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Review

Progress in the Management of Rice Blast Disease: The Role of Avirulence and Resistance Genes through Gene-for-Gene Interactions

by
Muhammad Usama Younas
1,*,
Irshad Ahmad
2,
Muhammad Qasim
3,
Zainab Ijaz
2,
Nimra Rajput
1,
Saima Parveen Memon
4,
Waqar UL Zaman
2,
Xiaohong Jiang
1,
Yi Zhang
1 and
Shimin Zuo
1,2,*
1
Key Laboratory of Plant Functional Genomics of the Ministry of Education, Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding, Agricultural College of Yangzhou University, Yangzhou 225009, China
2
Joint International Research Laboratory of Agriculture and Agri-Product Safety of the Ministry of Education of China, Yangzhou University, Yangzhou 225009, China
3
Microelement Research Center, College of Resources and Agricultural University, Wuhan 430070, China
4
Key Laboratory of Crop Cultivation and Tillage Agricultural College of Yangzhou University, Yangzhou 225009, China
*
Authors to whom correspondence should be addressed.
Agronomy 2024, 14(1), 163; https://doi.org/10.3390/agronomy14010163
Submission received: 17 December 2023 / Revised: 8 January 2024 / Accepted: 9 January 2024 / Published: 11 January 2024
(This article belongs to the Section Pest and Disease Management)
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Abstract

:
Rice is a vital component in the diets of many people worldwide, supplying necessary calories for subsistence. Nevertheless, the yield of this crucial agricultural crop is consistently hindered by a range of biotic stresses. Out of these, rice blast, claused mainly by the fungus Magnaporthe oryzae, poses a significant menace to worldwide rice cultivation as well as yield in recent years. The consequences are particularly crucial given the current climate change challenges. In recent decades, substantial progress has been achieved in the development of efficient ways to manage rice blast disease. These procedures entail using a variety of rice genetic resources to find, map, clone, and functionally validate individual resistance (R) genes and quantitative trait loci (QTLs) that provide long-lasting resistance to rice blast disease. Moreover, the replication and practical confirmation of homologous avirulence (Avr) genes in various M. oryzae strains have been crucial in comprehending the fundamental molecular mechanisms of host–pathogen interactions. This article offers a thorough examination of the cloning and functional verification of different R genes and QTLs linked to resistance against rice blast disease. The complex interplay between R–Avr pairings, which contributes to the development of resistance against rice blast throughout a wide range, is thoroughly explained. Finally, this study explores the most recent progress in next-generation sequencing (NGS) and genome editing technologies (GETs), examining their potential uses in improving the treatment of rice blast disease.

1. Introduction

Rice (Oryza sativa L.) is vital to human existence, particularly in Asia. A substantial portion of the population in this region relies on rice consumption, either directly or indirectly, to meet their caloric needs. For thousands of years, rice has laid the foundations for the establishment of ancient civilizations, cultures, economies, and diets for billions of people. The International Year of Rice was designated by the United Nations Organization (UNO) in 2002, recognizing the significance of rice as a primary cereal crop in ensuring global food security [1]. Rice is a member of the Poaceae family, commonly known as the grass family, and is well-known for its cultivation of essential cereal crops such as wheat, barley, and maize. Rice exists in two forms: wild and domesticated. Two well-known species, Oryza sativa and Oryza glaberrima, belong to the domesticated rice category. Rice is believed to have originated in tropical and subtropical parts of South Asia and Southeast Africa [2]. The wild type of rice was initially cultivated without an aquatic environment, but later mutations allowed it to specifically grow in submerged conditions. Currently, rice can be grown in diverse environments, but humid, warm, and wet conditions enhance its growth and yield.
Rice blast, caused by the fungus Magnaporthe oryzae, is one of the top three most important diseases that impact rice yield worldwide. Annually, it presents a significant menace to rice cultivation, leading to output declines ranging from 10% to 30% in average years and up to a drastic 50% decrease in more severe cases [3]. Rice blast occurs during the reproductive phase of rice and can be classified into many types, such as seedling blast, leaf blast, node blast, panicle blast, and grain blast, depending on when and where the infestation occurs on the rice plant. Panicle blast specifically arises as the most significant menace to rice production [4]. For disease prevention, plants adapt different resistance mechanisms, such as horizontal or vertical resistance mechanisms. Plants with horizontal resistance have a wide, non-specific defense against a range of infections, as this defense heavily relies on several genes for long-lasting protection against diseases [5]. Vertical resistance is powerful, but acts as a transient barrier because viruses may readily overcome it via mutation. It is based on a unique gene-for-gene interaction between the host and the pathogen [6]. The co-evolution of host–pathogen interactions is akin to a continuous arms race in which both sides continuously evolve new offensive and defensive tactics, which results in the generation of new pathogen strains and resistant plant types in a dynamic, evolutionary struggle [7]. Choosing resistant rice types through meticulous selection and sensible application is the most cost-effective and efficient method of blast disease control, in contrast to the disadvantages of using chemical fungicides. Consequently, there has been a shift in focus towards the identification of genes that confer resistance to rice blast disease (R genes), which is essential for the production of robust cultivars [8]. Moreover, the use of genetic approaches in rice crop protection provides targeted and sustainable solutions that minimize chemical usage and increase crop resistance to a variety of diseases [9].
In summary, this review will delve into the resistance conferred by R genes against rice blast, shedding light on the groundbreaking research in this area. As we conclude this introduction, it is essential to highlight that, while significant progress has been made, there is still work to be undertaken in understanding the intricacies of R gene-mediated resistance against rice blast. This work will provide valuable insights into the ongoing challenges and future directions of research in this field.

