic traits comparable to their wild-type counterparts [103,104]. These findings demonstrate that precise editing of EBEs and S genes in the rice genome can effectively reduce disease incidence without compromising plant performance.
MAS breeding is increasingly used to enhance crop resistance (Figure 3). The success of MAS relies on the availability of strong genes and effective molecular markers. Scientists have developed markers like PR-Bs3, Xa27Fun, Xa23Fun, and MX7 based on E gene promoter characteristics, leading to the creation of rice varieties with improved resistance [105,106]. Resistance in E genes largely depends on the EBEs in their promoters. It was reported that adding six EBEs to the Xa27 promoter allowed the susceptible rice cultivar Kitaake to gain broad-spectrum resistance to both Xoo and Xoc [107]. Similarly, using a promoter with five EBEs to drive Xa10 expression also provideed broad-spectrum resistance to Xoo [108].
The elucidation of the molecular mechanisms underlying rice disease resistance, especially through the application of multi-omics approaches, remains insufficiently explored. The study of plant–pathogen protein interactions (PPI) is crucial for understanding plant diseases and developing effective control strategies (Figure 3). Researchers have constructed plant–pathogen interactomes through predictions and experimental methods. For instance, a study identified 3074 potential PPIs between Ralstonia solanacearum and Arabidopsis thaliana, highlighting the importance of pathogen-targeted proteins in the Arabidopsis PPI network [100]. A computational framework based on structural information has also been proposed to predict PPIs, which is more effective than sequence-based methods [109]. Experimental studies are revealing PPIs as well. Two pathogens and approximately 8000 Arabidopsis proteins were used to create an immune system protein interaction network, finding critical links between effectors and immune receptors [110]. Additionally, researchers developed a network of virulence effector protein interactions involving both ascomycete pathogens and Arabidopsis host proteins, identifying converging host proteins [110,111]. An ABA–T3SE interactome network was also established to study how T3SEs influence abscisic acid responses [112].
However, studies on pathogen–rice interaction networks, particularly those involving Xanthomonas oryzae, remain limited. Developing comprehensive interaction networks between pathogens and rice could help clarify the relationships between effector proteins and rice genes, paving the way for the identification of novel resistance (R) genes and a deeper understanding of the associated mechanisms.
In summary, the rice–Xoo/Xoc pathosystem is a powerful model for advancing disease control research. By combining genomics, proteomics, transcriptomics, and metabolomics, this system provides a multi-omics framework to dissect rice resistance genes and their regulatory networks (Figure 3). A thorough understanding of the interactions between rice and Xanthomonas oryzae is crucial for designing more effective and sustainable strategies to combat bacterial diseases in rice.

Author Contributions

Conceptualization, Y.H. and J.G.; writing—original draft preparation, Y.Q., Q.R. and C.L.; writing—review and editing, Y.H. and J.G.; funding acquisition, Y.H. and J.G. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by grants from the National Natural Science Foundation of China (Grant No. 32472115), the Zhejiang Provincial Natural Science Foundation of China (Grant No. LY23C130004), and the Agricultural Sciences and Technologies Innovation Program of Chinese Academy of Agricultural Sciences.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

No new data were created or analyzed in this study.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Ryan, R.P.; Vorhölter, F.J.; Potnis, N.; Jones, J.B.; Van Sluys, M.A.; Bogdanove, A.J.; Dow, J.M. Pathogenomics of Xanthomonas: Understanding bacterium-plant interactions. Nat. Rev. Microbiol. 2011, 9, 344–355. [Google Scholar] [CrossRef]
  2. Niño-Liu, D.O.; Ronald, P.C.; Bogdanove, A.J. Xanthomonas oryzae pathovars: Model pathogens of a model crop. Mol. Plant Pathol. 2006, 7, 303–324. [Google Scholar] [CrossRef] [PubMed]
  3. Joshi, J.B.; Arul, L.; Ramalingam, J.; Uthandi, S. Advances in the Xoo-rice pathosystem interaction and its exploitation in disease management. J. Biosci. 2020, 45, 112. [Google Scholar] [CrossRef]
  4. Hsu, Y.C.; Chiu, C.H.; Yap, R.; Tseng, Y.C.; Wu, Y.P. Pyramiding Bacterial Blight Resistance Genes in Tainung82 for Broad-Spectrum Resistance Using Marker-Assisted Selection. Int. J. Mol. Sci. 2020, 21, 1281. [Google Scholar] [CrossRef] [PubMed]