2. Rice Blast and the Pathogen

The growth and productivity of rice are subject to ongoing challenges posed by a range of biotic and abiotic stressors. The cultivation of rice encounters significant challenges resulting from a confluence of abiotic factors, including drought, salinity, heat, and nutritional deficiencies, as well as biotic stresses in the form of insect infestations and viral, bacterial, and fungal infections. One of the biotic factors that significantly impacts rice production is a fungal disease referred to as rice blast. The pathogen Magnaporthe oryzae is accountable for the occurrence of rice blast, a disease that leads to annual reductions in crop output ranging from 10% to 30%. In certain cases, like pandemics, the possibility of even more substantial losses exists [10]. The life cycle of M. oryzae is described in (Figure 1).
Several factors contribute to the increased incidence of rice blast: the prevailing climatic conditions encompass elevated humidity above 80%, overcast skies accompanied by precipitation, frequent rainfall events, relatively low temperatures between 15 and 25%, windy conditions with constant dew, excessive fertilizer application, and the existence of multiple pathogenic strains of the causal pathogen [11,12]. During pandemic years, yield losses can approach complete crop loss (100%) [13,14]. Rice blast affects various parts of the rice plant, from the leaf blades to the collar, and from the neck to the panicles [15,16]. The initial infection of the pathogen is characterized by lesions or brown spots on the upper surface of the leaf tissue, which later develop into spindle-shaped structures [17]. The margins of the infection turn brown, while the center becomes grayish. These lesions gradually extend, covering the entire leaf surface and ultimately resulting in the death of the entire leaf [18].
Rice blast disease has spread to over 85 countries [19,20]. There are over fifty species of grasses and sedges containing the Magnaporthe oryzae species complex, including oats (Avena sativa L.), rice (Oryza sativa L.), maize (Zea mays L.), wheat (Triticum aestivum L.), oats (Avena sativa L.), barley (Hordeum vulgare L.), rye (Secale cereale L.), ornamental and weed grasses, finger millet (Eleusine corocana L.), and perennial ryegrass (Lolium perenne L.) [21,22]. It infects a diverse array of species. While extensive research has been conducted on the life cycle of Magnaporthe blast in its primary host, rice, there is still a need for additional investigations into its non-host range and the possibility of its occurrence in hosts other than rice.

3. Chemical Control of Rice Blast

Chemicals, particularly fungicides, represent the most convenient and widely used method for the control and management of rice blast disease. Japan has emerged as a paradigmatic example of the effective and widespread utilization of chemical pesticides in the battle against rice blast disease. Initially, copper fungicides were the most successful and effective means of controlling rice blast in Japan [23,24]. Nevertheless, it quickly became apparent that copper fungicides exhibited phytotoxicity and had detrimental impacts on both human health and soil microbiology. Diligent endeavors were undertaken to explore alternate options that offer enhanced safety in comparison to copper fungicides [25].
Subsequently, a combination of phenylmercuric acetate (PMA) and copper fungicides was found to be more effective in managing rice blast, and was less toxic to human health and the rice plant compared to copper alone [26]. Later, a new group of fungicides, mainly organo-phosphorous compounds, was tested and widely applied in rice blast disease management programs in Japan [27]. However, reports confirmed the emergence of resistance to these fungicides in M. oryzae in the late 1970s. It was suggested that the large-scale applications of different fungicides or combinations thereof in rotations, rather than the sole use of a particular fungicide, is the most effective strategy for rice blast management [28]. This strategy not only proved effective but also reduced the chances of the emergence of highly resistant populations. These efforts paved the way for the discovery of novel groups of fungicides with different mechanisms of action against the rice blast pathogen, such as ergosterol biosynthesis inhibitors (EBIs), melanin inhibitors, and anti-mitotic compounds [29,30].
The widespread utilization of various contemporary fungicides has not only substantially mitigated the detrimental effects caused by M. oryzae strains, but has also tremendously augmented the overall quality and yield capacity of rice production on a global scale. The increased utilization of various fungicides has resulted in the establishment of novel pathogenic strains, hence emphasizing the necessity to explore innovative chemicals for addressing the issue of resistance-breaking strains in rice blast. Magnaporthe oryzae, a fungal pathogen, exhibits the formation of melanized appressoria as a means to successfully breach the resilient cuticle layer of the rice plant [31]. Consequently, research endeavors were directed towards the discovery of melanin biosynthesis inhibitors (MBIs) in order to impede the growth of appressoria and the subsequent penetration of the cuticle layer.
In a general sense, two categories of melanin biosynthesis inhibitors (MBIs), namely scytalone dehydratase (MBI-D) and poly-hydroxynaphthalene reductase (MBI-R), have demonstrated efficacy in suppressing appressorium development inside the rice plant. The second group, which mostly consists of phthalide, pyroquilon, and tricyclazole, has not exhibited any indications of the formation of resistance pathogens despite being widely applied for over three decades. Several resistant mutants have been found and subjected to laboratory-based investigations in China. However, no instances of resistant strains emerging or being isolated in natural environments have been reported [32].