  5. Liu, W.; Liu, J.; Triplett, L.; Leach, J.E.; Wang, G.L. Novel insights into rice innate immunity against bacterial and fungal pathogens. Annu. Rev. Phytopathol. 2014, 52, 213–241. [Google Scholar] [CrossRef]
  6. Mew, T.W.; Alvarez, A.M.; Leach, J.E.; Swings, J. Focus on bacterial blight of rice. Plant Dis. 1993, 77, 5–12. [Google Scholar] [CrossRef]
  7. Wang, L.; Makino, S.; Subedee, A.; Bogdanove, A.J. Novel candidate virulence factors in rice pathogen Xanthomonas oryzae pv. oryzicola as revealed by mutational analysis. Appl. Environ. Microbiol. 2007, 73, 8023–8027. [Google Scholar] [CrossRef]
  8. Jiang, N.; Yan, J.; Liang, Y.; Shi, Y.; He, Z.; Wu, Y.; Zeng, Q.; Liu, X.; Peng, J. Resistance Genes and their Interactions with Bacterial Blight/Leaf Streak Pathogens (Xanthomonas oryzae) in Rice (Oryza sativa L.)—An Updated Review. Rice 2020, 13, 3. [Google Scholar] [CrossRef]
  9. Timilsina, S.; Potnis, N.; Newberry, E.A.; Liyanapathiranage, P.; Iruegas-Bocardo, F.; White, F.F.; Goss, E.M.; Jones, J.B. Xanthomonas diversity, virulence and plant-pathogen interactions. Nat. Rev. Microbiol. 2020, 18, 415–427. [Google Scholar] [CrossRef]
  10. Xu, X.; Li, Y.; Xu, Z.; Yan, J.; Wang, Y.; Wang, Y.; Cheng, G.; Zou, L.; Chen, G. TALE-induced immunity against the bacterial blight pathogen Xanthomonas oryzae pv. oryzae in rice. Phytopathol. Res. 2022, 4, 1434–1446. [Google Scholar] [CrossRef]
  11. Boch, J.; Bonas, U. Xanthomonas AvrBs3 family-type III effectors: Discovery and function. Annu. Rev. Phytopathol. 2010, 48, 419–436. [Google Scholar] [CrossRef] [PubMed]
  12. Bonas, U.; Stall, R.E.; Staskawicz, B. Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Mol. Gen. Genet. 1989, 218, 127–136. [Google Scholar] [CrossRef] [PubMed]
  13. Swarup, S. Isolation of Pathogenicity Genes from Xanthomonas Species and Study of Their Regulation. Ph.D. Thesis, University of Florida, Gainesville, FL, USA, 1991. [Google Scholar]
  14. Swarup, S.; Yang, Y.; Kingsley, M.T.; Gabriel, D.W. An Xanthomonas citri pathogenicity gene, pthA, pleiotropically encodes gratuitous avirulence on nonhosts. Mol. Plant Microbe Interact. 1992, 5, 204–213. [Google Scholar] [CrossRef]
  15. Hopkins, C.M.; White, F.F.; Choi, S.H.; Guo, A.; Leach, J.E. Identification of a family of avirulence genes from Xanthomonas oryzae pv. oryzae. Mol. Plant Microbe Interact. 1992, 5, 451–459. [Google Scholar] [CrossRef]
  16. Yang, B.; White, F.F. Diverse members of the AvrBs3/PthA family of type III effectors are major virulence determinants in bacterial blight disease of rice. Mol. Plant Microbe Interact. 2004, 17, 1192–1200. [Google Scholar] [CrossRef]
  17. Scholze, H.; Boch, J. TAL effectors are remote controls for gene activation. Curr. Opin. Microbiol. 2011, 14, 47–53. [Google Scholar] [CrossRef]
  18. White, F.F.; Potnis, N.; Jones, J.B.; Koebnik, R. The type III effectors of Xanthomonas. Mol. Plant Pathol. 2009, 10, 749–766. [Google Scholar] [CrossRef]
  19. Ji, Z.; Ji, C.; Liu, B.; Zou, L.; Chen, G.; Yang, B. Interfering TAL effectors of Xanthomonas oryzae neutralize R-gene-mediated plant disease resistance. Nat. Commun. 2016, 7, 13435. [Google Scholar] [CrossRef] [PubMed]
  20. Lee, M.Y.; Kim, H.Y.; Lee, S.; Kim, J.G.; Suh, J.W.; Lee, C.H. Metabolomics-Based Chemotaxonomic Classification of Streptomyces spp. and Its Correlation with Antibacterial Activity. J. Microbiol. Biotechnol. 2015, 25, 1265–1274. [Google Scholar] [CrossRef]
  21. Salzberg, S.L.; Sommer, D.D.; Schatz, M.C.; Phillippy, A.M.; Rabinowicz, P.D.; Tsuge, S.; Furutani, A.; Ochiai, H.; Delcher, A.L.; Kelley, D.; et al. Erratum to: Genome sequence and rapid evolution of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A. BMC Genom. 2008, 9, 534. [Google Scholar] [CrossRef]
  22. Ochiai, H.; Inoue, Y.; Takeya, M.; Sasaki, A.; Kaku, H. Genome Sequence of Xanthomonas oryzae pv. oryzae Suggests Contribution of Large Numbers of Effector Genes and Insertion Sequences to Its Race Diversity. Jarq-Jpn. Agric. Res. Q. 2005, 39, 275–287. [Google Scholar] [CrossRef]
  23. White, F.F.; Yang, B. Host and pathogen factors controlling the rice-Xanthomonas oryzae interaction. Plant Physiol. 2009, 150, 1677–1686. [Google Scholar] [CrossRef]
  24. Song, C.; Yang, B. Mutagenesis of 18 type III effectors reveals virulence function of XopZ(PXO99) in Xanthomonas oryzae pv. oryzae. Mol. Plant Microbe Interact. 2010, 23, 893–902. [Google Scholar] [CrossRef] [PubMed]
  25. Kearney, B.; Staskawicz, B.J. Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene avrBs2. Nature 1990, 346, 385–386. [Google Scholar] [CrossRef]