4. Problems with Fungicides

Despite the widespread use of fungicides to manage plant diseases and protect plants, it is essential to acknowledge that they pose a significant threat to both human health and the environment [33]. Using fungicides has been found to have detrimental impacts on the populations of beneficial bacteria and fungi that inhabit the soil [34]. These beneficial microorganisms include Trichoderma, beneficial bacteria, algae, and arbuscular mycorrhizal fungi [35]. Specific microorganisms are essential for the modification of soil structure and fertility, the fixation of nitrogen, the development of nutrient utilization efficiency, and the decomposition of organic matter [36,37].
Soil microbiota represent the first line of microorganisms that directly or indirectly come into contact with toxic substances, including fungicides introduced into the soil [33]. Consequently, soil microbiota can serve as biomarkers for assessing the negative impacts caused by fungicides or other toxic substances introduced into the soil [38,39].

5. Blast Resistance Rice Cultivars as Safer Alternatives

Blast is a major factor contributing to the reduction in global rice yields when it comes to biotic stresses [40]. Fungicides can effectively control rice blast, but come at the cost of environmental damage and risks to farmers’ health. Therefore, new strategies have been developed to manage rice blast disease that are not only environmentally friendly, but also cost-effective and sustainable [41]. One such strategy involves the deployment of rice blast-resistant cultivars to bridge the yield gap caused by different strains of M. oryzae [42].
Significant endeavors have been undertaken in recent decades to ascertain resistance genes capable of effectively countering M. oryzae strains and introducing them into susceptible cultivars through breeding techniques [43]. This methodology enables the utilization of resistant cultivars as more secure alternatives to hazardous fungicides. Furthermore, the development of rice cultivars possessing broad-spectrum resistance against rice blast has been improved through the integration of conventional breeding methods and genetic engineering techniques. A systematic and in-depth study of the rice blast pathogen has contributed to the identification of various single R genes and QTLs conferring rice blast resistance. In agricultural practice, the preference is for broad-spectrum resistance over short-lived resistance.

6. Problems with Blast Resistance Rice Varieties

Currently, the most environmentally sustainable and economical technique for agricultural practitioners is to utilize rice cultivars that carry a single dominant resistance (R) gene while maintaining high yield potential [44]. This strategy operates on the gene-for-gene hypothesis, which underlines the constant battle within plants between the R gene and Avr gene in a particular pathogen strain [45]. The R gene contains five chromosomes on the locus on positions between 10,000,000 bp and 10,050,000 bp; their architecture has an NBS domain (exon 1–exon 3), TIR domain (exon 4–exon 6), LRR domain (exon 7–exon 12), CC domain (exon 13–exon 15), introns interspersed between exons, a promoter region (upstream of exon 1), and enhancer element (upstream of exon 7). The Avr proteins contain three subdomains (P-loop, Kinase-2, and Glutamine–Leucine–Isoleucine (QLI) motifs), a leucine-rich repeat domain (size ranges from 300 to 1000 amino acids), an interleukin -1 receptor domain containing 200–300 amino acids, and a coiled-coil domain containing 100–200 amino acids. An immunological response is triggered when a pathogen’s Avr gene interacts with a particular resistance gene in the host plant. This accurate detection triggers a defensive reaction that often involves localized cell death to stop the spread of the virus. This process is essential to the gene-for-gene theory of vertical resistance. More than 100 blast resistance genes have been identified in rice, the majority of them being monogenic R genes, as seen in (Table 1). However, single-locus resistance controlled by monogenic R genes has shown limitations, often lasting for only 2–4 years [46].

7. Durable Blast Resistance Varieties

The sought-after principal technique involves the utilization of gene combinations and their integration into a single rice cultivar, intending to attain resistance that is both comprehensive in scope and long-lasting in effectiveness. However, this strategy can sometimes result in negative yield penalties when several R genes are stacked in a single cultivar. In some cases, yield was either unaffected or increased through gene pyramiding, but it decreased when tested in fields where multiple strains of M. oryzae were prevalent [59].
Despite the challenges and implications, achieving both broad-spectrum rice blast resistance and high yield remains a top priority for rice breeders worldwide. Although the past few decades have led to the identification of numerous single R genes and QTLs, only a few R or durable resistance (DR) genes have been identified with low or no yield penalty. Of particular interest are likely the genes that strike a balance between immunity and yield, such as the NBS–LRR pair PigmR and PigmS [60], bsr-d1, and bsr-k1, as they all provide broad-spectrum blast resistance without significant yield penalties [61,62].