  26. Swords, K.M.; Dahlbeck, D.; Kearney, B.; Roy, M.; Staskawicz, B.J. Spontaneous and induced mutations in a single open reading frame alter both virulence and avirulence in Xanthomonas campestris pv. vesicatoria avrBs2. J. Bacteriol. 1996, 178, 4661–4669. [Google Scholar] [CrossRef]
  27. Long, J.; Song, C.; Yan, F.; Zhou, J.; Zhou, H.; Yang, B. Non-TAL Effectors From Xanthomonas oryzae pv. oryzae Suppress Peptidoglycan-Triggered MAPK Activation in Rice. Front. Plant Sci. 2018, 9, 1857. [Google Scholar] [CrossRef] [PubMed]
  28. Dodds, P.N.; Rathjen, J.P. Plant immunity: Towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 2010, 11, 539–548. [Google Scholar] [CrossRef]
  29. Zhao, Q.; Bao, J.; Li, H.; Hu, W.; Kong, Y.; Zhong, Y.; Fu, Q.; Xu, G.; Liu, F.; Jiao, X.; et al. Structural and biochemical basis of FLS2-mediated signal activation and transduction in rice. Plant Commun. 2024, 5, 100785. [Google Scholar] [CrossRef]
  30. Yoshimura, S.; Yamanouchi, U.; Katayose, Y.; Toki, S.; Wang, Z.X.; Kono, I.; Kurata, N.; Yano, M.; Iwata, N.; Sasaki, T. Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc. Natl. Acad. Sci. USA 1998, 95, 1663–1668. [Google Scholar] [CrossRef]
  31. Kumar, A.; Kumar, R.; Sengupta, D.; Das, S.N.; Pandey, M.K.; Bohra, A.; Sharma, N.K.; Sinha, P.; Sk, H.; Ghazi, I.A.; et al. Deployment of Genetic and Genomic Tools Toward Gaining a Better Understanding of Rice-Xanthomonas oryzae pv. oryzae Interactions for Development of Durable Bacterial Blight Resistant Rice. Front. Plant Sci. 2020, 11, 1152. [Google Scholar] [CrossRef]
  32. Ji, C.; Ji, Z.; Liu, B.; Cheng, H.; Liu, H.; Liu, S.; Yang, B.; Chen, G. Xa1 Allelic R Genes Activate Rice Blight Resistance Suppressed by Interfering TAL Effectors. Plant Commun. 2020, 1, 100087. [Google Scholar] [CrossRef] [PubMed]
  33. Zhang, B.; Han, X.; Yuan, W.; Zhang, H. TALEs as double-edged swords in plant-pathogen interactions: Progress, challenges, and perspectives. Plant Commun. 2022, 3, 100318. [Google Scholar] [CrossRef]
  34. Gu, K.; Yang, B.; Tian, D.; Wu, L.; Wang, D.; Sreekala, C.; Yang, F.; Chu, Z.; Wang, G.L.; White, F.F.; et al. R gene expression induced by a type-III effector triggers disease resistance in rice. Nature 2005, 435, 1122–1125. [Google Scholar] [CrossRef]
  35. Tian, D.; Wang, J.; Zeng, X.; Gu, K.; Qiu, C.; Yang, X.; Zhou, Z.; Goh, M.; Luo, Y.; Murata-Hori, M.; et al. The rice TAL effector-dependent resistance protein XA10 triggers cell death and calcium depletion in the endoplasmic reticulum. Plant Cell 2014, 26, 497–515. [Google Scholar] [CrossRef] [PubMed]
  36. Wang, C.; Zhang, X.; Fan, Y.; Gao, Y.; Zhu, Q.; Zheng, C.; Qin, T.; Li, Y.; Che, J.; Zhang, M.; et al. XA23 is an executor R protein and confers broad-spectrum disease resistance in rice. Mol. Plant 2014, ssu132. [Google Scholar] [CrossRef]
  37. Chen, X.; Liu, P.; Mei, L.; He, X.; Chen, L.; Liu, H.; Shen, S.; Ji, Z.; Zheng, X.; Zhang, Y.; et al. Xa7, a new executor R gene that confers durable and broad-spectrum resistance to bacterial blight disease in rice. Plant Commun. 2021, 2, 100143. [Google Scholar] [CrossRef] [PubMed]
  38. Cai, L.; Cao, Y.; Xu, Z.; Ma, W.; Zakria, M.; Zou, L.; Cheng, Z.; Chen, G. A Transcription Activator-Like Effector Tal7 of Xanthomonas oryzae pv. oryzicola Activates Rice Gene Os09g29100 to Suppress Rice Immunity. Sci. Rep. 2017, 7, 5089. [Google Scholar] [CrossRef]
  39. Moscou, M.J.; Bogdanove, A.J. A simple cipher governs DNA recognition by TAL effectors. Science 2009, 326, 1501. [Google Scholar] [CrossRef]
  40. Zhang, B.; Zhang, H.; Li, F.; Ouyang, Y.; Yuan, M.; Li, X.; Xiao, J.; Wang, S. Multiple Alleles Encoding Atypical NLRs with Unique Central Tandem Repeats in Rice Confer Resistance to Xanthomonas oryzae pv. oryzae. Plant Commun. 2020, 1, 100088. [Google Scholar] [CrossRef]
  41. Luo, D.; Huguet-Tapia, J.C.; Raborn, R.T.; White, F.F.; Brendel, V.P.; Yang, B. The Xa7 resistance gene guards the rice susceptibility gene SWEET14 against exploitation by the bacterial blight pathogen. Plant Commun. 2021, 2, 100164. [Google Scholar] [CrossRef]
  42. Wang, C.; Zhang, X.; Fan, Y.; Gao, Y.; Zhu, Q.; Zheng, C.; Qin, T.; Li, Y.; Che, J.; Zhang, M.; et al. XA23 is an executor R protein and confers broad-spectrum disease resistance in rice. Mol. Plant 2015, 8, 290–302. [Google Scholar] [CrossRef]
  43. Chu, Z.; Fu, B.; Yang, H.; Xu, C.; Li, Z.; Sanchez, A.; Park, Y.J.; Bennetzen, J.L.; Zhang, Q.; Wang, S. Targeting xa13, a recessive gene for bacterial blight resistance in rice. Theor. Appl. Genet. 2006, 112, 455–461. [Google Scholar] [CrossRef] [PubMed]
  44. Zhou, J.; Peng, Z.; Long, J.; Sosso, D.; Liu, B.; Eom, J.S.; Huang, S.; Liu, S.; Vera Cruz, C.; Frommer, W.B.; et al. Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. Plant J. 2015, 82, 632–643. [Google Scholar] [CrossRef] [PubMed]
  45. Singh, A.; Dharmraj, E.; Nayak, R.; Singh, P.K.; Singh, N. Identification of bacterial leaf blight resistance genes in wild rice of eastern India. Turk. J. Bot. 2015, 39, 1060–1066. [Google Scholar] [CrossRef]
  46. Sugio, A.; Yang, B.; Zhu, T.; White, F.F. Two type III effector genes of Xanthomonas oryzae pv. oryzae control the induction of the host genes OsTFIIAgamma1 and OsTFX1 during bacterial blight of rice. Proc. Natl. Acad. Sci. USA 2007, 104, 10720–10725. [Google Scholar] [CrossRef]
  47. Zou, H.; Zhao, W.; Zhang, X.; Han, Y.; Zou, L.; Chen, G. Identification of an avirulence gene, avrxa5, from the rice pathogen Xanthomonas oryzae pv. oryzae. Sci. China Life Sci. 2010, 53, 1440–1449. [Google Scholar] [CrossRef]
  48. Jiang, G.H.; Xia, Z.H.; Zhou, Y.L.; Wan, J.; Li, D.Y.; Chen, R.S.; Zhai, W.X.; Zhu, L.H. Testifying the rice bacterial blight resistance gene xa5 by genetic complementation and further analyzing xa5 (Xa5) in comparison with its homolog TFIIAgamma1. Mol. Genet. Genom. 2006, 275, 354–366. [Google Scholar] [CrossRef]
  49. Yang, B.; Sugio, A.; White, F.F. Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc. Natl. Acad. Sci. USA 2006, 103, 10503–10508. [Google Scholar] [CrossRef]
  50. Antony, G.; Zhou, J.; Huang, S.; Li, T.; Liu, B.; White, F.; Yang, B. Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. Plant Cell 2010, 22, 3864–3876. [Google Scholar] [CrossRef]
  51. Yu, Y.; Streubel, J.; Balzergue, S.; Champion, A.; Boch, J.; Koebnik, R.; Feng, J.; Verdier, V.; Szurek, B. Colonization of rice leaf blades by an African strain of Xanthomonas oryzae pv. oryzae depends on a new TAL effector that induces the rice nodulin-3 Os11N3 gene. Mol. Plant Microbe Interact. 2011, 24, 1102–1113. [Google Scholar] [CrossRef]
  52. Streubel, J.; Pesce, C.; Hutin, M.; Koebnik, R.; Boch, J.; Szurek, B. Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. New Phytol. 2013, 200, 808–819. [Google Scholar] [CrossRef] [PubMed]
  53. Xu, Z.; Xu, X.; Gong, Q.; Li, Z.; Li, Y.; Wang, S.; Yang, Y.; Ma, W.; Liu, L.; Zhu, B.; et al. Engineering Broad-Spectrum Bacterial Blight Resistance by Simultaneously Disrupting Variable TALE-Binding Elements of Multiple Susceptibility Genes in Rice. Mol. Plant 2019, 12, 1434–1446. [Google Scholar] [CrossRef] [PubMed]
  54. Yuan, M.; Ke, Y.; Huang, R.; Ma, L.; Yang, Z.; Chu, Z.; Xiao, J.; Li, X.; Wang, S. A host basal transcription factor is a key component for infection of rice by TALE-carrying bacteria. Elife 2016, 5, e19605. [Google Scholar] [CrossRef]
  55. Tran, T.T.; Pérez-Quintero, A.L.; Wonni, I.; Carpenter, S.C.D.; Yu, Y.; Wang, L.; Leach, J.E.; Verdier, V.; Cunnac, S.; Bogdanove, A.J.; et al. Functional analysis of African Xanthomonas oryzae pv. oryzae TALomes reveals a new susceptibility gene in bacterial leaf blight of rice. PLoS Pathog. 2018, 14, e1007092. [Google Scholar] [CrossRef]
  56. Zhao, B.; Lin, X.; Poland, J.; Trick, H.; Leach, J.; Hulbert, S. A maize resistance gene functions against bacterial streak disease in rice. Proc. Natl. Acad. Sci. USA 2005, 102, 15383–15388. [Google Scholar] [CrossRef]
  57. Zhou, Y.L.; Xu, M.R.; Zhao, M.F.; Xie, X.W.; Zhu, L.H.; Fu, B.Y.; Li, Z.K. Genome-wide gene responses in a transgenic rice line carrying the maize resistance gene Rxo1 to the rice bacterial streak pathogen, Xanthomonas oryzae pv. oryzicola. BMC Genom. 2010, 11, 78. [Google Scholar] [CrossRef] [PubMed]
  58. Read, A.C.; Rinaldi, F.C.; Hutin, M.; He, Y.Q.; Triplett, L.R.; Bogdanove, A.J. Suppression of Xo1-Mediated Disease Resistance in Rice by a Truncated, Non-DNA-Binding TAL Effector of Xanthomonas oryzae. Front. Plant Sci. 2016, 7, 1516. [Google Scholar] [CrossRef]
  59. Triplett, L.R.; Cohen, S.P.; Heffelfinger, C.; Schmidt, C.L.; Huerta, A.I.; Tekete, C.; Verdier, V.; Bogdanove, A.J.; Leach, J.E. A resistance locus in the American heirloom rice variety Carolina Gold Select is triggered by TAL effectors with diverse predicted targets and is effective against African strains of Xanthomonas oryzae pv. oryzicola. Plant J. 2016, 87, 472–483. [Google Scholar] [CrossRef]
  60. Read, A.C.; Hutin, M.; Moscou, M.J.; Rinaldi, F.C.; Bogdanove, A.J. Cloning of the Rice Xo1 Resistance Gene and Interaction of the Xo1 Protein with the Defense-Suppressing Xanthomonas Effector Tal2h. Mol. Plant Microbe Interact. 2020, 33, 1189–1195. [Google Scholar] [CrossRef]
  61. Chen, L.Q.; Hou, B.H.; Lalonde, S.; Takanaga, H.; Hartung, M.L.; Qu, X.Q.; Guo, W.J.; Kim, J.G.; Underwood, W.; Chaudhuri, B.; et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 2010, 468, 527–532. [Google Scholar] [CrossRef]