8. PTI-ETI Interplay as a Mechanism of Defense

Plants have evolved a sophisticated mechanism for detecting and reacting to pathogenic assaults, facilitated by specialized receptors called pattern-recognition receptors (PRRs) [63]. The term used to describe the primary defense mechanism that hinders the invasion of pathogens is known as pattern-triggered immunity (PTI) [64]. This initial response further activates a special class of intracellular receptors known as nucleotide-binding domain leucine-rich repeat-containing receptors (NLRs) [65], leading to effector-triggered immunity (ETI) [66,67]. The primary function of PTI is not only to limit the infiltration of pathogens, but also to sustain a favorable microbial population within the foliage of plants, thereby promoting plant well-being [68,69,70]. Genes included in PTI for pattern recognition receptors are PRR1 and PRR2, calcium signaling with CDPK, the transcription factor WRKY, the defense-related genes PR1 to 3, and secondary metabolism genes PAL and CHS. In the ETI network, R proteins R1 and R2, effector proteins AVR1 and 2, and the signal transduction gene SGT1 are included. They interact with each other through shared MAPD cascades, common transcription factors, by overlapping in gene transcription, or through cell wall modification.
Pathogens, such as fungi, oomycetes, bacteria, and nematodes, produce diverse virulence-inducing chemicals called effectors. Plant pathogens such as oomycetes cause diseases like downy mildew in grapes and late blight in potatoes. Mycoplasmas cause aster yellows and deadly yellowing of the palms, while nematodes cause cyst and root knot infections, which have a serious negative effect on crops including potatoes, tomatoes, and soybeans. These effectors are transported into the plant cell or apoplast to circumvent PTI [71]. Plants exhibit the activation of a secondary layer of immunity (ETI) upon the recognition and subsequent neutralization of pathogen effectors by intracellular NLR proteins within plant cells [72,73]. The hypothesis developed by Dangl in 2006 posits that the “zig-zag” mechanism encompasses both PTI and ETI, functioning as a dual-layered defense system that effectively combats many pathogenic agents. In the scientific community, the interaction between PTI and ETI and its effect on the development of specific or extensive resistance in plants has been the subject of ongoing debate for the past decade [74]. To combat fungal infections, rice uses both effector- and pattern-triggered immunity or senescence (ETI or PTI) to mount a dual immune defense. While ETI delivers targeted responses by means of resistance genes that target pathogen effectors, PTI offers broad protection through the use of cell receptors that recognize patterns of the pathogen. Their interaction builds a strong network that is always changing to thwart pathogen tactics.
Numerous studies conducted within this framework have established that initiating two discrete categories of receptors, namely PRRs and NLRs, in the context of PTI and ETI instigates a series of initial signaling processes that ultimately result in the successful elimination of pathogens [75,76]. The signaling cascades give rise to various outcomes, such as the generation of reactive oxygen species (ROS), the movement of calcium ions, the transmission of hormonal signals, the reprogramming of gene transcription, and the activation of the mitogen-activated protein kinase (MAPK) cascade [77,78,79]. The results, as mentioned earlier, accurately identify the locations where PTI–ETI interactions intersect, hence guaranteeing a robust immune response against a wide range of infections [80].

9. Isolation of Blast Resistance Genes and Its Utilization in Practice

Over the past two decades, a multitude of research tools have been employed to map, isolate, and clone major rice blast resistance genes. Many of these cloned genes have played a significant role in enhancing rice blast resistance and have been widely used in breeding programs. Resistance is attained through gene-for-gene interactions, wherein an R gene within a plant cell detects and acknowledges a corresponding Avr gene in the pathogen [81,82]. A successful R-Avr interaction leads to the activation of the host’s defense response, effectively suppressing pathogen infection [83,84].
Since resistance conferred by single R genes deployed on a large scale is often overcome by the emergence of novel virulent strains, it is essential to identify which R genes have been extensively used to develop rice blast-resistant germplasms in specific regions. Modern breeding programs aim to introgress different R genes into modern rice varieties and subsequently tag/characterize these varieties with molecular markers, a strategy known as marker-assisted selection (MAS). By employing meticulous phenotyping techniques and marker tagging methods, many research groups have conducted a comprehensive characterization of a wide range of rice germplasms. The primary objective of this endeavor was to ascertain the prevalence and distribution patterns of different rice blast R genes across the cultivated rice varieties in China [85].
In a study by Xiang et al. [86], the rice varieties in Heilongjiang Province, China, were examined [87]. It was observed that the distribution frequencies (DFs) of Pi-ta, Pi5, and Pib were comparatively higher than those of other genes, with percentages of 31.37%, 29.41%, and 18.62%, respectively. Following these, Pi2, Pi-d2, and Pi-d3 had DFs of 9.80%, 1.96%, and 1.96%, respectively. In a study conducted by Li et al. [88], it was observed that the core rice germplasm in Ningxia Province, China, exhibited the presence of Pi54, Pi5, Pi-ta, Pib, and Pikm, whereas the absence of Pi9 was noted [8]. In a recent study conducted by Ma et al. [89] in Guizhou Province, local varieties exhibited significantly high disease frequencies (DFs) of Pi5 and Pi54, amounting to 32.35% and 30.86%, respectively [8]. The dominance frequencies (DFs) of Pi9 and Pi2 had comparatively lower values, measuring 2.56% and 2.47%, respectively. The studies above offer a comprehensive analysis of the current situation and underscore the significance of utilizing rice blast R genes as a more secure fungicide option in managing rice blast disease in China.