  62. Yuan, T.; Li, X.; Xiao, J.; Wang, S. Characterization of Xanthomonas oryzae-responsive cis-acting element in the promoter of rice race-specific susceptibility gene Xa13. Mol. Plant 2011, 4, 300–309. [Google Scholar] [CrossRef] [PubMed]
  63. Blanvillain-Baufumé, S.; Reschke, M.; Solé, M.; Auguy, F.; Doucoure, H.; Szurek, B.; Meynard, D.; Portefaix, M.; Cunnac, S.; Guiderdoni, E.; et al. Targeted promoter editing for rice resistance to Xanthomonas oryzae pv. oryzae reveals differential activities for SWEET14-inducing TAL effectors. Plant Biotechnol. J. 2017, 15, 306–317. [Google Scholar] [CrossRef] [PubMed]
  64. Liu, Q.; Yuan, M.; Zhou, Y.; Li, X.; Xiao, J.; Wang, S. A paralog of the MtN3/saliva family recessively confers race-specific resistance to Xanthomonas oryzae in rice. Plant Cell Env. 2011, 34, 1958–1969. [Google Scholar] [CrossRef] [PubMed]
  65. Chu, Z.; Yuan, M.; Yao, J.; Ge, X.; Yuan, B.; Xu, C.; Li, X.; Fu, B.; Li, Z.; Bennetzen, J.L.; et al. Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes. Dev. 2006, 20, 1250–1255. [Google Scholar] [CrossRef]
  66. Ma, W.; Zou, L.; Zhiyuan, J.I.; Xiameng, X.U.; Zhengyin, X.U.; Yang, Y.; Alfano, J.R.; Chen, G. Xanthomonas oryzae pv. oryzae TALE proteins recruit OsTFIIAγ1 to compensate for the absence of OsTFIIAγ5 in bacterial blight in rice. Mol. Plant Pathol. 2018, 19, 2248–2262. [Google Scholar] [CrossRef]
  67. Xu, X.; Xu, Z.; Ma, W.; Haq, F.; Li, Y.; Shah, S.M.A.; Zhu, B.; Zhu, C.; Zou, L.; Chen, G. TALE-triggered and iTALE-suppressed Xa1-mediated resistance to bacterial blight is independent of rice transcription factor subunits OsTFIIAγ1 or OsTFIIAγ5. J. Exp. Bot. 2021, 72, 3249–3262. [Google Scholar] [CrossRef]
  68. Xie, X.; Chen, Z.; Cao, J.; Guan, H.; Lin, D.; Li, C.; Lan, T.; Duan, Y.; Mao, D.; Wu, W. Toward the positional cloning of qBlsr5a, a QTL underlying resistance to bacterial leaf streak, using overlapping sub-CSSLs in rice. PLoS ONE 2014, 9, e95751. [Google Scholar] [CrossRef]
  69. Cernadas, R.A.; Doyle, E.L.; Niño-Liu, D.O.; Wilkins, K.E.; Bancroft, T.; Wang, L.; Schmidt, C.L.; Caldo, R.; Yang, B.; White, F.F.; et al. Code-assisted discovery of TAL effector targets in bacterial leaf streak of rice reveals contrast with bacterial blight and a novel susceptibility gene. PLoS Pathog. 2014, 10, e1003972. [Google Scholar] [CrossRef]
  70. Cheong, H.; Kim, C.Y.; Jeon, J.S.; Lee, B.M.; Sun Moon, J.; Hwang, I. Xanthomonas oryzae pv. oryzae type III effector XopN targets OsVOZ2 and a putative thiamine synthase as a virulence factor in rice. PLoS ONE 2013, 8, e73346. [Google Scholar] [CrossRef]
  71. Liao, Z.-X.; Li, J.-Y.; Mo, X.-Y.; Ni, Z.; Jiang, W.; He, Y.-Q.; Huang, S. Type III effectors xopN and avrBS2 contribute to the virulence of Xanthomonas oryzae pv. oryzicola strain GX01. Res. Microbiol. 2020, 171, 102–106. [Google Scholar] [CrossRef]
  72. Wang, S.; Sun, J.; Fan, F.; Tan, Z.; Zou, Y.; Lu, D. A Xanthomonas oryzae pv. oryzae effector, XopR, associates with receptor-like cytoplasmic kinases and suppresses PAMP-triggered stomatal closure. Sci. China Life Sci. 2016, 59, 897–905. [Google Scholar] [CrossRef] [PubMed]
  73. Yamaguchi, K.; Yamada, K.; Ishikawa, K.; Yoshimura, S.; Hayashi, N.; Uchihashi, K.; Ishihama, N.; Kishi-Kaboshi, M.; Takahashi, A.; Tsuge, S.; et al. A receptor-like cytoplasmic kinase targeted by a plant pathogen effector is directly phosphorylated by the chitin receptor and mediates rice immunity. Cell Host Microbe 2013, 13, 347–357. [Google Scholar] [CrossRef]
  74. Yamaguchi, K.; Nakamura, Y.; Ishikawa, K.; Yoshimura, Y.; Tsuge, S.; Kawasaki, T. Suppression of rice immunity by Xanthomonas oryzae type III effector Xoo2875. Biosci. Biotechnol. Biochem. 2013, 77, 796–801. [Google Scholar] [CrossRef] [PubMed]
  75. Qin, J.; Zhou, X.; Sun, L.; Wang, K.; Yang, F.; Liao, H.; Rong, W.; Yin, J.; Chen, H.; Chen, X.; et al. The Xanthomonas effector XopK harbours E3 ubiquitin-ligase activity that is required for virulence. New Phytol. 2018, 220, 219–231. [Google Scholar] [CrossRef] [PubMed]
  76. Ishikawa, K.; Yamaguchi, K.; Sakamoto, K.; Yoshimura, S.; Inoue, K.; Tsuge, S.; Kojima, C.; Kawasaki, T. Bacterial effector modulation of host E3 ligase activity suppresses PAMP-triggered immunity in rice. Nat. Commun. 2014, 5, 5430. [Google Scholar] [CrossRef]
  77. Ma, W.; Xu, X.; Cai, L.; Cao, Y.; Haq, F.; Alfano, J.R.; Zhu, B.; Zou, L.; Chen, G. A Xanthomonas oryzae type III effector XopL causes cell death through mediating ferredoxin degradation in Nicotiana benthamiana. Phytopathol. Res. 2020, 2, 16. [Google Scholar] [CrossRef]