10. Isolation of Quantitative or Partial Resistance Genes and Its Utilization in Practice

Single R genes that provide race-specific qualitative resistance follow a gene-for-gene model. However, when the same type of R gene is widely deployed in rice cultivars, it results in uniformity, which finally results in genetic variations in the relevant Magnaporthe oryzae strain. These genetic alterations result in the emergence of novel and highly virulent strains that are capable of overcoming resistance mechanisms, leading to the occurrence of pandemics. It is mainly attributed to the targeting of blast resistance genes [90]. Consequently, race-specific resistance has considerable strength and efficacy against a certain pathotype, yet its sustainability is limited.
In contrast, quantitative resistance, also called partial resistance, allows lesion development but prevents lesion spread and spore formation. Consequently, this mechanism decelerates the progression of infection and offers a sustained or protracted type of resistance. The durability and broad-spectrum nature of this resistance can be attributed to its ability to exert decreased selection pressure on the causal pathogen [91]. Reduced selection pressure decrease the likelihood of mutations among the fungal pathogenic genotypes of a specific population, leading to a decrease in the emergence of new virulent strains. [60]. Hence, contemporary breeding initiatives are focused on cultivating superior rice germplasms through long-lasting partial resistance strategies to manage rice blast disease effectively. At present, a total of more than 350 quantitative trait loci (QTLs) have been identified within diverse rice germplasms [92]. Notably, a subset of these QTLs, characterized by their substantial impact, have been effectively employed in mitigating rice blast disease [19].
Current research has mainly concentrated on the genetic examination of partial blast resistance, with a specific emphasis on quantitative trait loci (QTLs), including Pb1, pi21, Pi34, Pi35, and Pi39. These investigations have employed molecular markers that are closely linked to these QTLs [93,94,95,96]. Marker-assisted selection (MAS) has been shown to be a valuable tool for rice breeders in the identification and selection of rice lines harboring certain rice blast QTLs of interest during the last decade. Research has indicated that the implementation of a solitary partial resistance strategy may need to be more adequately effective in the management of rice blast, as well as the integration of specific QTLs without negative impacts, which would be beneficial through race-specific and non-race-specific immunity. Nevertheless, recorded information is scarce regarding the specific combinations of QTLs that effectively control rice blast disease. Fukuoka et al. [97] conducted a study wherein they observed the accumulation of three significant rice blast quantitative trait loci (QTLs), specifically qBR4-2a, qBR4-2b, and qBR4-2c. This pyramiding of QTLs resulted in a notable reduction in the lesion area [98].

11. Isolation of Avirulence Genes from Rice Blast Pathogen

At present, more than 24 Avr genes of M. oryzae have been mapped, and 12 of them have been cloned (Table 2). Except for ACE1 and AVR-Pita, most Avr genes under consideration encode secretory proteins consisting of fewer than 200 amino acids [99]. The evolution of Avr genes is driven by natural selection, genetic drift, mutation, and gene flow [100]. These mechanisms allow pathogen populations to adapt to host resistance, often through allelic variation, gene duplication, or horizontal gene transfer, leading to a dynamic co-evolutionary arms race between pathogen and host [101]. The angiotensin-converting enzyme (ACE1) is a protein derived from secondary metabolites characterized by its non-secretory nature. It is formed through non-ribosomal peptide synthetase (NRPS) and polyketide synthase (PKS) mechanisms. It has been demonstrated that the β-ketoacyl synthase domain within the NRPS component can induce pathogenicity [102]. Out of the 24 Avr genes that have been mapped, 15 are located towards the ends of the chromosome. Additionally, five Avr genes are interspersed by transposons, which are present on either one or both sides of the Avr genes. The co-occurrence of transposons flanking Avr genes provides evidence in favor of the concept that Avr genes could have undergone gain or loss events along pathogen evolution. Furthermore, it has been observed that around nine of the cloned genes display variability in terms of their presence or absence among the population of rice-infecting organisms. An expanded Avr gene, AVR-Pia, was found to be acquired by different M. oryzae isolates or transferred between chromosomes 5 and 7 in different isolates [103].
Extensive research has been conducted on the molecular interactions of seven out of the nine R–Avr pairings, with the exceptions being Pi9/AVRPi9 and Pib/AVRPib. These R–Avr pairs either interact directly or indirectly. Within this group, there are two pairings, namely Pii/AVR-Pii and Piz-t/AvrPiz-t, which engage in indirect interaction and mutual recognition. The remaining pairs engage in direct interaction through three distinct mechanisms. The initial approach is the utilization of the standard gene-for-gene paradigm, wherein a specific Avr protein produced by the pathogen is directly acknowledged by the equivalent R gene present in rice. This phenomenon is exemplified by the interactions between Pi54/AVR-Pi54 and Pi-ta/AVR-Pita [118]. The second category of contact entails the perception and interaction of a single Avr protein with two homologous R proteins, hence initiating an immune response upon detection. An example of this interaction is Pik-1/Pik-2/AVR-Pik [119,120]. The third type of interaction is the reciprocal of the second one, in which a complex of R proteins recognizes two different Avr proteins. An example of this is when two leucine-rich repeat (NLR) proteins, including RGA4 and RGA5, interact. This heterodimer can interact with either AVR-Pia or AVR1-CO39 to confer resistance [121,122].