  78. Ji, H.; Li, T.; Li, X.; Li, J.; Yu, J.; Zhang, X.; Liu, D. XopZ and ORP1C cooperate to regulate the virulence of Xanthomonas oryzae pv. oryzae on Nipponbare. Plant Signal. Behav. 2022, 17, 2035126. [Google Scholar] [CrossRef]
  79. Fiehn, O.; Kopka, J.; Dörmann, P.; Altmann, T.; Trethewey, R.N.; Willmitzer, L. Metabolite profiling for plant functional genomics. Nat. Biotechnol. 2000, 18, 1157–1161. [Google Scholar] [CrossRef]
  80. Finkelstein, D.; Ewing, R.; Gollub, J.; Sterky, F.; Cherry, J.M.; Somerville, S. Microarray data quality analysis: Lessons from the AFGC project. Arabidopsis Functional Genomics Consortium. Plant Mol. Biol. 2002, 48, 119–131. [Google Scholar] [CrossRef]
  81. Henikoff, S.; Comai, L. Single-nucleotide mutations for plant functional genomics. Annu. Rev. Plant Biol. 2003, 54, 375–401. [Google Scholar] [CrossRef]
  82. Sana, T.R.; Fischer, S.; Wohlgemuth, G.; Katrekar, A.; Jung, K.H.; Ronald, P.C.; Fiehn, O. Metabolomic and transcriptomic analysis of the rice response to the bacterial blight pathogen Xanthomonas oryzae pv. oryzae. Metabolomics 2010, 6, 451–465. [Google Scholar] [CrossRef]
  83. Jiang, N.; Fu, J.; Zeng, Q.; Liang, Y.; Shi, Y.; Li, Z.; Xiao, Y.; He, Z.; Wu, Y.; Long, Y.; et al. Genome-wide association mapping for resistance to bacterial blight and bacterial leaf streak in rice. Planta 2021, 253, 94. [Google Scholar] [CrossRef] [PubMed]
  84. Lu, J.; Wang, C.; Zeng, D.; Li, J.; Shi, X.; Shi, Y.; Zhou, Y. Genome-Wide Association Study Dissects Resistance Loci against Bacterial Blight in a Diverse Rice Panel from the 3000 Rice Genomes Project. Rice 2021, 14, 22. [Google Scholar] [CrossRef] [PubMed]
  85. Zhang, F.; Wu, Z.C.; Wang, M.M.; Zhang, F.; Dingkuhn, M.; Xu, J.L.; Zhou, Y.L.; Li, Z.K. Genome-wide association analysis identifies resistance loci for bacterial blight in a diverse collection of indica rice germplasm. PLoS ONE 2017, 12, e0174598. [Google Scholar] [CrossRef]
  86. Wu, G.; Zhang, Y.; Wang, B.; Li, K.; Lou, Y.; Zhao, Y.; Liu, F. Proteomic and Transcriptomic Analyses Provide Novel Insights into the Crucial Roles of Host-Induced Carbohydrate Metabolism Enzymes in Xanthomonas oryzae pv. oryzae Virulence and Rice-Xoo Interaction. Rice 2021, 14, 57. [Google Scholar] [CrossRef] [PubMed]
  87. Zhao, Y.; Qian, G.; Yin, F.; Fan, J.; Zhai, Z.; Liu, C.; Hu, B.; Liu, F. Proteomic analysis of the regulatory function of DSF-dependent quorum sensing in Xanthomonas oryzae pv. oryzicola. Microb. Pathog. 2011, 50, 48–55. [Google Scholar] [CrossRef]
  88. Zhang, F.; Zhang, F.; Huang, L.; Zeng, D.; Cruz, C.V.; Li, Z.; Zhou, Y. Comparative proteomic analysis reveals novel insights into the interaction between rice and Xanthomonas oryzae pv. oryzae. BMC Plant Biol. 2020, 20, 563. [Google Scholar] [CrossRef]
  89. Bi, Y.; Yu, Y.; Mao, S.; Wu, T.; Wang, T.; Zhou, Y.; Xie, K.; Zhang, H.; Liu, L.; Chu, Z. Comparative transcriptomic profiling of the two-stage response of rice to Xanthomonas oryzae pv. oryzicola interaction with two different pathogenic strains. BMC Plant Biol. 2024, 24, 347. [Google Scholar] [CrossRef]
  90. Sahu, A.; Das, A.; Saikia, K.; Barah, P. Temperature differentially modulates the transcriptome response in Oryza sativa to Xanthomonas oryzae pv. oryzae infection. Genomics 2020, 112, 4842–4852. [Google Scholar] [CrossRef]
  91. Das, P.P.; Kumar, A.; Mohammed, M.; Bhati, K.; Babu, K.R.; Bhandari, K.P.; Sundaram, R.M.; Ghazi, I.A. Comparative metabolites analysis of resistant, susceptible and wild rice species in response to bacterial blight disease. BMC Plant Biol. 2025, 25, 178. [Google Scholar] [CrossRef]
  92. Chen, P.; Wang, J.; Liu, Q.; Liu, J.; Mo, Q.; Sun, B.; Mao, X.; Jiang, L.; Zhang, J.; Lv, S.; et al. Transcriptome and Metabolome Analysis of Rice Cultivar CBB23 after Inoculation by Xanthomonas oryzae pv. oryzae Strains AH28 and PXO99(A). Plants 2024, 13, 1411. [Google Scholar] [CrossRef] [PubMed]
  93. Vo, K.T.X.; Rahman, M.M.; Rahman, M.M.; Trinh, K.T.T.; Kim, S.T.; Jeon, J.S. Proteomics and Metabolomics Studies on the Biotic Stress Responses of Rice: An Update. Rice 2021, 14, 30. [Google Scholar] [CrossRef]
  94. Erb, M.; Kliebenstein, D.J. Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy. Plant Physiol. 2020, 184, 39–52. [Google Scholar] [CrossRef] [PubMed]
  95. Erb, M. Volatiles as inducers and suppressors of plant defense and immunity-origins, specificity, perception and signaling. Curr. Opin. Plant Biol. 2018, 44, 117–121. [Google Scholar] [CrossRef] [PubMed]
  96. Bouwmeester, H.; Schuurink, R.C.; Bleeker, P.M.; Schiestl, F. The role of volatiles in plant communication. Plant J. 2019, 100, 892–907. [Google Scholar] [CrossRef]