12. Common R–AVR Pairs and Their Interplay in Rice Blast Resistance

12.1. Pi-ta and AVR-Pita

AVR-Pita and Pi-ta from the fungal pathogen Magnaporthe oryzae are among the first R–Avr interactions to be thoroughly explored [122]. This particular interaction has played a pivotal role in establishing a fundamental understanding of the complex dynamics between plants and pathogens, specifically about disease initiation and the development of resistance mechanisms. The gene AVR-Pita, which is located near to telomeres and is responsible for encoding a protein, secretes and possesses a unique domain known as Zn-metalloprotease [113]. The Avr-Pita protein attains its mature state as a protease, consisting of a sequence of 176 amino acids located at the C-terminus [123]. Avr-Pita is a member of a unique subclass within the AVR-Pita gene family, comprising three different genes: AVR-Pita1, AVR-Pita2, and AVR-Pita3. The first two genes mentioned possess functional properties that initiate Pi-ta-mediated resistance, whereas the third gene is a pseudogene lacking Avr functionality [124]. Moreover, rice plants use their leaf design to change cell structures and modify cuticles, close stomata, and manipulate chemical defenses to impart inherent immunity. A strong defensive system against pathogens is also produced by these physical, chemical, and signaling alterations, which together demonstrate the dynamic interactions between the structural adaptations and biological responses.
The Pi-ta R gene counterpart is a conventional NLR (928 amino acids) receptor that is situated in the cytoplasm and generally exhibits constitutive expression [8]. The direct interaction between the leucine-rich domain (LRD) of the Pi-ta protein and the AVR-Pita176 protein leads to the activation of downstream signaling cascades. The utilization of site-directed mutagenesis has facilitated the functional validation of AVR-Pita, leading to the identification of two critical amino acid substitutions, avr-pita176E177D and avr-pita176M178W, which result in the loss of its virulence function. In a similar vein, the presence of a mutated form of the Pi-ta R gene, characterized by a single amino acid substitution (LRDA918S), has been observed to reduce the physical interaction between the AVR-Pita176 and Pi-ta LRD proteins. This finding underscores the significance of the interplay between R–Avr pairs in the establishment of immunity against M. oryzae [125]. Plant gene connections orchestrate a strong defensive network by triggering immunity via pattern recognition, effector sensing, signaling, transcription control, and feedback loops.

12.2. Pia and AVR-Pia

This is the second class of interaction in which two NLRs, RGA4 and RGA5, interact with a single Avr protein [121,122]. The encoded secretory protein of AVR-Pia contains an N-terminal SP [112]. Different isolates of M. oryzae that are resistant to Pia genes in rice have different numbers of copies, ranging from one to three; this depends on the isolate. For instance, the avirulent strain Ina168 possesses three copies of AVR-Pia genes [99]. The NMR (nuclear magnetic resonance)-determined structure of AVR-Pia reveals a MAX-effector β-sandwich-like structure, while Pia is composed of RGA4 and RGA5 protein genes, oriented face-to-face in opposite directions [121]. Furthermore, two isoforms of RGA5 called RGA5-A and RGA5-B are the consequences of RGA5 alternative splicing, in which only RGA5-A mediates Pia resistance. According to in vitro experiments, it has been observed that the continuous production of RGA4 leads to the initiation of cell death. However, in the absence of infection, this cell death is suppressed by RGA5 in planta. It is important to note that the NB (nucleotide-binding) domain of RGA4 is essential for the induction of cell death [90,91]. Physical contact between AVR-Pia and the non-LRR C-terminal domain of RGA5 facilitates the inhibition and promotion of RGA4-mediated cell damage.

12.3. Pii and AVR-Pii

This is the third type of interaction in which the R–Avr pair (Pii and AVR-Pii) mediates the immune response through an indirect interaction with each other [112]. The secreted protein encoded by AVR-Pii belongs to a protein family known as pex33. The protein structure is composed of four homologs with two conserved motifs [95]. Conversely, the protein encoded by Pii is a common NLR consisting of 1025 amino acids [121]. Two different forms (I and II) of AVR-Pii exist in different isolates. Form I is a hybrid of two rice proteins (OsExo70-F2 and OsExo70-F3) and AVR-Pii. Though both rice proteins are required for the immune response, the latter (OsExo70-F3) instead of the former rice protein induces a Pii-mediated immune response. This result implies that OsExo70 serves as a helper protein in the interaction of Pii/AVR-Pii [125].

12.4. Piz-t and AvrPiz-t

One such form of R–Avr contact pertains to the indirect interaction that occurs between Piz-t and AvrPiz-t, which is a classic example of a plant–pathogen interaction where a single, broad-spectrum R gene recognizes and interacts with multiple variants of an Avr gene [114]. The AvrPiz-t protein has secretory characteristics akin to those of other well-known Avr genes [115]. The structure of AvrPiz-t and similar ToXB genes was determined via NMR. AvrPiz-t is composed of a β-sheet consisting of six disulfide chains from Cys62 to Cys75. Single point mutations on any cysteine residue reduce the toxicity of AvrPiz-t [115]. Piz-t functions as a broad-spectrum NLR gene. The LRR domain of Piz-t exhibits 18 amino acid alterations, which not only determine the activation of resistance but also differentiate Piz-t from Pi-2 [50]. Being a broad-spectrum R gene, twelve different interacting proteins of AvrPiz-t (APIPs) interact with AvrPiz-t in different lines of rice. The nature of resistance or immunological response is contingent upon both the specific AvrPiz-t protein and the genetic composition of the rice host harboring the Piz-t gene. In the context of Piz-t-lacking Nipponbare rice, the suppression of PTI is observed as a result of the interaction between AvrPiz-t and PTI. Conversely, in the presence of Piz-t, PTI is stabilized when the rice plant is infected by M. oryzae [116].

13. Future Trends in Rice Blast Research

Rice blast disease continues to pose a significant threat to world food security, despite the progress made in cloning rice blast resistance R genes and their corresponding Avr genes in M. oryzae, as well as gaining insights into different models concerning R–Avr interactions. One ongoing concern is that changing global climate patterns may induce unusual mutations in pathogens, potentially leading to the emergence of novel rice blast resistance-breaking strains. Consequently, establishing a comprehensive surveillance system to monitor the emergence of these lethal strains is critical. The application of next-generation sequencing (NGS) and molecular breeding technologies has provided rice breeders with enhanced capabilities to devise effective strategies for monitoring and managing rice blast. Mutiga et al. [100] introduced the Mobile and Real-Time Plant Disease (MARPLE) system, which is a patho-genomics-based rice blast surveillance system (Figure 2) [121]. Within this framework, rice leaf tissue that has been infected is gathered in the field for the purpose of discerning the attributes, genomic markers, and genetic alterations present within the population of the pathogen. Following this, DNA is extracted from the infected leaves and amplified with potential avirulence genes using multiplex PCR, followed by targeted genome sequencing utilizing Oxford nanopore sequencers. Subsequently, the sequencing data are subjected to analysis in order to provide predictions regarding the evolutionary patterns of Avr genes and the development of resistance to fungicides. Based on the analysis of these data, rice breeders are able to make accurate and timely decisions on the breeding and deployment of rice cultivars that are specifically resistant to rice blast disease.
Advancements in the field of rice genetics and development have facilitated the cloning of a growing repertoire of rice blast R and M. oryzae Avr genes by rice breeders. The achievement of successfully cloning Pi2, Pi9, and Pigm has provided new opportunities for the identification of functional single-nucleotide polymorphisms (SNPs) that are strongly linked to the resistant genotype. The utilization of these functional single-nucleotide polymorphisms (SNPs) holds promise in the development of robust kompetitive allele-specific PCR (KASP) markers. These markers have significant value in marker-assisted breeding efforts aimed at enhancing rice blast resistance [117]. In a comparable manner, studies have been conducted on the sequencing and assembly of a genome of Tetep, a germplasm explosion-resistant rice genetic resource with a wide range of functions [98]. This particular cultivar is noteworthy, as it serves as the donor of the Pi5 gene. The Tetep genome assembly was found to include a total of 455 NLR genes. The utilization of molecular markers specifically tailored for these anticipated NLRs has not only empowered rice breeders in the process of selecting resistant rice cultivars, but has also facilitated the incorporation of these NLRs into novel breeding variations, hence enhancing the durability of rice blast resistance. Genome editing technologies (GETs) have emerged as pivotal tools in the field of gene functional study. CRISPR/Cas9 has gained significant popularity among researchers as a reliable and technically accessible gene-editing technology within the realm of genetic engineering [119]. The utilization of this technology is becoming favored as the major method for gene editing among rice breeders. The utilization of CRISPR/Cas9 technology has been employed in recent studies to confirm the efficacy of many rice blast R genes. Researchers have observed that the resulting altered line exhibited enhanced resistance to M. oryzae compared to the wild type. In a similar vein, the function of the persistent rice blast-resistant Ptr gene was effectively validated through the successful application of CRISPR/Cas9-mediated targeted modification, resulting in the gene’s susceptibility [46]. More rice blast R–Avr genes will soon be edited using CRISPR/Cas9, which will further guarantee long-term and sustainable resistance to the fatal rice blast disease [54].

14. Conclusions

Developing resistant rice varieties is a highly cost-effective and efficient technique for reducing the impact of rice blast. To achieve success in this technique, it is essential to have a thorough grasp of the processes that control rice resistance and the pathogenicity of the pathogen. This paper summarizes the advancements achieved in isolating R and qR genes from the rice host and Avr genes from Magnaporthe oryzae. The complex interactions between the rice host and the pathogen depend on the presence of specific R–Avr gene pairs. Moreover, the review article explores the difficulties of implementing these breakthroughs in disease management. Expanding on these progressions and tackling possible obstacles, this review suggests five crucial research areas for the future. These study areas are crucial for advancing rice blast-resistant varieties with a wide range of effectiveness.