  97. Yang, W.; Zhang, L.; Yang, Y.; Xiang, H.; Yang, P. Plant secondary metabolites-mediated plant defense against bacteria and fungi pathogens. Plant Physiol. Biochem. 2024, 217, 109224. [Google Scholar] [CrossRef]
  98. Yang, Y.; Zhou, Y.; Sun, J.; Liang, W.; Chen, X.; Wang, X.; Zhou, J.; Yu, C.; Wang, J.; Wu, S.; et al. Research Progress on Cloning and Function of Xa Genes Against Rice Bacterial Blight. Front. Plant Sci. 2022, 13, 847199. [Google Scholar]
  99. Hou, Y.; Liang, Y.; Yang, C.; Ji, Z.; Zeng, Y.; Li, G.; E, Z. Complete Genomic Sequence of Xanthomonas oryzae pv. oryzae Strain, LA20, for Studying Resurgence of Rice Bacterial Blight in the Yangtze River Region, China. Int. J. Mol. Sci. 2023, 24, 8132. [Google Scholar] [CrossRef]
  100. Li, Z.G.; He, F.; Zhang, Z.; Peng, Y.L. Prediction of protein-protein interactions between Ralstonia solanacearum and Arabidopsis thaliana. Amino Acids 2012, 42, 2363–2371. [Google Scholar] [CrossRef]
  101. Gupta, A.; Liu, B.; Chen, Q.J.; Yang, B. High-efficiency prime editing enables new strategies for broad-spectrum resistance to bacterial blight of rice. Plant Biotechnol. J. 2023, 21, 1454–1464. [Google Scholar] [CrossRef]
  102. Gupta, A.; Liu, B.; Raza, S.; Chen, Q.-J.; Yang, B. Modularly assembled multiplex prime editors for simultaneous editing of agronomically important genes in rice. Plant Commun. 2024, 5, 100741. [Google Scholar] [CrossRef]
  103. Ni, Z.; Cao, Y.; Jin, X.; Fu, Z.; Li, J.; Mo, X.; He, Y.; Tang, J.; Huang, S. Engineering Resistance to Bacterial Blight and Bacterial Leaf Streak in Rice. Rice 2021, 14, 38. [Google Scholar] [CrossRef] [PubMed]
  104. Duy, P.N.; Lan, D.T.; Pham Thu, H.; Thi Thu, H.P.; Nguyen Thanh, H.; Pham, N.P.; Auguy, F.; Bui Thi Thu, H.; Manh, T.B.; Cunnac, S.; et al. Improved bacterial leaf blight disease resistance in the major elite Vietnamese rice cultivar TBR225 via editing of the OsSWEET14 promoter. PLoS ONE 2021, 16, e0255470. [Google Scholar] [CrossRef] [PubMed]
  105. Römer, P.; Jordan, T.; Lahaye, T. Identification and application of a DNA-based marker that is diagnostic for the pepper (Capsicum annuum) bacterial spot resistance gene Bs3. Plant Breed. 2010, 129, 737–740. [Google Scholar] [CrossRef]
  106. Huang, F.; He, N.; Yu, M.; Li, D.; Yang, D. Identification and fine mapping of a new bacterial blight resistance gene, Xa43(t), in Zhangpu wild rice (Oryza rufipogon). Plant Biol. 2023, 25, 433–439. [Google Scholar] [CrossRef]
  107. Hummel, A.W.; Doyle, E.L.; Bogdanove, A.J. Addition of transcription activator-like effector binding sites to a pathogen strain-specific rice bacterial blight resistance gene makes it effective against additional strains and against bacterial leaf streak. New Phytol. 2012, 195, 883–893. [Google Scholar] [CrossRef] [PubMed]
  108. Zeng, X.; Tian, D.; Gu, K.; Zhou, Z.; Yang, X.; Luo, Y.; White, F.F.; Yin, Z. Genetic engineering of the Xa10 promoter for broad-spectrum and durable resistance to Xanthomonas oryzae pv. oryzae. Plant Biotechnol. J. 2015, 13, 993–1001. [Google Scholar] [CrossRef]
  109. Zheng, C.; Liu, Y.; Sun, F.; Zhao, L.; Zhang, L. Predicting Protein-Protein Interactions Between Rice and Blast Fungus Using Structure-Based Approaches. Front. Plant Sci. 2021, 12, 690124. [Google Scholar] [CrossRef]
  110. Mukhtar, M.S.; Carvunis, A.R.; Dreze, M.; Epple, P.; Steinbrenner, J.; Moore, J.; Tasan, M.; Galli, M.; Hao, T.; Nishimura, M.T.; et al. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 2011, 333, 596–601. [Google Scholar] [CrossRef]
  111. Weßling, R.; Epple, P.; Altmann, S.; He, Y.; Yang, L.; Henz, S.R.; McDonald, N.; Wiley, K.; Bader, K.C.; Gläßer, C.; et al. Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life. Cell Host Microbe 2014, 16, 364–375. [Google Scholar] [CrossRef]
  112. Cao, F.Y.; Khan, M.; Taniguchi, M.; Mirmiran, A.; Moeder, W.; Lumba, S.; Yoshioka, K.; Desveaux, D. A host-pathogen interactome uncovers phytopathogenic strategies to manipulate plant ABA responses. Plant J. 2019, 100, 187–198. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Infection modes of Xoo and Xoc in rice. (A) Schematic representation of the infection modes of Xoo and Xoc in rice leaf tissue. (B) Symptoms of BB and BLS caused by Xoo and Xoc, respectively. (C) The magnified images of BB and BLS symptoms.
Figure 1. Infection modes of Xoo and Xoc in rice. (A) Schematic representation of the infection modes of Xoo and Xoc in rice leaf tissue. (B) Symptoms of BB and BLS caused by Xoo and Xoc, respectively. (C) The magnified images of BB and BLS symptoms.
Biology 14 00471 g001
Figure 2. Structural features of TALEs and non-TALEs.