Author Contributions

M.U.Y., participated in the conceptualization, writing, reviewing, and editing of the original manuscript. S.Z. contributed to the reviewing and editing of the manuscript. I.A., M.Q., Z.I., N.R., and S.P.M. helped with the literature review and participated in writing the original manuscript, and W.U.Z., X.J. and Y.Z. revised the manuscript and eliminated grammatical mistakes. All authors have read and agreed to the published version of the manuscript.

Funding

This study was partially supported by the Jiangsu Government (JBGS2021-040), the Key Studying and Developing Project of Jiangsu Province for Modern Agriculture (BE2022335), and a project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflicts of interest.

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Agronomy 14 00163 g001
Figure 1. Mind map diagram showing the life cycle of M. oryzae.
Figure 1. Mind map diagram showing the life cycle of M. oryzae.
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Figure 2. Schematic diagram of MARPLE system. (1) Tissue collection from rice leaf, (2) DNA isolation, (3) multiplex PCR, (4) gene-enrichment sequencing, (5) data analysis. Modified from [117].
Figure 2. Schematic diagram of MARPLE system. (1) Tissue collection from rice leaf, (2) DNA isolation, (3) multiplex PCR, (4) gene-enrichment sequencing, (5) data analysis. Modified from [117].
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Table 1. Mapped and cloned rice blast resistance genes.
Table 1. Mapped and cloned rice blast resistance genes.
R GeneProtein StructureResistanceReferences
Pi-bNBS-LRR
two genes		Broad-spectrum to Japanese blast isolates[47]
Pi-taNBS-LRR
two genes		Race-specific resistance to US blast isolates until 2004 Arkansas blast outbreak[48]
Pi9NBS-LRR member of multi-gene family (nine genes), high amino acid identity to Pi2 and Piz-tBroad-spectrum to SE Asia blast isolates; low-level resistance in S. Korea isolates[49]
Pi2 (Piz-5)NBS-LRR
see Pi9 and Piz-t
nine genes		Broad-spectrum to some Philippine isolates but different range from Piz-t[50]
Piz-tNBS-LRR
see Pi9 and Pi2
nine genes, eight aa differences between
Piz-t and Pi2		Broad-spectrum to some Philippine isolates but different range from Pi2[51]
Pi-d2Receptor-like kinase, mannose
binding lectin, and serine threonine
kinase domain, single gene		Largely undefined: tested only against limited number of Chinese isolates[51]
Pi33Finely mapped NBS-LRR but RPM1- likeLargely undefined: tested only against limited number of isolates[52]
Pi36NBS-LRR
Single gene		Unknown[53]
Pi37NBS-LRR
four genes		Unknown[54]
Pi-CO39(t)Locus carries multiple NBS-LRR-like genes, flanked by serpinsUnknown[55]
Pi40Finely mapped, nests within six NBSLRRs:
single gene		Broad-spectrum to Korean and Philippine blast isolate[56]
PikhNBS-LRR
six genes		Broad-spectrum to NW Himalayan blast isolates[57]
Pi21Novel protein with heavy-metal-binding and proline-rich domainsPartial R gene[58]
Table 2. List of all cloned Avr genes.
Table 2. List of all cloned Avr genes.
Avr GenesProtein Size (aa)Cognate Cloned R GenesReferences
PWL1147Unknown[104]
PWL2145Unknown [105]
AVR1-CO3989Pi-CO39[106,107]
AVR-Pita224Pi-ta[108]
ACE14035Pi33 (Un-cloned)[109]
AVR-Pia85Pia[110,111]
AVR-Pii70Pii[112]
AVR-Pik/km/kp (AVR-Pikh)113; 5 Alleles (A–E)Pik/Pik-m/Pik-p, Pik-h[103,113]
AvrPiz-t108Piz-t[114]
AVR-Pi991Pi9[115]
AVRPib75Pib[116]
AVR-Pi54153Pi54[102]
MoHTR1UnknownUnknown[117]
MoHTR2UnknownUnknown[117]
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Younas, M.U.; Ahmad, I.; Qasim, M.; Ijaz, Z.; Rajput, N.; Parveen Memon, S.; UL Zaman, W.; Jiang, X.; Zhang, Y.; Zuo, S. Progress in the Management of Rice Blast Disease: The Role of Avirulence and Resistance Genes through Gene-for-Gene Interactions. Agronomy 2024, 14, 163. https://doi.org/10.3390/agronomy14010163

AMA Style

Younas MU, Ahmad I, Qasim M, Ijaz Z, Rajput N, Parveen Memon S, UL Zaman W, Jiang X, Zhang Y, Zuo S. Progress in the Management of Rice Blast Disease: The Role of Avirulence and Resistance Genes through Gene-for-Gene Interactions. Agronomy. 2024; 14(1):163. https://doi.org/10.3390/agronomy14010163

Chicago/Turabian Style

Younas, Muhammad Usama, Irshad Ahmad, Muhammad Qasim, Zainab Ijaz, Nimra Rajput, Saima Parveen Memon, Waqar UL Zaman, Xiaohong Jiang, Yi Zhang, and Shimin Zuo. 2024. "Progress in the Management of Rice Blast Disease: The Role of Avirulence and Resistance Genes through Gene-for-Gene Interactions" Agronomy 14, no. 1: 163. https://doi.org/10.3390/agronomy14010163

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