Figure 2. Structural features of TALEs and non-TALEs.
Biology 14 00471 g002
Figure 3. Multi-omics research and modern biotechnology strategies in rice–Xoo/Xoc interactions. (A) Application of four omics approaches (genomics, transcriptomics, proteomics, and metabolomics) in rice–Xoo/Xoc interactions. (B) Utilization of modern molecular biotechnology for resistance breeding against Xoo/Xoc.
Figure 3. Multi-omics research and modern biotechnology strategies in rice–Xoo/Xoc interactions. (A) Application of four omics approaches (genomics, transcriptomics, proteomics, and metabolomics) in rice–Xoo/Xoc interactions. (B) Utilization of modern molecular biotechnology for resistance breeding against Xoo/Xoc.
Biology 14 00471 g003
Table 1. Rice genes targeted by TALEs.
Table 1. Rice genes targeted by TALEs.
Tale-Targeted
(R/S Gene)
Encoding ProductsMatched TALEsReferences
ResistanceXa1
Xo1
Xa2/31
Xa14
Xa45
NLRMultiple TALEs,
iTALEs/truncTALE
[19,30,33,40]
Xa7ExecutorAvrXa7, PthXo3[37,41]
Xa10ExecutorAvrXa10[35]
Xa23ExecutorAvrXa23[42]
Xa27executorAvrXa27[34]
xa13Sweet transporterPthXo1[43]
xa25Sweet transporterPthXo2[44]
xa41Sweet transporterAvrXa7,
PthXo3, Tal5, TalC
[45]
xa5TFIIA transcription
factor
AvrXa5, PthXo7[46,47,48]
SusceptibilityOsSWEET11(Xa13/Os8N3)Sweet transporterPthXo1[49]
OsSWEET14(Xa41/Os11N3)Sweet transporterAvrXa7,
PthXo3,
TalC, Tal5
[50,51,52]
OsSWEET13(Xa25/Os12N3)Sweet transporterPthXo2[44,53]
OsSWEET12Sweet transporterArtTAL12[52]
OsSWEET15Sweet transporterArtTAL15[52]
OsTFIIAγ5Gamma subunit of rice basal transcription factorMultiple TALEs[54]
OsTFIIAγ1Gamma subunit of rice basal transcription factorPthXo7[46]
OsTFX1bZIP transcription factorPthXo6
TalBMAl1
[46,55]
OsERF#123AP2/ERF
transcription factor
TalBMAl1[55]
OsSULTR3;6Sulfate transporterTal2g[56,57]
Table 2. Rice genes interacted with non-TALEs.
Table 2. Rice genes interacted with non-TALEs.
Rice Genes
(Interaction Genes)
Encoding ProductsMatched TALEsReferences
OsVOZ2, OsXNP Vascular plant one zinc finger protein 2,
putative thiamine synthase
XopN[27,70,71]
OsBIK1 Receptor-like kinases XopR[72]
OsRLCK185Receptor-like kinaseXopY[74]
OsBAK1 Receptor-like kinase XopAA[74]
OsSERK1Somatic embryogenic receptor kinase 2XopK[75]
OsPUB44Ubiquitin E3 ligase XopP[76]
NbFdFerredoxin proteinXopL[77]
OsORP1COxysterol-binding related proteinXopZ[78]
Table 3. Holistic analysis of rice–Xoo/Xoc interactions throuth multi-omics.
Table 3. Holistic analysis of rice–Xoo/Xoc interactions throuth multi-omics.
OmicsRice VarietiesXanthomonas oryzaeMain ConclusionReferences
Genomics 895 accessions from the 3K RGP Xoo
Xoc
7 and 77 loci linked to resistance for Xoo and Xoc, respectively, were identified[83]
Genomics 340 accessions from the 3K RGP Xoo11 loci linked to resistance against Xoo
were identified
[84]
Genomics172 indica riceXooChromosomes 11 and 12 were important for the evolution of rice resistance for Xoo[85]
Proteomics IR24 XooCarbohydrate-metabolizing enzymes play a key roles in rice–Xoo interactions[86]
ProteomicsShanyou63XocDSF may play an important role in Xoc virulence and growth[87]
Proteomics H471 and HHZ XooPhytoalexin and SA signaling pathways were activated faster in the incompatible interaction than in the compatible interaction[88]
Transcriptomics ZH11 XocEarly PTI: conserved DEGs drive basal defense; Late ETI/ETS: TALE targets and specialized DR genes prevail[89]
TranscriptomicsIR24XooThe ΔxanA and Δimp mutants dysregulated photosynthesis, redox balance, and secondary metabolism[86]
TranscriptomicsIR24XooRice plants tend to shift their focus from defensive responses to growth and reproduction at high temperatures[90]
MetabolomicsIRBB27, Oryza minuta-CG154, IR24 XooKey metabolites such as flavonoids, terpenes, and phenolic compounds showed significantly higher levels in resistant varieties[91]
MetabolomicsCBB23XooMetabolites such as alkaloids and amino acid
were involved in rice defense against Xoo
[92]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Qi, Y.; Rao, Q.; Lu, C.; Gong, J.; Hou, Y. Recent Progress in Rice–Xanthomonas oryzae Interactions. Biology 2025, 14, 471. https://doi.org/10.3390/biology14050471

AMA Style

Qi Y, Rao Q, Lu C, Gong J, Hou Y. Recent Progress in Rice–Xanthomonas oryzae Interactions. Biology. 2025; 14(5):471. https://doi.org/10.3390/biology14050471

Chicago/Turabian Style

Qi, Yuting, Qiong Rao, Chenglong Lu, Junyi Gong, and Yuxuan Hou. 2025. "Recent Progress in Rice–Xanthomonas oryzae Interactions" Biology 14, no. 5: 471. https://doi.org/10.3390/biology14050471

APA Style

Qi, Y., Rao, Q., Lu, C., Gong, J., & Hou, Y. (2025). Recent Progress in Rice–Xanthomonas oryzae Interactions. Biology, 14(5), 471. https://doi.org/10.3390/biology14050471

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop