Next Article in Journal
Immortalizing Cells for Human Consumption
Next Article in Special Issue
Transcriptome Analysis of Triple Mutant for OsMADS62, OsMADS63, and OsMADS68 Reveals the Downstream Regulatory Mechanism for Pollen Germination in Rice (Oryza sativa)
Previous Article in Journal
A Multi-Perspective Proximity View on the Dynamic Head Region of the Ribosomal 40S Subunit
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
IJMS
Volume 22
Issue 21
10.3390/ijms222111658
ijms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Recent Progress in Rice Broad-Spectrum Disease Resistance

by
Zhiquan Liu
1,
Yujun Zhu
1,
Huanbin Shi
1,
Jiehua Qiu
1,
Xinhua Ding
2 and
Yanjun Kou
1,*
1
State Key Lab of Rice Biology, China National Rice Research Institute, Hangzhou 311400, China
2
State Key Laboratory of Crop Biology, Shandong Provincial Key Laboratory for Biology of Vegetable Diseases and Insect Pests, College of Plant Protection, Shandong Agricultural University, Taian 271018, China
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2021, 22(21), 11658; https://doi.org/10.3390/ijms222111658
Submission received: 4 October 2021 / Revised: 25 October 2021 / Accepted: 25 October 2021 / Published: 28 October 2021
(This article belongs to the Special Issue Crop Genome Editing and Plant Breeding Innovation)
Browse Figures
Versions Notes

Abstract

:
Rice is one of the most important food crops in the world. However, stable rice production is constrained by various diseases, in particular rice blast, sheath blight, bacterial blight, and virus diseases. Breeding and cultivation of resistant rice varieties is the most effective method to control the infection of pathogens. Exploitation and utilization of the genetic determinants of broad-spectrum resistance represent a desired way to improve the resistance of susceptible rice varieties. Recently, researchers have focused on the identification of rice broad-spectrum disease resistance genes, which include R genes, defense-regulator genes, and quantitative trait loci (QTL) against two or more pathogen species or many isolates of the same pathogen species. The cloning of broad-spectrum disease resistance genes and understanding their underlying mechanisms not only provide new genetic resources for breeding broad-spectrum rice varieties, but also promote the development of new disease resistance breeding strategies, such as editing susceptibility and executor R genes. In this review, the most recent advances in the identification of broad-spectrum disease resistance genes in rice and their application in crop improvement through biotechnology approaches during the past 10 years are summarized.

1. Introduction

Rice (Oryza sativa L.) is the most important food crop, which is consumed by approximately 50% of the world’s population, with its consumption growing dramatically in many parts of the world. Stable rice production is constrained by various biotic stresses, including fungal blast caused by Magnaporthe oryzae, sheath blight caused by Rhizoctonia solani, false smut caused by Ustilaginoidea virens, bakanae disease due to Fusarium fujikuroi, bacterial blight caused by Xanthomonas oryzae pv. oryzae (Xoo), bacterial leaf streak caused by Xanthomonas oryzae pv. oryzicola (Xoc), and virus diseases. The yield loss of rice caused by various diseases averages upward of 30%. Therefore, it is critical to adopt effective means to control these diseases to ensure global food security. In addition to encouraging farmers to exercise good farming practices, application of pesticides remains one of the main methods of disease control, but the increase in costs and their harmful effects on the environment and operators cannot be discounted. These make the farmers largely dependent on the cultivation of new resistant varieties, which is considered to be the most effective method so far.
Broad-spectrum resistance, which refers to resistance against two or more types of pathogen species or the majority of races/isolates of the same pathogen species, is one of the ultimate goals of breeders for rice improvement [1]. Exploitation of the genetic determinants of broad-spectrum resistance will improve the resistance of the susceptible varieties. On this account, breeders and biotechnologists are trying to obtain the source of broad-spectrum resistance to understand and utilize the genetics underlying this process. With the development of rice molecular biology, functional genomics, and gene editing technology, great progress has been made in the broad-spectrum disease resistance genes in rice. It is worth mentioning that many extremely important broad-spectrum disease resistance genes and their mechanisms and applications were reported 10 years ago. These works have been well summarized in several reviews and will not be highlighted here [1,2]. This review focuses on the progress in the identification of broad-spectrum disease resistance genes in rice and their application in crop improvement during the past 10 years.

2. Identified Rice Broad-Spectrum Disease Resistance Genes in Past 10 Years

2.1. R Genes Confer Broad-Spectrum Disease Resistance in Rice

The ability of plants to defend themselves against microbes is specified by disease resistance (R) genes-mediated resistance and basal resistance. Upon recognition of an invading pathogen, R proteins, mostly from the nucleotide-binding leucine-rich repeat receptor (NLR) family, detect the secreted pathogen effectors to activate a multitude of responses that ultimately lead to resistance. These responses include Ca2+ influx, ROS (reactive oxygen species) accumulation, mitogen-activated protein (MAP) kinase activation, defense hormone signaling activation, and upregulation of defense-related genes [3]. In recent years, important progress has been achieved in cloning and mechanical analysis of R genes. These identified R genes provide not only new genetic resources for breeding broad-spectrum rice varieties, but also new strategies to improve resistance.
Rice blast, caused by M. oryzae, is the most devastating disease of rice and reduces yield by 10–35%. To date, approximately 100 R genes/alleles against M. oryzae have been identified, of which more than 26 R genes/alleles were cloned [2]. Among these genes, Pi50, Pi54rh, Pi56(t), Pi64, Pigm, Pizh, Ptr, and Pita2 were cloned as broad-spectrum resistance R genes in the past 10 years [4,5,6,7,8,9,10] (Figure 1, Table 1). Pi50, Pigm, and Pizh are allelic to Pi2/Pi9, which are well-known broad-spectrum resistance NBS-LRR (nucleotide binding site-leucine rich repeat) genes on the chromosome 6, with different resistance spectra against M. oryzae. One of these alleles Pigm has been confirmed with stable resistance to panicle blast [7]. Pi54rh, an ortholog of Pi54, encodes an NBS-LRR protein with a unique Zinc finger domain. Both Pi56(t) and Pi64 also belong to the NBS-LRR family of disease resistance genes. Notably, the constitutively expressed Pi64 conferred resistance to both leaf and neck blast. Unlike most blast R genes, Ptr, which is required for broad-spectrum blast resistance mediated by R genes Pita and Pita2, encodes a four Armadillo (ARM) repeat protein. Furthermore, more alleles or natural variation of broad-spectrum blast resistance R genes have been investigated, including geographically distinct and domain-specific sequence variations of Pib, novel alleles of Pik locus Pi1, Pike, and Pikg, Pi54 alleles, novel Pi21 haplotypes, and novel alleles of Pi2/9 locus [11,12,13,14,15,16,17,18,19,20,21,22]. In addition, four broad-spectrum resistance R genes, Pi-hk1, Pi57(t), Pi65(t), and Pi69(t), were finely mapped in the past 10 years [23,24,25,26].
In addition to rice blast, bacterial blight, caused by Xoo, is also a globally devastating rice disease. In rice, at least 46 genes that confer dominant or recessive host resistance to Xoo have been identified, of which more than 16 R genes were cloned [27]. Among them, Xa7, Xa23, Xa41(t), and Xa47(t) were cloned as broad-spectrum resistance R genes in the past 10 years [27] (Figure 1, Table 1). Xa7, which encodes a 113 aa unknown protein, is a dominant R gene that provides broad-spectrum and extremely durable resistance to Xoo. The transcription of Xa7 is specifically activated by the Xoo isolates with transcription activator-like effector (TALE) AvrXa7 or PthXo3 to act as an executor [27]. Another executor R gene, Xa23, which is induced by TALE AvrXa23, confers extremely broad-spectrum resistance to Xoo [28]. xa41(t), an allele of sugar transporter OsSWEET14, confers resistance to half of the tested Xoo isolates [29]. Similar to Xa23, Xa47(t) is from the wild rice Oryza rufipogon. Xa47(t), encoding a NLR protein, is highly resistant to all tested ten Xoo isolates [30]. In addition to these cloned R genes, a broad-spectrum bacterial blight resistance gene Xa33 from Oryza nivara has been finely mapped [31].
Unlike rice blast and bacterial blight, no R gene for serious diseases sheath blight and rice false smut has been identified [32,33]. Moreover, only one rice stripe virus (RVS) resistance gene, STV11, has been cloned [34]. The molecular mechanisms underlying rice–virus interaction remain poorly understood. Therefore, so far, there is no broad-spectrum resistance R gene for these diseases.
For broad-spectrum resistance R genes, it is worth noting that the R genes are tagged as broad-spectrum resistance genes because they can resist multiple isolates of one pathogen rather than two or more types of pathogen species. However, in the case of many isolates tested, it is unlikely for any R gene to be resistant to only one isolate. At present, there is no standard in terms of how many isolates or what proportion of isolates an R gene confers resistance to for it to be claimed as a broad-spectrum resistance R gene. Furthermore, although so many broad-spectrum resistance genes have been identified, the mechanism of these genes mediating broad-spectrum resistance to rice disease is not yet clear. In the broad-spectrum resistance R gene Pi9 case, the corresponding Avirulence gene AvrPi9 exists widely in various M. oryzae isolates [35]. To determine whether other blast R genes are similar, the cloning of their corresponding Avirulence genes and analysis of their distribution in M. oryzae isolates will give some hints. Similar to R genes against blast, the resistance spectrum of R genes against Xoo may also be determined by the distribution of corresponding Avirulence genes, TALE in most of cases, in Xoo isolates. Actually, considering current knowledge, it is difficult to predict the mechanism underlying R protein-mediated broad-spectrum resistance in addition to the wide distribution of corresponding Avirulence genes. The research progress of the interactions between R protein and effectors from pathogens will increase our understanding of R protein-mediated broad-spectrum resistance.

2.2. Defense Regulator Genes Contribute to Broad-Spectrum Disease Resistance

Differing from R genes, defense regulator genes often confer partial resistance to a broad spectrum of pathogen isolates or various pathogens. In the past 10 years, there were at least 56 broad-spectrum resistant defense regulator genes identified which positively or negatively regulate the resistance to rice diseases (Figure 1, listed in Table 2). The proteins encoded by these genes are transcriptional factors, kinases, peroxidases, E3 ubiquitin ligases, ferredoxin-dependent glutamate synthases, glutaredoxins, etc. In this review, we classify these broad-spectrum resistant defense regulator genes according to the types of pathogens they resist.
In the past 10 years, several broad-spectrum resistant defense regulator genes against M. oryzae were identified. Through a genome-wide association study (GWAS), a natural allele of a C2H2-type transcription factor bsr-d1 was identified in rice that confers non-race-specific resistance to blast. This allele causes a lower gene expression level, and then downregulates expression of three peroxidase-encoding genes, Os05g04470, Os10g39170, and Perox3, resulting in accumulation of H2O2 and enhanced broad-spectrum resistance to M. oryzae [36,37]. In addition, an MYB transcription factor (OsMYB30) is also involved in bsr-d1-mediated broad-spectrum blast resistance by activating the lignin biosynthesis genes Os4CL3 and Os4CL5 to strengthen cell walls [38]. The other three transcription factors, OsNAC60, OsWRKY45, and RRM (RNA recognition motif) protein PIBP1 (PigmR-interacting and blast resistance protein 1), also contribute to broad-spectrum blast resistance in rice. OsNAC60, which is a target of Osa-miR164a, negatively regulates rice immunity against the blast fungus M. oryzae by decreasing programmed cell death, ion leakage, ROS accumulation, callose deposition, and defense-related gene expression [39]. OsWRKY45 mediates the blast resistance of CC-NB-LRR protein Pb1 [40]. PIBP1 specifically interacts with PigmR and other similar NLRs, and it functions as an unconventional transcription factor to activate the expression of OsWAK14 and OsPAL1 to trigger blast resistance [41]. In addition to transcription factors, the RING protein OsBBI1 with E3 ligase activity and light-harvesting complex II protein LHCB5 are also involved in broad-spectrum blast resistance. OsBBI1 confers broad-spectrum resistance against M. oryzae by increasing H2O2 accumulation in cells and modifying the cell-wall defense [42]. Phosphorylation of LHCB5 enhances resistance to M. oryzae through the accumulation of ROS in the chloroplast [43].
Several broad-spectrum resistant defense-regulator genes against Xoo were also identified in rice in the past 10 years. In rice, several genes involved in receptor-mediated broad-spectrum resistance and systemic acquired resistance (SAR) likely contribute to broad-spectrum resistance to Xoo. The XA21-binding protein XB25, a plant-specific ankyrin repeat (PANK) protein, contributes to the accumulation of receptor XA21 and maintenance of XA21-mediated broad-spectrum resistance to Xoo [44]. The endoplasmic reticulum (ER) chaperone, luminal-binding protein 3 (BiP3) negatively regulates resistance mediated by rice XA3, a receptor that provides broad-spectrum resistance to Xoo [45]. Overexpression of OsNPR1 (non-expressor of pathogenesis-related genes 1), a master gene for SAR in rice, greatly enhances resistance to Xoo [46]. Moreover, the cysteine-rich-receptor-like kinases (OsCRK6 and OsCRK10) are required for OsNPR1-mediated immunity [47]. In addition to CRK6 and CRK10, some kinases have been identified as conferring broad-spectrum resistance to Xoo. For instance, overexpression of a constitutively activated form of calcium-dependent protein kinases OsCDPK1 confers Xoo resistance by affecting OsPR10a expression in rice [48]. OsILA1, a Raf-like MAPKKK, functions as a negative regulator and acts upstream of the OsMAPKK4–OsMAPK6 cascade against Xoo [49]. Unlike the type of genes mentioned above, lc7, encoding a mutant ferredoxin-dependent glutamate synthase 1 (Fd-GOGAT1), promotes ROS accumulation in the leaves and has high broad-spectrum resistance against seven Xoo strains [50].
Defense regulator genes are different from pathogen-specific R genes, which can confer resistance to multiple pathogens. For instance, Lysin motif-containing protein genes LYP4 and LYP6, transcriptional regulator genes OsWRKY67 and IPA1, the host basal transcription factor IIA subunit genes OsTFIIAα and OsTFIIAβ, germin-like protein gene OsGLP2-1, sucrose nonfermenting 1-related protein kinase 1 genes OsSnRK1a and OsSnRK1b/OSK35, calcium-dependent protein kinase gene OsCPK4, and receptor-like cytoplasmic kinase gene broad-spectrum resistance 1 (BSR1) play a positive role in basal resistance against M. oryzae and Xoo [51,52,53,54,55,56,57,58,59,60]. In contrast, mutations in E3 ubiquitin ligase gene EBR1 (enhanced blight and blast resistance 1), RhoGAP SPIN6, rice wall-associated kinase gene OsWAK25, Cullin 3-based RING E3 ligase gene OsCUL3a, dynamin-related protein gene OsDRP1E, eEF1A-like protein gene SPL33, eukaryotic translation elongation factor 1A-like genes LMM5.1 and LMM5.4, eukaryotic release factor 1 gene LMM1, abscisic acid 2 (OsABA2), and CUE domain-containing protein gene SPL35 result in lesion mimic leaves and enhanced broad-spectrum resistance to M. oryzae and Xoo [61,62,63,64,65,66,67,68,69,70]. Differing from these lesion mimic genes, histone H4 deacetylase gene HDT701 and mitogen-activated protein kinase OsMPK15, whose mutant or overexpressing lines do not show lesion mimic leaves, negatively regulate the resistance against M. oryzae and Xoo [71,72]. Similarly, loss of function of the Bsr-k1 gene, encoding a tetratricopeptide repeat (TPR)-containing protein, leads to accumulation of OsPAL1–7 mRNAs, which confer broad-spectrum resistance against M. oryzae and Xoo with no major penalty on key agronomic traits [73].
In addition, several genes have been reported as conferring broad-spectrum resistance against multiple pathogens other than both M. oryzae and Xoo. Aldehyde dehydrogenase OsALDH2B1 has a moonlight function as a transcriptional regulator to regulate a diverse range of biological processes involving G protein, brassinolide, jasmonic acid, and salicylic acid signaling pathways. Loss of function of OsALDH2B1 greatly enhanced resistance to M. oryzae, Xoo, and Xoc [74]. Similarly, rice phenylalanine ammonia-lyase gene OsPAL4 is associated with resistance to M. oryzae, Xoo, and Xoc [75]. Heat-shock factor OsHsfB4d binds the promoter and regulates the expression of a small heat-shock protein gene OsHsp18.0-CI to be resistant against Xoo and Xoc [76,77]. Moreover, suppression of phytoalesin-deficient 4 OsPAD4 results in increased susceptibility to the Xoo and Xoc [78]. Rice glutaredoxin gene OsGRXS15 and a novel NPR1 homolog gene OsNH5N16 contribute to broad-spectrum resistance to Xoo and F. fujikuroi by regulating the expression of PR genes related to SAR [79,80]. Abscisic acid, stress, and ripening 2 (ASR2) contributes to broad-spectrum resistance against Xoo and R. solani by regulating the expression of a defense regulator gene Os2H16 [81,82]. In contrast, 14-3-3 protein (GF14e) negatively affects cell death and disease resistance to Xoo and R. solani [83]. WRKY transcription factor OsWRKY30 and 1-aminocyclopropane-1-carboxylic acid synthase gene ACS2 positively regulate the resistance against M. oryzae and R. solani [84,85]. Moreover, methyl esterase-like gene OsMESL and copine genes OsBON1 and OsBON3 are critical suppressors of immunity to M. oryzae, Xoo, and R. solani [86,87].
These excellent studies on broad-spectrum resistant defense regulator genes show multiple characteristics. Firstly, with the increasing attention to broad-spectrum resistance, the reports of broad-spectrum resistance related genes have increased sharply in the past 10 years [1]. For breeders, whether these genes also show broad-spectrum disease resistance in the natural field environment is still the focus of attention. Secondly, the connections between these broad-spectrum resistant defense regulator genes and their relationships with R genes remain largely unclear due to limited experimental evidence. It is possible that these broad-spectrum resistance defense regulator genes function in the convergence point of the crosstalk between the pathways of basal and R protein-mediated resistances or between the pathways initiated by different R proteins [1]. Thirdly, only a few broad-spectrum resistant defense regulator genes mediate resistance with little or no yield penalties. The tradeoff between broad-spectrum resistant defense regulator genes and rice yield is one of the important limiting factors, as summarized in Chen’s review [2]. Last but not least, there are rare examples of using these disease resistance-related genes to obtain broad-spectrum disease-resistant varieties in breeding programs. Although it was very difficult to effectively use these broad-spectrum resistant defense regulator genes in molecular breeding of rice until now, identification of natural variations/alleles of these genes from rice varieties with excellent agronomic traits, artificial mutation, and genome-editing technology would provide important methods for broad-spectrum disease resistance.

2.3. Identification of Broad-Spectrum Disease Resistance Loci by QTL Mapping and GWAS Analysis

Broad-spectrum resistance is a polygenic trait, whereby a combinatorial effect of major and minor genes mediates this trait [88]. With the advances of next-generation DNA sequencing and high-density molecular marker platforms, various quantitative trait loci (QTL) against rice blast, sheath blight, and/or bacterial leaf blight have been mapped to locate the source of these traits in the past 10 years. Using Heikezijing, a japonica rice landrace with broad resistance against rice blast and Suyunuo recombinant inbred lines, 13 QTLs were identified to be effective against only one M. oryzae isolate, while the other seven QTLs may be non-isolate-specific because each QTL confers resistance to more than one isolate [89]. By evaluating the disease reactions of 60 US weedy rice accessions with 14 M. oryzae isolates, 28 resistant QTLs were identified, of which three loci contribute to non-isolate-specific resistance [90]. With a combination of genome-wide association studies (GWAS) and interval mapping analyses, 51 QTLs against Xoo and Xoc were identified in multiparent advanced generation intercross populations, including 11 broad-spectrum resistance, three pathovar-specific, and 37 isolate-specific QTLs [88]. A GWAS analysis of 236 diverse rice accessions revealed 12 QTLs, of which two QTLs showed broad-spectrum resistance to Xoc [91]. Recently, 147 SNP associated with Xoo resistance were identified in 222 predominantly Thai rice accessions; however, the significantly associated SNP only occurred across a maximum of five Xoo isolates [92]. In rice, most resistance QTLs are conditioned to different populations and different QTL mapping analyses, which makes it difficult to handpick suitable QTL candidates for breeding programs with multiple resistances. To integrate QTL from different studies, a meta-analysis of QTLs represents a good approach. Using meta-analysis, 48 meta-QTLs were obtained from 27 studies, of which MQTL8.1 and MGTL2.5 were associated with resistance to rice blast, sheath blight, and bacterial leaf blight [93]. Resistant QTLs confer a partial but frequently referred resistance to broad-spectrum pathogen isolates or diverse pathogens, which are considered as effective resources for breeding to achieve broad-spectrum resistance [1]. However, the results from all these studies clearly showed that most QTLs confer isolate- and/or pathogen-specific resistance; in other words, not all resistance QTLs are broad-spectrum. Moreover, there are few broad-spectrum resistant QTLs available for crop improvement programs, which results in the breeder needing a longer time and higher cost to pyramid QTLs to obtain broad-spectrum disease-resistant varieties.

3. Strategies for Broad-Spectrum Disease Resistance Rice Breeding

3.1. Gene Pyramiding Breeding Is an Effective Way to Obtain Broad-Spectrum Disease Resistance Rice Varieties

Developing and using resistant varieties could effectively and economically control diseases. One of the effective ways to develop broad-spectrum resistance varieties is marker-assisted gene pyramiding. Numerous cloned R genes provide a wealth of information and resources for pyramiding breeding, which promoted the generation of pyramiding R gene lines with broader and enhanced resistance to bacterial blight and rice blast in the past 10 years. Introducing Piz/Pi2/Pi9, Pid3, or Pi54 or pyramiding the R genes Pi37 + Pid3, Pi5 + Pi54, Pi54 + Pid3, Pigm + Pi37, Pi9 + Pi54, Pigm + Pi1, Pigm + Pi33, Pigm + Pi54, Pi2 + Pi46 + Pita, Pi2 + Pi46 + Pigm, and Pib + Pi25 + Pi54 leads to broad-spectrum blast resistance [94,95,96,97,98,99,100,101]. Pyramiding the R genes Xa4 + xa5 + Xa21, xa5 + xa13 + Xa21, xa5 + Xa21, Xa21 + Xa33, and Xa23 with other genes, as well as Xa4 + xa5 + Xa7 + xa13 + Xa21, provides a higher and broader resistance to Xoo than individual resistance genes [102,103,104,105,106,107,108]. Moreover, pyramiding the genes Pi2 + Xa7 and xa5 + xa13 + Pi54 + qSBR7-1 + qSBR11-1 + qSBR11-2 confers broad-spectrum resistance to both M. oryzae and Xoo [109,110].
All aforementioned studies give excellent examples of pyramiding R genes to obtain broad-spectrum resistance rice. However, it is still very difficult to obtain broad-spectrum disease resistant varieties by polymerization breeding for several reasons [111,112]. The first is that only a few R genes have been successfully used for molecular breeding processes. The existence of R genes containing resistant germplasms with excellent comprehensive traits is an important perquisite for breeding application. Secondly, the utilization of R genes in main modern rice varieties and the effectiveness of R genes in different rice-cultivating regions are still not very clear. Thirdly, the resistance effect of pyramiding different R genes may not be a simple accumulation of resistance spectrum and improvement in the resistance level; meanwhile, with the increase in the number of pyramided R genes via traditional genetics approaches, the workload of breeding, time consumption, and linkage drag with unacceptable traits increase. Therefore, an accurate understanding of R gene utilization and the establishment of high-throughput molecular breeding methods to create R genes harboring resistant germplasms without linkage drag are important steps to overcome these difficult points, so as to improve broad-spectrum resistance breeding in the future.

3.2. Engineering Broad-Spectrum Disease Resistance Rice by Editing Susceptibility and Executor R Genes Is a New Method with Broad Application Prospects

During the plant–pathogen interaction, phytopathogens evolve to exploit the susceptibility (S) genes of plant to facilitate their infection. These S genes are associated with host recognition, penetration, pathogen proliferation and spread, or negative regulation of immune signals [113]. Disrupting these S genes can lead to enhanced resistance or reduced compatibility and, consequently, expand resources for broad-spectrum disease resistance. To date, many S genes have been identified in rice, such as Pi21, Xa5, Xa13/OsSWEET11, Xa25/OsSWEET13, and Xa41/OsSWEET14 [29,114,115,116,117,118,119,120,121]. Recent advances in genome editing technologies, such as the CRISPR (clustered regularly interspaced short palindromic repeats)/Cas9 (CRISPR-associated protein 9)-mediated gene editing system, have greatly accelerated the generation of new resistant rice through genetic manipulation of S genes [113,122].
The most reported examples of editing S genes in rice can be found in research related to Xoo resistance. During the infection process of Xoo, abundant transcription activator-like effectors (TALEs), which are the major virulence factors and compatibility determinants, are secreted into rice cells. Most TALEs bind to the cis-element effector-binding elements (EBEs) in the promoter of S gene and reprogram their transcription to promote disease. For instance, the TALEs PthXo1, PthXo2, and PthXo3/AvrXa7/TalC/TalF bind the EBEs in the promoters of rice OsSWEET11, OsSWEET13, and OsSWEET14 genes, respectively (Figure 2a) [122]. Editing the EBEs of S genes OsSWEET11, OsSWEET13, and OsSWEET14 in rice varieties japonica Kitaake and indica IR64 and Ciherang-sub1 resulted in loss of induction of these S genes by Xoo and broad-spectrum resistance against Xoo [123,124,125,126]. Similar strategies were used in the modification of S genes, Pi21, Bsr-d1, and Xa5 to obtain broad-spectrum resistance rice against Xoo and M. oryzae [127]. In addition, it was well summarized that editing the open reading frame of susceptibility defense regulators could obtain broad-spectrum resistance rice plants in the Wang’s review (Figure 2b) [128].
Contrary to the interaction between TALEs and rice S genes, the usually suppressed executor R genes, such as Xa10 and Xa23, are transcriptionally activated by TALEs to restrict the growth of Xoo [28]. Using an in-depth understanding of the mechanism underlying the interaction between TALEs and executor R genes, a new strategy for engineering broad-spectrum bacterial blight resistance through CRISPR/Cas9-mediated precise homology directed repair was proposed. Using this strategy, the EBEAvrXa23, which is bound by TALE AvrXa23 to activate the expression of Xa23, was inserted into the promoter region of the susceptible xa23 allele in the susceptible rice cultivar, resulting in a resistant variety (Figure 2c) [129]. This is a significant expansion to the application of executor R genes and a new genome editing strategy in improving rice disease resistance.

3.3. Transgenic Rice Expressing Genes from Other Species Shows Broad-Spectrum Disease Resistance

Along with pyramiding resistance genes and editing susceptibility genes in rice, development of transgenic rice plants by expressing defense genes from other species is an appropriate approach to control pathogens, especial in the absence of a resistant germplasm. For instance, the Arabidopsis NPR1 protein (non-expressor of PR1) is a key regulator in the signal transduction pathway leading to the activation of SAR, which is a broad-spectrum resistance response upon exposure to a pathogen [130]. Constitutive expression of the AtNPR1 gene in rice leads to high resistance but growth and agronomic trait defects. To overcome this problem, different strategies were developed by two groups [130,131]. Eventually, broad-spectrum resistant rice plants without a fitness cost were obtained by expression of AtNPR1 driven by green tissue-specific promoter or pathogen-responsive upstream open reading frames of key immune regulators TBF1 [130,131]. Similarly, transgenic rice lines expressing the auto-activated NLR genes RPS2 and RPM1 (D505V) from Arabidopsis conferred broad-spectrum resistance to pathogens M. oryzae and Xoo via early and strong induction of ROS, callose deposition, and expression of defense-related genes. These RPS2 and RPM1 cases revealed that auto-activated NLRs are a promising resource for breeding crops with broad-spectrum resistance, and they provide new insights for engineering disease resistance [132]. In addition to genes from Arabidopsis, transgenic rice plants expressing resistant Lr34 allele from wheat showed increased resistance against multiple isolates of the hemibiotrophic pathogen M. oryzae by delaying invasive hyphal growth [133]. In another example, transgenic rice lines expressing the isoflavone synthase (GmIFS1) gene from soybean contributed to the synthesis of isoflavone (genistein) to promote M. oryzae resistance, indicating that the synthesis of heterologous secondary metabolites, such as isoflavone, is a good way to develop blast resistance in rice [134]. As such, we believe that engineering resistant rice through ectopic transcription of defense genes cloud be a broadly applicable new strategy, which may lead to reduced use of pesticides and lightening the selection pressure of resistance pathogens.

4. Conclusions

In the past 10 years, several broad-spectrum R genes, defense regulators, and QTLs were identified in rice with resistance against two or more types of pathogen species or many isolates of the same pathogen species. This emerging knowledge of broad-spectrum resistance genes formulates efficient ways to best use these genetic resources for crop improvement via biotechnological approaches. However, there are still many gaps in our knowledge of the mechanisms underlying broad-spectrum resistance. To reveal these mechanisms, more research about the interactions between the host R protein and pathogen effectors, as well as the cooperation among these broad-spectrum resistance genes, is required in future. Furthermore, there is still a long way to using these genes to create broad-spectrum disease-resistant varieties. An accurate understanding of R gene utilization, the establishment of high-throughput molecular breeding methods to create R genes harboring resistant germplasms without linkage drag, and an investigation of new strategies for using defense regulator genes without a yield penalty will be helpful for improving broad-spectrum resistance breeding in the future.

Funding

This research was supported in part by the Natural Science Foundation of China (32000103 to Y.K.) and the key R&D project of China National Rice Research Institute, grant number “CNRRI-2020-04”.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Acknowledgments

This project was also supported by the Chinese Academy of Agricultural Sciences under the “Elite Youth” program and the Agricultural Sciences and Technologies Innovation Program. We thank the Rice–Pathogen Interaction group of China National Rice Research Institute for helpful discussion and suggestions.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

References

  1. Kou, Y.; Wang, S. Broad-spectrum and durability: Understanding of quantitative disease resistance. Curr. Opin. Plant Biol. 2010, 13, 181–185. [Google Scholar] [CrossRef]
  2. Li, W.; Chern, M.; Yin, J.; Wang, J.; Chen, X. Recent advances in broad-spectrum resistance to the rice blast disease. Curr. Opin. Plant Biol. 2019, 50, 114–120. [Google Scholar] [CrossRef]
  3. Peng, Y.; Yang, J.; Li, X.; Zhang, Y. Salicylic acid: Biosynthesis and signaling. Annu. Rev. Plant Biol. 2021, 72, 761–791. [Google Scholar] [CrossRef]
  4. Das, A.; Soubam, D.; Singh, P.K.; Thakur, S.; Singh, N.K.; Sharma, T.R. A novel blast resistance gene, Pi54rh cloned from wild species of rice, Oryza rhizomatis confers broad spectrum resistance to Magnaporthe oryzae. Funct. Integr. Genom. 2012, 12, 215–228. [Google Scholar] [CrossRef]
  5. Liu, Y.; Liu, B.; Zhu, X.; Yang, J.; Bordeos, A.; Wang, G.; Leach, J.E.; Leung, H. Fine-mapping and molecular marker development for Pi56(t), a NBS-LRR gene conferring broad-spectrum resistance to Magnaporthe oryzae in rice. Theor. Appl. Genet. 2013, 126, 985–998. [Google Scholar] [CrossRef] [PubMed]
  6. Ma, J.; Lei, C.; Xu, X.; Hao, K.; Wang, J.; Cheng, Z.; Ma, X.; Ma, J.; Zhou, K.; Zhang, X.; et al. Pi64, encoding a novel CC-NBS-LRR protein, confers resistance to leaf and neck blast in rice. Mol. Plant-Microbe Interact. 2015, 28, 558–568. [Google Scholar] [CrossRef] [Green Version]
  7. Deng, Y.; Zhai, K.; Xie, Z.; Yang, D.; Zhu, X.; Liu, J.; Wang, X.; Qin, P.; Yang, Y.; Zhang, G. Epigenetic regulation of antagonistic receptors confers rice blast resistance with yield balance. Science 2017, 355, 962–965. [Google Scholar] [CrossRef]
  8. Xie, Z.; Yan, B.; Shou, J.; Tang, J.; Wang, X.; Zhai, K.; Liu, J.; Li, Q.; Luo, M.; Deng, Y.; et al. A nucleotide-binding site-leucine-rich repeat receptor pair confers broad-spectrum disease resistance through physical association in rice. Philos. Trans. R. Soc. B Biol. Sci. 2019, 374, 20180308. [Google Scholar] [CrossRef] [Green Version]
  9. Zhao, H.; Wang, X.; Jia, Y.; Minkenberg, B.; Wheatley, M.; Fan, J.; Jia, M.H.; Famoso, A.; Edwards, J.D.; Wamishe, Y.; et al. The rice blast resistance gene Ptr encodes an atypical protein required for broad-spectrum disease resistance. Nat. Commun. 2018, 9, 2039. [Google Scholar] [CrossRef] [PubMed]
  10. Meng, X.; Xiao, G.; Telebanco-Yanoria, M.J.; Siazon, P.M.; Padilla, J.; Opulencia, R.; Bigirimana, J.; Habarugira, G.; Wu, J.; Li, M.; et al. The broad-spectrum rice blast resistance (R) gene Pita2 encodes a novel R protein unique from Pita. Rice 2020, 13, 1–15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  11. Vasudevan, K.; Vera Cruz, C.M.; Gruissem, W.; Bhullar, N.K. Geographically distinct and domain-specific sequence variations in the alleles of rice blast resistance gene Pib. Front. Plant Sci. 2016, 7, 915. [Google Scholar] [CrossRef] [Green Version]
  12. Roychowdhury, M.; Jia, Y.; Jia, M.H.; Fjellstrom, R.; Cartwright, R.D. Identification of the rice blast resistance gene Pib in the national small grains collection. Phytopathology 2012, 102, 700–706. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Hua, L.; Wu, J.; Chen, C.; Wu, W.; He, X.; Lin, F.; Wang, L.; Ashikawa, I.; Matsumoto, T.; Wang, L.; et al. The isolation of Pi1, an allele at the Pik locus which confers broad spectrum resistance to rice blast. Theor. Appl. Genet. 2012, 125, 1047–1055. [Google Scholar] [CrossRef]
  14. Thakur, S.; Singh, P.K.; Das, A.; Rathour, R.; Variar, M.; Prashanthi, S.K.; Singh, A.K.; Singh, U.D.; Chand, D.; Singh, N.K.; et al. Extensive sequence variation in rice blast resistance gene Pi54 makes it broad spectrum in nature. Front. Plant Sci. 2015, 6, 345. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Meng, F.; He, Y.; Chen, J.; Long, X.; Wang, H.; Zhu, M.; Liu, S.; Cai, Q.; Zhang, Z. Analysis of natural variation of the rice blast resistance gene Pike and identification of a novel allele Pikg. Mol. Genet. Genom. 2021, 296, 939–952. [Google Scholar] [CrossRef] [PubMed]
  16. Liang, T.; Chi, W.; Huang, L.; Qu, M.; Zhang, S.; Chen, Z.Q.; Chen, Z.J.; Tian, D.; Gui, Y.; Chen, X.; et al. Bulked segregant analysis coupled with whole-genome sequencing (BSA-seq) mapping identifies a novel pi21 haplotype conferring basal resistance to rice blast disease. Int. J. Mol. Sci. 2020, 21, 2162. [Google Scholar] [CrossRef] [Green Version]
  17. Feng, X.; Lin, K.; Zhang, W.; Nan, J.; Zhang, X.; Wang, C.; Wang, R.; Jiang, G.; Yuan, Q.; Lin, S. Improving the blast resistance of the elite rice variety Kongyu-131 by updating the pi21 locus. BMC Plant Biol. 2019, 19, 1–12. [Google Scholar] [CrossRef]
  18. Zhou, Y.; Lei, F.; Wang, Q.; He, W.; Yuan, B.; Yuan, W. Identification of novel alleles of the rice blast-resistance gene Pi9 through sequence-based allele mining. Rice 2020, 13, 1–12. [Google Scholar] [CrossRef]
  19. Xiao, G.; Borja, F.N.; Mauleon, R.; Padilla, J.; Telebanco-Yanoria, M.J.; Yang, J.; Lu, G.; Dionisio-Sese, M.; Zhou, B. Identification of resistant germplasm containing novel resistance genes at or tightly linked to the Pi2/9 locus conferring broad-spectrum resistance against rice blast. Rice 2017, 10, 1–12. [Google Scholar] [CrossRef]
  20. Tian, D.; Chen, Z.; Chen, Z.; Zhou, Y.; Wang, Z.; Wang, F.; Chen, S. Allele-specific marker-based assessment revealed that the rice blast resistance genes Pi2 and Pi9 have not been widely deployed in Chinese indica rice cultivars. Rice 2016, 9, 1–11. [Google Scholar] [CrossRef] [Green Version]
  21. Imam, J.; Mandal, N.P.; Variar, M.; Shukla, P. Allele mining and selective patterns of Pi9 gene in a set of rice landraces from india. Front. Plant Sci. 2016, 7, 1846. [Google Scholar] [CrossRef] [Green Version]
  22. Su, J.; Wang, W.; Han, J.; Chen, S.; Wang, C.; Zeng, L.; Feng, A.; Yang, J.; Zhou, B.; Zhu, X. Functional divergence of duplicated genes results in a novel blast resistance gene Pi50 at the Pi2/9 locus. Theor. Appl. Genet. 2015, 128, 2213–2225. [Google Scholar] [CrossRef]
  23. Wu, Y.Y.; Bao, Y.M.; Xie, L.J.; Su, Y.Y.; Chu, R.Z.; He, W.W.; Huang, J.; Wang, J.F.; Zhang, H.S. Fine mapping and identification of blast resistance gene Pi-hk1 in a broad-spectrum resistant japonica rice landrace. Phytopathology 2013, 103, 1162–1168. [Google Scholar] [CrossRef] [Green Version]
  24. Dong, L.; Liu, S.; Xu, P.; Deng, W.; Li, X.; Tharreau, D.; Li, J.; Zhou, J.; Wang, Q.; Tao, D.; et al. Fine mapping of Pi57(t) conferring broad spectrum resistance against Magnaporthe oryzae in introgression line IL-E1454 derived from Oryza longistaminata. PLoS ONE 2017, 12, e0186201. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Zheng, W.; Wang, Y.; Wang, L.; Ma, Z.; Zhao, J.; Wang, P.; Zhang, L.; Liu, Z.; Lu, X. Genetic mapping and molecular marker development for Pi65(t), a novel broad-spectrum resistance gene to rice blast using next-generation sequencing. Theor. Appl. Genet. 2016, 129, 1035–1044. [Google Scholar] [CrossRef]
  26. Dong, L.; Liu, S.; Kyaing, M.S.; Xu, P.; Tharreau, D.; Deng, W.; Li, X.; Bi, Y.; Zeng, L.; Li, J.; et al. Identification and fine mapping of Pi69(t), a new gene conferring broad-spectrum resistance against Magnaporthe oryzae from Oryza glaberrima steud. Front. Plant Sci. 2020, 11, 1190. [Google Scholar] [CrossRef] [PubMed]
  27. 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]
  28. 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] [PubMed] [Green Version]
  29. Hutin, M.; Sabot, F.; Ghesquiere, A.; Koebnik, R.; Szurek, B. A knowledge-based molecular screen uncovers a broad-spectrum OsSWEET14 resistance allele to bacterial blight from wild rice. Plant J. 2015, 84, 694–703. [Google Scholar] [CrossRef] [PubMed]
  30. Xing, J.; Zhang, D.; Yin, F.; Zhong, Q.; Wang, B.; Xiao, S.; Ke, X.; Wang, L.; Zhang, Y.; Zhao, C.; et al. Identification and fine-mapping of a new bacterial blight resistance gene, Xa47(t), in G252, an introgression line of yuanjiang common wild rice (Oryza rufipogon). Plant Dis. 2021. [Google Scholar] [CrossRef]
  31. Du, D.; Zhang, C.; Xing, Y.; Lu, X.; Cai, L.; Yun, H.; Zhang, Q.; Zhang, Y.; Chen, X.; Liu, M.; et al. The CC-NB-LRR OsRLR1 mediates rice disease resistance through interaction with OsWRKY19. Plant Biotechnol. J. 2021, 19, 1052–1064. [Google Scholar] [CrossRef]
  32. Li, D.; Li, S.; Wei, S.; Sun, W. Strategies to manage rice sheath blight: Lessons from interactions between rice and Rhizoctonia solani. Rice 2021, 14, 1–15. [Google Scholar] [CrossRef] [PubMed]
  33. Sun, W.; Fan, J.; Fang, A.; Li, Y.; Tariqjaveed, M.; Li, D.; Hu, D.; Wang, W.M. Ustilaginoidea virens: Insights into an emerging rice pathogen. Annu. Rev. Phytopathol. 2020, 58, 363–385. [Google Scholar] [CrossRef]
  34. Wang, Q.; Liu, Y.; He, J.; Zheng, X.; Hu, J.; Liu, Y.; Dai, H.; Zhang, Y.; Wang, B.; Wu, W.; et al. STV11 encodes a sulphotransferase and confers durable resistance to rice stripe virus. Nat. Commun. 2014, 5, 4768. [Google Scholar] [CrossRef]
  35. Wu, J.; Kou, Y.; Bao, J.; Li, Y.; Tang, M.; Zhu, X.; Ponaya, A.; Xiao, G.; Li, J.; Li, C.; et al. Comparative genomics identifies the Magnaporthe oryzae avirulence effector AvrPi9 that triggers Pi9-mediated blast resistance in rice. New Phytol. 2015, 206, 1463–1475. [Google Scholar] [CrossRef] [PubMed]
  36. Zhu, Z.; Yin, J.; Chern, M.; Zhu, X.; Yang, C.; He, K.; Liu, Y.; He, M.; Wang, J.; Song, L.; et al. New insights into bsr-d1-mediated broad-spectrum resistance to rice blast. Mol. Plant Pathol. 2020, 21, 951–960. [Google Scholar] [CrossRef]
  37. Li, W.; Zhu, Z.; Chern, M.; Yin, J.; Yang, C.; Ran, L.; Cheng, M.; He, M.; Wang, K.; Wang, J.; et al. A natural allele of a transcription factor in rice confers broad-spectrum blast resistance. Cell 2017, 170, 114–126. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  38. Li, W.T.; Wang, K.; Chern, M.; Liu, Y.C.; Zhu, Z.W.; Liu, J.; Zhu, X.B.; Yin, J.J.; Ran, L.; Xiong, J.; et al. Sclerenchyma cell thickening through enhanced lignification induced by OsMYB30 prevents fungal penetration of rice leaves. New Phytol. 2020, 226, 1850–1863. [Google Scholar] [CrossRef] [PubMed]
  39. Wang, Z.; Xia, Y.; Lin, S.; Wang, Y.; Guo, B.; Song, X.; Ding, S.; Zheng, L.; Feng, R.; Chen, S.; et al. Osa-miR164a targets OsNAC60 and negatively regulates rice immunity against the blast fungus Magnaporthe oryzae. Plant J. 2018, 95, 584–597. [Google Scholar] [CrossRef] [Green Version]
  40. Inoue, H.; Hayashi, N.; Matsushita, A.; Xinqiong, L.; Nakayama, A.; Sugano, S.; Jiang, C.J.; Takatsuji, H. Blast resistance of CC-NB-LRR protein Pb1 is mediated by WRKY45 through protein-protein interaction. Proc. Natl. Acad. Sci. USA 2013, 110, 9577–9582. [Google Scholar] [CrossRef] [Green Version]
  41. Zhai, K.R.; Deng, Y.W.; Liang, D.; Tang, J.; Liu, J.; Yan, B.X.; Yin, X.; Lin, H.; Chen, F.D.; Yang, D.Y.; et al. RRM transcription factors Interact with NLRs and regulate broad-spectrum blast resistance in rice. Mol. Cell 2019, 74, 996–1009.e7. [Google Scholar] [CrossRef]
  42. Li, W.; Zhong, S.; Li, G.; Li, Q.; Mao, B.; Deng, Y.; Zhang, H.; Zeng, L.; Song, F.; He, Z. Rice RING protein OsBBI1 with E3 ligase activity confers broad-spectrum resistance against Magnaporthe oryzae by modifying the cell wall defence. Cell Res. 2011, 21, 835–848. [Google Scholar] [CrossRef]
  43. Liu, M.X.; Zhang, S.B.; Hu, J.X.; Sun, W.X.; Padilla, J.; He, Y.L.; Li, Y.; Yin, Z.Y.; Liu, X.Y.; Wang, W.H.; et al. Phosphorylation-guarded light-harvesting complex II contributes to broad-spectrum blast resistance in rice. Proc. Natl. Acad. Sci. USA 2019, 116, 17572–17577. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Jiang, Y.; Chen, X.; Ding, X.; Wang, Y.; Chen, Q.; Song, W.Y. The XA21 binding protein XB25 is required for maintaining XA21-mediated disease resistance. Plant J. 2013, 73, 814–823. [Google Scholar] [CrossRef]
  45. Park, C.-J.; Song, M.-Y.; Kim, C.-Y.; Jeon, J.-S.; Ronald, P.C. Rice bip3 regulates immunity mediated by the PRRs XA3 and XA21 but not immunity mediated by the NB-LRR protein, Pi5. Biochem. Biophys. Res. Commun. 2014, 448, 70–75. [Google Scholar] [CrossRef]
  46. Feng, J.X.; Cao, L.; Li, J.; Duan, C.J.; Luo, X.M.; Le, N.; Wei, H.H.; Liang, S.J.; Chu, C.C.; Pan, Q.H.; et al. Involvement of OsNPR1/NH1 in rice basal resistance to blast fungus Magnaporthe oryzae. Eur. J. Plant Pathol. 2011, 131, 221–235. [Google Scholar] [CrossRef]
  47. Chern, M.; Xu, Q.; Bart, R.S.; Bai, W.; Ruan, D.; Sze-To, W.H.; Canlas, P.E.; Jain, R.; Chen, X.; Ronald, P.C. A genetic screen identifies a requirement for cysteine-rich-receptor-like kinases in rice NH1 (OsNPR1)-mediated immunity. PLoS Genet. 2016, 12, e1006049. [Google Scholar] [CrossRef]
  48. He, S.L.; Jiang, J.Z.; Chen, B.H.; Kuo, C.H.; Ho, S.L. Overexpression of a constitutively active truncated form of OsCDPK1 confers disease resistance by affecting OsPR10a expression in rice. Sci. Rep. 2018, 8, 403. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  49. Chen, J.; Wang, L.; Yang, Z.; Liu, H.; Chu, C.; Zhang, Z.; Zhang, Q.; Li, X.; Xiao, J.; Wang, S.; et al. The rice Raf-like MAPKKK OsILA1 confers broad-spectrum resistance to bacterial blight by suppressing the OsMAPKK4-OsMAPK6 cascade. J. Integr. Plant Biol. 2021, 63, 1815–1842. [Google Scholar] [CrossRef]
  50. Chen, H.; Li, C.; Liu, L.; Zhao, J.; Cheng, X.; Jiang, G.; Zhai, W. The Fd-GOGAT1 mutant gene lc7 confers resistance to Xanthomonas oryzae pv. oryzae in rice. Sci. Rep. 2016, 6, 1–13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  51. Liu, B.; Li, J.F.; Ao, Y.; Qu, J.W.; Li, Z.Q.; Su, J.B.; Zhang, Y.; Liu, J.; Feng, D.R.; Qi, K.B.; et al. Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 2012, 24, 3406–3419. [Google Scholar] [CrossRef] [Green Version]
  52. Vo, K.T.X.; Kim, C.Y.; Hoang, T.V.; Lee, S.K.; Shirsekar, G.; Seo, Y.S.; Lee, S.W.; Wang, G.L.; Jeon, J.S. OsWRKY67 plays a positive role in basal and XA21-mediated resistance in rice. Front. Plant Sci. 2017, 8, 2220. [Google Scholar] [CrossRef] [Green Version]
  53. Liu, M.M.; Shi, Z.Y.; Zhang, X.H.; Wang, M.X.; Zhang, L.; Zheng, K.Z.; Liu, J.Y.; Hu, X.M.; Di, C.R.; Qian, Q.; et al. Inducible overexpression of Ideal Plant Architecture1 improves both yield and disease resistance in rice. Nat. Plants 2019, 5, 902. [Google Scholar] [CrossRef] [PubMed]
  54. Wang, J.; Zhou, L.; Shi, H.; Chern, M.; Yu, H.; Yi, H.; He, M.; Yin, J.J.; Zhu, X.B.; Li, Y.; et al. A single transcription factor promotes both yield and immunity in rice. Science 2018, 361, 1026–1028. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  55. Hui, S.; Liu, H.; Zhang, M.; Chen, D.; Li, Q.; Tian, J.; Xiao, J.; Li, X.; Wang, S.; Yuan, M. The host basal transcription factor IIA subunits coordinate for facilitating infection of TALEs-carrying bacterial pathogens in rice. Plant Sci. 2019, 284, 48–56. [Google Scholar] [CrossRef]
  56. Liu, Q.; Yang, J.; Yan, S.; Zhang, S.; Zhao, J.; Wang, W.; Yang, T.; Wang, X.; Mao, X.; Dong, J.; et al. The germin-like protein OsGLP2-1 enhances resistance to fungal blast and bacterial blight in rice. Plant Mol. Biol. 2016, 92, 411–423. [Google Scholar] [CrossRef]
  57. Filipe, O.; De Vleesschauwer, D.; Haeck, A.; Demeestere, K.; Hofte, M. The energy sensor OsSnRK1a confers broad-spectrum disease resistance in rice. Sci. Rep. 2018, 8, 3864. [Google Scholar] [CrossRef] [Green Version]
  58. Kim, C.-Y.; Vo, K.T.X.; An, G.; Jeon, J.-S. A rice sucrose non-fermenting-1 related protein kinase 1, OSK35, plays an important role in fungal and bacterial disease resistance. J. Korean Soc. Appl. Biol. Chem. 2015, 58, 669–675. [Google Scholar] [CrossRef]
  59. Wang, J.; Wang, S.; Hu, K.; Yang, J.; Xin, X.; Zhou, W.; Fan, J.; Cui, F.; Mou, B.; Zhang, S.; et al. The calcium-dependent protein kinase OsCPK4 regulates a buffering mechanism that fine-tunes innate immunity in rice. Phytopathology 2018, 108, 35. [Google Scholar]
  60. Kanda, Y.; Nishizawa, Y.; Kamakura, T.; Mori, M. Overexpressed BSR1-mediated enhancement of disease resistance depends on the MAMP-recognition system. Int. J. Mol. Sci. 2020, 21, 5397. [Google Scholar] [CrossRef]
  61. You, Q.; Zhai, K.; Yang, D.; Yang, W.; Wu, J.; Liu, J.; Pan, W.; Wang, J.; Zhu, X.; Jian, Y.; et al. An E3 ubiquitin ligase-bag protein module controls plant innate immunity and broad-spectrum disease resistance. Cell Host Microbe 2016, 20, 758–769. [Google Scholar] [CrossRef] [Green Version]
  62. Liu, J.; Park, C.H.; He, F.; Nagano, M.; Wang, M.; Bellizzi, M.; Zhang, K.; Zeng, X.; Liu, W.; Ning, Y.; et al. The RhoGAP SPIN6 associates with SPL11 and OsRac1 and negatively regulates programmed cell death and innate immunity in rice. PLoS Pathog. 2015, 11, e1004629. [Google Scholar] [CrossRef]
  63. Harkenrider, M.; Sharma, R.; De Vleesschauwer, D.; Tsao, L.; Zhang, X.T.; Chern, M.; Canlas, P.; Zuo, S.M.; Ronald, P.C. Overexpression of rice wall-associated kinase 25 (OsWAK25) alters resistance to bacterial and fungal pathogens. PLoS ONE 2016, 11, e0147310. [Google Scholar] [CrossRef] [Green Version]
  64. Liu, Q.E.; Ning, Y.S.; Zhang, Y.X.; Yu, N.; Zhao, C.D.; Zhan, X.D.; Wu, W.X.; Chen, D.B.; Wei, X.J.; Wang, G.L.; et al. OsCUL3a negatively regulates cell death and immunity by degrading OsNPR1 in rice. Plant Cell 2017, 29, 345–359. [Google Scholar] [CrossRef] [Green Version]
  65. Li, Z.; Ding, B.; Zhou, X.; Wang, G.L. The rice dynamin-related protein OsDRP1E negatively regulates programmed cell death by controlling the release of cytochrome c from mitochondria. PLoS Pathog. 2017, 13, e1006157. [Google Scholar] [CrossRef]
  66. Wang, S.; Lei, C.; Wang, J.; Ma, J.; Tang, S.; Wang, C.; Zhao, K.; Tian, P.; Zhang, H.; Qi, C.; et al. SPL33, encoding an eEF1A-like protein, negatively regulates cell death and defense responses in rice. J. Exp. Bot. 2017, 68, 899–913. [Google Scholar] [CrossRef]
  67. Zhao, J.; Liu, P.; Li, C.; Wang, Y.; Guo, L.; Jiang, G.; Zhai, W. LMM5.1 and LMM5.4, two eukaryotic translation elongation factor 1A-like gene family members, negatively affect cell death and disease resistance in rice. J. Genet. Genom. 2017, 44, 107–118. [Google Scholar] [CrossRef]
  68. Qin, P.; Fan, S.; Deng, L.; Zhong, G.; Zhang, S.; Li, M.; Chen, W.; Wang, G.; Tu, B.; Wang, Y.; et al. LML1, encoding a conserved eukaryotic release factor 1 protein, regulates cell death and pathogen resistance by forming a conserved complex with SPL33 in rice. Plant Cell Physiol. 2018, 59, 887–902. [Google Scholar] [CrossRef] [Green Version]
  69. Liao, Y.; Bai, Q.; Xu, P.; Wu, T.; Guo, D.; Peng, Y.; Zhang, H.; Deng, X.; Chen, X.; Luo, M.; et al. Mutation in rice abscisic acid2 results in cell death, enhanced disease-resistance, altered seed dormancy and development. Front. Plant Sci. 2018, 9, 405. [Google Scholar] [CrossRef] [Green Version]
  70. Ma, J.; Wang, Y.; Ma, X.; Meng, L.; Jing, R.; Wang, F.; Wang, S.; Cheng, Z.; Zhang, X.; Jiang, L.; et al. Disruption of gene SPL35, encoding a novel CUE domain-containing protein, leads to cell death and enhanced disease response in rice. Plant Biotechnol. J. 2019, 17, 1679–1693. [Google Scholar] [CrossRef] [Green Version]
  71. Ding, B.; Bellizzi Mdel, R.; Ning, Y.; Meyers, B.C.; Wang, G.L. HDT701, a histone H4 deacetylase, negatively regulates plant innate immunity by modulating histone H4 acetylation of defense-related genes in rice. Plant Cell 2012, 24, 3783–3794. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  72. Hong, Y.; Liu, Q.; Cao, Y.; Zhang, Y.; Chen, D.; Lou, X.; Cheng, S.; Cao, L. The Osmpk15 negatively regulates Magnaporthe oryza and Xoo disease resistance via SA and JA signaling pathway in rice. Front. Plant Sci. 2019, 10, 752. [Google Scholar] [CrossRef] [PubMed]
  73. Zhou, X.; Liao, H.; Chern, M.; Yin, J.; Chen, Y.; Wang, J.; Zhu, X.; Chen, Z.; Yuan, C.; Zhao, W.; et al. Loss of function of a rice TPR-domain RNA-binding protein confers broad-spectrum disease resistance. Proc. Natl. Acad. Sci. USA 2018, 115, 3174–3179. [Google Scholar] [CrossRef] [Green Version]
  74. Ke, Y.; Yuan, M.; Liu, H.; Hui, S.; Qin, X.; Chen, J.; Zhang, Q.; Li, X.; Xiao, J.; Zhang, Q.; et al. The versatile functions of OsALDH2B1 provide a genic basis for growth-defense trade-offs in rice. Proc. Natl. Acad. Sci. USA 2020, 117, 3867–3873. [Google Scholar] [CrossRef] [PubMed]
  75. Tonnessen, B.W.; Manosalva, P.; Lang, J.M.; Baraoidan, M.; Bordeos, A.; Mauleon, R.; Oard, J.; Hulbert, S.; Leung, H.; Leach, J.E. Rice phenylalanine ammonia-lyase gene OsPAL4 is associated with broad spectrum disease resistance. Plant Mol. Biol. 2015, 87, 273–286. [Google Scholar] [CrossRef]
  76. Yang, W.; Ju, Y.; Zuo, L.; Shang, L.; Li, X.; Li, X.; Feng, S.; Ding, X.; Chu, Z. OsHsfB4d binds the promoter and regulates the expression of oshsp18.0-ci to resistant against Xanthomonas oryzae. Rice 2020, 13, 28. [Google Scholar] [CrossRef]
  77. Ju, Y.; Tian, H.; Zhang, R.; Zuo, L.; Jin, G.; Xu, Q.; Ding, X.; Li, X.; Chu, Z. Overexpression of OsHSP18.0-CI enhances resistance to bacterial leaf streak in rice. Rice 2017, 10, 12. [Google Scholar] [CrossRef] [Green Version]
  78. Ke, Y.; Liu, H.; Li, X.; Xiao, J.; Wang, S. Rice OsPAD4 functions differently from Arabidopsis AtPAD4 in host-pathogen interactions. Plant J. 2014, 78, 619–631. [Google Scholar] [CrossRef]
  79. Son, S.; Kim, H.; Lee, K.S.; Kim, S.; Park, S.R. Rice glutaredoxin GRXS15 confers broad-spectrum resistance to Xanthomonas oryzae pv. oryzae and Fusarium fujikuroi. Biochem. Biophys. Res. Commun. 2020, 533, 1385–1392. [Google Scholar] [CrossRef]
  80. Son, S.; Moon, S.J.; Kim, H.; Lee, K.S.; Park, S.R. Identification of a novel NPR1 homolog gene, OsNH5N16, which contributes to broad-spectrum resistance in rice. Biochem. Biophys. Res. Commun. 2021, 549, 200–206. [Google Scholar] [CrossRef]
  81. Li, N.; Wei, S.; Chen, J.; Yang, F.; Kong, L.; Chen, C.; Ding, X.; Chu, Z. OsASR2 regulates the expression of a defence-related gene, Os2H16, by targeting the GT-1 cis-element. Plant Biotechnol. J. 2018, 16, 771–783. [Google Scholar] [CrossRef] [Green Version]
  82. Li, N.; Kong, L.; Zhou, W.; Zhang, X.; Wei, S.; Ding, X.; Chu, Z. Overexpression of Os2H16 enhances resistance to phytopathogens and tolerance to drought stress in rice. Plant Cell Tissue Organ Cult. 2013, 115, 429–441. [Google Scholar] [CrossRef]
  83. Manosalva, P.M.; Bruce, M.; Leach, J.E. Rice 14-3-3 protein (GF14e) negatively affects cell death and disease resistance. Plant J. 2011, 68, 777–787. [Google Scholar] [CrossRef] [PubMed]
  84. Peng, X.; Hu, Y.; Tang, X.; Zhou, P.; Deng, X.; Wang, H.; Guo, Z. Constitutive expression of rice WRKY30 gene increases the endogenous jasmonic acid accumulation, PR gene expression and resistance to fungal pathogens in rice. Planta 2012, 236, 1485–1498. [Google Scholar] [CrossRef]
  85. Helliwell, E.E.; Wang, Q.; Yang, Y. Transgenic rice with inducible ethylene production exhibits broad-spectrum disease resistance to the fungal pathogens Magnaporthe oryzae and Rhizoctonia solani. Plant Biotechnol. J. 2013, 11, 33–42. [Google Scholar] [CrossRef]
  86. Hu, B.; Zhou, Y.; Zhou, Z.; Sun, B.; Zhou, F.; Yin, C.; Ma, W.; Chen, H.; Lin, Y. Repressed OsMESL expression triggers reactive oxygen species-mediated broad-spectrum disease resistance in rice. Plant Biotechnol. J. 2021, 19, 1511–1522. [Google Scholar] [CrossRef]
  87. Yin, X.; Zou, B.; Hong, X.; Gao, M.; Yang, W.; Zhong, X.; He, Y.; Kuai, P.; Lou, Y.; Huang, J.; et al. Rice copine genes OsBON1 and OsBON3 function as suppressors of broad-spectrum disease resistance. Plant Biotechnol. J. 2018, 16, 1476–1487. [Google Scholar] [CrossRef]
  88. Bossa-Castro, A.M.; Tekete, C.; Raghavan, C.; Delorean, E.E.; Dereeper, A.; Dagno, K.; Koita, O.; Mosquera, G.; Leung, H.; Verdier, V.; et al. Allelic variation for broad-spectrum resistance and susceptibility to bacterial pathogens identified in a rice MAGIC population. Plant Biotechnol. J. 2018, 16, 1559–1568. [Google Scholar] [CrossRef] [Green Version]
  89. Shi, X.; Wang, J.; Bao, Y.; Li, P.; Xie, L.; Huang, J.; Zhang, H. Identification of the quantitative trait loci in japonica rice landrace Heikezijing responsible for broad-spectrum resistance to rice blast. Phytopathology 2010, 100, 822–829. [Google Scholar] [CrossRef] [Green Version]
  90. Liu, Y.; Qi, X.; Gealy, D.R.; Olsen, K.M.; Caicedo, A.L.; Jia, Y. QTL analysis for resistance to blast disease in U.S. weedy rice. Mol. Plant-Microbe Interact. 2015, 28, 834–844. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  91. Sattayachiti, W.; Wanchana, S.; Arikit, S.; Nubankoh, P.; Patarapuwadol, S.; Vanavichit, A.; Darwell, C.T.; Toojinda, T. Genome-wide association analysis identifies resistance loci for bacterial leaf streak resistance in rice (Oryza sativa L.). Plants 2020, 9, 1673. [Google Scholar] [CrossRef]
  92. Korinsak, S.; Darwell, C.T.; Wanchana, S.; Praphaisal, L.; Korinsak, S.; Thunnom, B.; Patarapuwadol, S.; Toojinda, T. Identification of bacterial blight resistance loci in rice (Oryza sativa L.) against diverse Xoo thai strains by genome-wide association study. Plants 2021, 10, 518. [Google Scholar] [CrossRef] [PubMed]
  93. Kumar, I.S.; Nadarajah, K. A meta-analysis of quantitative trait loci associated with multiple disease resistance in rice (Oryza sativa L.). Plants 2020, 9, 1491. [Google Scholar] [CrossRef] [PubMed]
  94. Miah, G.; Rafii, M.Y.; Ismail, M.R.; Puteh, A.B.; Rahim, H.A.; Latif, M.A. Marker-assisted introgression of broad-spectrum blast resistance genes into the cultivated MR219 rice variety. J. Sci. Food Agric. 2017, 97, 2810–2818. [Google Scholar] [CrossRef]
  95. Jiang, H.; Li, Z.; Liu, J.; Shen, Z.; Gao, G.; Zhang, Q.; He, Y. Development and evaluation of improved lines with broad-spectrum resistance to rice blast using nine resistance genes. Rice 2019, 12, 29. [Google Scholar] [CrossRef] [Green Version]
  96. Jain, P.; Dubey, H.; Singh, P.K.; Solanke, A.U.; Singh, A.K.; Sharma, T.R. Deciphering signalling network in broad spectrum near isogenic lines of rice resistant to Magnaporthe oryzae. Sci. Rep. 2019, 9, 16939. [Google Scholar] [CrossRef]
  97. Wu, Y.; Xiao, N.; Chen, Y.; Yu, L.; Pan, C.; Li, Y.; Zhang, X.; Huang, N.; Ji, H.; Dai, Z.; et al. Comprehensive evaluation of resistance effects of pyramiding lines with different broad-spectrum resistance genes against Magnaporthe oryzae in rice (Oryza sativa L.). Rice 2019, 12, 1–13. [Google Scholar] [CrossRef]
  98. Yang, D.; Tang, J.; Yang, D.; Chen, Y.; Ali, J.; Mou, T. Improving rice blast resistance of Feng39S through molecular marker-assisted backcrossing. Rice 2019, 12, 1–16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  99. Wang, L.; Zhao, L.; Zhang, X.; Zhang, Q.; Jia, Y.; Wang, G.; Li, S.; Tian, D.; Li, W.H.; Yang, S. Large-scale identification and functional analysis of NLR genes in blast resistance in the Tetep rice genome sequence. Proc. Natl. Acad. Sci. USA 2019, 116, 18479–18487. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  100. Ramalingam, J.; Palanisamy, S.; Alagarasan, G.; Renganathan, V.G.; Ramanathan, A.; Saraswathi, R. Improvement of stable restorer lines for blast resistance through functional marker in rice (Oryza sativa L.). Genes 2020, 11, 1266. [Google Scholar] [CrossRef] [PubMed]
  101. Peng, M.; Lin, X.; Xiang, X.; Ren, H.; Fan, X.; Chen, K. Characterization and evaluation of transgenic rice pyramided with the Pi Genes Pib, Pi25 and Pi54. Rice 2021, 14, 1–14. [Google Scholar] [CrossRef]
  102. Suh, J.P.; Jeung, J.U.; Noh, T.H.; Cho, Y.C.; Park, S.H.; Park, H.S.; Shin, M.S.; Kim, C.K.; Jena, K.K. Development of breeding lines with three pyramided resistance genes that confer broad-spectrum bacterial blight resistance and their molecular analysis in rice. Rice 2013, 6, 1–11. [Google Scholar] [CrossRef] [Green Version]
  103. Pradhan, S.K.; Nayak, D.K.; Mohanty, S.; Behera, L.; Barik, S.R.; Pandit, E.; Lenka, S.; Anandan, A. Pyramiding of three bacterial blight resistance genes for broad-spectrum resistance in deepwater rice variety, Jalmagna. Rice 2015, 8, 1–14. [Google Scholar] [CrossRef] [PubMed]
  104. Ramalingam, J.; Savitha, P.; Alagarasan, G.; Saraswathi, R.; Chandrababu, R. Functional marker assisted improvement of stable cytoplasmic male sterile lines of rice for bacterial blight resistance. Front. Plant Sci. 2017, 8, 1131. [Google Scholar] [CrossRef] [Green Version]
  105. Gao, L.; Fang, Z.; Zhou, J.; Li, L.; Lu, L.; Li, L.; Li, T.; Chen, L.; Zhang, W.; Zhai, W.; et al. Transcriptional insights into the pyramided resistance to rice bacterial blight. Sci. Rep. 2018, 8, 12358. [Google Scholar] [CrossRef] [PubMed]
  106. Ch, B.; Hk, M.S.; Sk, H.; Rr, K.; Mbvn, K.; Vp, B.; As, H.; Gs, L.; Sm, B.; Ms, M. Marker-assisted pyramiding of two major, broad-spectrum bacterial blight resistance genes, Xa21 and Xa33 into an elite maintainer line of rice, DRR17B. PLoS ONE 2018, 13, e0201271. [Google Scholar]
  107. Wang, S.; Liu, W.; Lu, D.; Lu, Z.; Wang, X.; Xue, J.; He, X. Distribution of bacterial blight resistance genes in the main cultivars and application of Xa23 in rice breeding. Front. Plant Sci. 2020, 11, 555228. [Google Scholar] [CrossRef]
  108. 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] [Green Version]
  109. Mi, J.; Yang, D.; Chen, Y.; Jiang, J.; Mou, H.; Huang, J.; Ouyang, Y.; Mou, T. Accelerated molecular breeding of a novel P/TGMS line with broad-spectrum resistance to rice blast and bacterial blight in two-line hybrid rice. Rice 2018, 11, 1–12. [Google Scholar] [CrossRef]
  110. Ramalingam, J.; Raveendra, C.; Savitha, P.; Vidya, V.; Chaithra, T.L.; Velprabakaran, S.; Saraswathi, R.; Ramanathan, A.; Arumugam Pillai, M.P.; Arumugachamy, S.; et al. Gene pyramiding for achieving enhanced resistance to bacterial blight, blast, and sheath blight diseases in rice. Front. Plant Sci. 2020, 11, 591457. [Google Scholar] [CrossRef]
  111. Ashkani, S.; Rafii, M.Y.; Shabanimofrad, M.; Miah, G.; Sahebi, M.; Azizi, P.; Tanweer, F.A.; Akhtar, M.S.; Nasehi, A. Molecular breeding strategy and challenges towards improvement of blast disease resistance in rice crop. Front. Plant Sci. 2015, 6, 886. [Google Scholar] [CrossRef] [Green Version]
  112. Ning, X.; Yunyu, W.; Aihong, L. Strategy for use of rice blast resistance genes in rice molecular breeding. Rice Sci. 2020, 27, 263–277. [Google Scholar] [CrossRef]
  113. Zaidi, S.S.; Mukhtar, M.S.; Mansoor, S. Genome editing: Targeting susceptibility genes for plant disease resistance. Trends Biotechnol. 2018, 36, 898–906. [Google Scholar] [CrossRef]
  114. Fukuoka, S.; Saka, N.; Koga, H.; Ono, K.; Shimizu, T.; Ebana, K.; Hayashi, N.; Takahashi, A.; Hirochika, H.; Okuno, K.; et al. Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 2009, 325, 998–1001. [Google Scholar] [CrossRef] [PubMed]
  115. Iyer, A.S.; McCouch, S.R. The rice bacterial blight resistance gene xa5 encodes a novel form of disease resistance. Mol. Plant-Microbe Interact. 2004, 17, 1348–1354. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  116. 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 TFIIAγ1. Mol. Genet. Genom. 2006, 275, 354–366. [Google Scholar] [CrossRef]
  117. Antony, G.; Zhou, J.H.; 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] [Green Version]
  118. 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] [PubMed] [Green Version]
  119. 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]
  120. Liu, Q.S.; Yuan, M.; Zhou, Y.; Li, X.H.; Xiao, J.H.; Wang, S.P. A paralog of the MtN3/saliva family recessively confers race-specific resistance to Xanthomonas oryzae in rice. Plant Cell Environ. 2011, 34, 1958–1969. [Google Scholar] [CrossRef]
  121. 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]
  122. Tian, J.; Xu, G.; Yuan, M. Precise editing enables crop broad-spectrum resistance. Mol. Plant 2019, 12, 1542–1544. [Google Scholar] [CrossRef] [PubMed]
  123. 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] [Green Version]
  124. Oliva, R.; Ji, C.; Atienza-Grande, G.; Huguet-Tapia, J.C.; Perez-Quintero, A.; Li, T.; Eom, J.S.; Li, C.; Nguyen, H.; Liu, B.; et al. Broad-spectrum resistance to bacterial blight in rice using genome editing. Nat. Biotechnol. 2019, 37, 1344–1350. [Google Scholar] [CrossRef] [Green Version]
  125. Zafar, K.; Khan, M.Z.; Amin, I.; Mukhtar, Z.; Yasmin, S.; Arif, M.; Ejaz, K.; Mansoor, S. Precise CRISPR-Cas9 mediated genome editing in super basmati rice for resistance against bacterial blight by targeting the major susceptibility gene. Front. Plant Sci. 2020, 11, 575. [Google Scholar] [CrossRef] [PubMed]
  126. Zeng, X.; Luo, Y.; Vu, N.T.Q.; Shen, S.; Xia, K.; Zhang, M. CRISPR/Cas9-mediated mutation of OsSWEET14 in rice cv. Zhonghua11 confers resistance to Xanthomonas oryzae pv. oryzae without yield penalty. BMC Plant Biol. 2020, 20, 1–11. [Google Scholar] [CrossRef]
  127. Tao, H.; Shi, X.; He, F.; Wang, D.; Xiao, N.; Fang, H.; Wang, R.; Zhang, F.; Wang, M.; Li, A.; et al. Engineering broad-spectrum disease-resistant rice by editing multiple susceptibility genes. J. Integr. Plant Biol. 2021, 63, 1639–1648. [Google Scholar] [CrossRef]
  128. Li, W.; Deng, Y.; Ning, Y.; He, Z.; Wang, G.L. Exploiting broad-spectrum disease resistance in crops: From molecular dissection to breeding. Annu. Rev. Plant Biol. 2020, 71, 575–603. [Google Scholar] [CrossRef] [Green Version]
  129. Wei, Z.; Abdelrahman, M.; Gao, Y.; Ji, Z.; Mishra, R.; Sun, H.; Sui, Y.; Wu, C.; Wang, C.; Zhao, K. Engineering broad-spectrum resistance to bacterial blight by CRISPR-Cas9-mediated precise homology directed repair in rice. Mol. Plant 2021, 14, 1215–1218. [Google Scholar] [CrossRef]
  130. Molla, K.A.; Karmakar, S.; Chanda, P.K.; Sarkar, S.N.; Datta, S.K.; Datta, K. Tissue-specific expression of Arabidopsis NPR1 gene in rice for sheath blight resistance without compromising phenotypic cost. Plant Sci. 2016, 250, 105–114. [Google Scholar] [CrossRef]
  131. Xu, G.; Yuan, M.; Ai, C.; Liu, L.; Zhuang, E.; Karapetyan, S.; Wang, S.; Dong, X. uORF-mediated translation allows engineered plant disease resistance without fitness costs. Nature 2017, 545, 491–494. [Google Scholar] [CrossRef]
  132. Li, Z.; Huang, J.; Wang, Z.; Meng, F.; Zhang, S.; Wu, X.; Zhang, Z.; Gao, Z. Overexpression of Arabidopsis nucleotide-binding and leucine-rich repeat genes RPS2 and RPM1(D505V) confers broad-spectrum disease resistance in rice. Front. Plant Sci. 2019, 10, 417. [Google Scholar] [CrossRef] [PubMed]
  133. Krattinger, S.G.; Sucher, J.; Selter, L.L.; Chauhan, H.; Zhou, B.; Tang, M.; Upadhyaya, N.M.; Mieulet, D.; Guiderdoni, E.; Weidenbach, D.; et al. The wheat durable, multipathogen resistance gene Lr34 confers partial blast resistance in rice. Plant Biotechnol. J. 2016, 14, 1261–1268. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  134. Pokhrel, S.; Ponniah, S.K.; Jia, Y.; Yu, O.; Manoharan, M. Transgenic rice expressing isoflavone synthase gene from soybean shows resistance against blast fungus (Magnaporthe oryzae). Plant Dis. 2021. [Google Scholar] [CrossRef] [PubMed]
Ijms 22 11658 g001 550
Figure 1. R and defense regulator genes with broad-spectrum disease resistance identified in past 10 years. The R genes are represented in bold black font. The black dots on each chromosome represent centromeres.
Figure 1. R and defense regulator genes with broad-spectrum disease resistance identified in past 10 years. The R genes are represented in bold black font. The black dots on each chromosome represent centromeres.
Ijms 22 11658 g001
Ijms 22 11658 g002 550
Figure 2. Engineering broad-spectrum disease-resistant rice by editing susceptibility and executor R genes. (a) Editing the EBEs (effector-binding elements) of S genes OsSWEET11, OsSWEET13, and OsSWEET14; (b) disruption of S genes; (c) editing the EBEs of executor R gene by CRISPR/Cas9-mediated precise homology directed repair.
Figure 2. Engineering broad-spectrum disease-resistant rice by editing susceptibility and executor R genes. (a) Editing the EBEs (effector-binding elements) of S genes OsSWEET11, OsSWEET13, and OsSWEET14; (b) disruption of S genes; (c) editing the EBEs of executor R gene by CRISPR/Cas9-mediated precise homology directed repair.
Ijms 22 11658 g002
Table
Table 1. R genes with broad-spectrum disease resistance in rice reported in past 10 years.
Table 1. R genes with broad-spectrum disease resistance in rice reported in past 10 years.
Gene NameProtein TypeIsolates or Pathogens 1ChromosomeReference
Pi64NBS-LRR9 Mo isolates1[6]
PizhNBS-LRR31 Mo isolates6[8]
PigmNBS-LRR30 Mo isolates6[7]
Pi50NBS-LRR20 Mo isolates6[22]
Pi56(t)NBS-LRR19 Mo isolates9[5]
Pi54rhNBS-LRR7 Mo isolates11[4]
PtrARM repeat protein331 Mo isolates12[9]
Pita2ARM repeat protein64 Mo isolates12[10]
Xa7Executor R protein8 Xoo isolates6[27]
Xa23Executor R protein39 Xoo isolates11[28]
xa41(t)Sugar transporter (SWEET)18 Xoo isolates11[29]
Xa47(t)NBS-LRR10 Xoo isolates11[30]
1 The pathogens and number of isolates to which resistance is conferred by the gene in the first column. Magnaporthe oryzae, Mo; Xanthomonas oryzae pv. oryzae, Xoo.
Table
Table 2. Defense regulator genes showing broad-spectrum disease resistance.
Table 2. Defense regulator genes showing broad-spectrum disease resistance.
Gene NameProtein TypeIsolates or Pathogens 1Chr 2Reference
Bsr-d1C2H2-type transcription factor9 Mo isolates3[36,37]
OsMYB30MYB transcription factor5 Mo isolates2[38]
OsNAC60NAC transcription factor20 Mo isolates12[39]
OsWRKY45WRKY transcription factor1 Mo isolate5[40]
PIBP1RRM (RNA recognition motif) protein3 Mo isolates3[41]
OsBBI1RING E3 ubiquitin ligase7 Mo isolates6[42]
LHCB5Light-harvesting complex II protein21 Mo isolates11[43]
OsXB25Plant-specific ankyrin-repeat (PANK) protein1 Xoo isolate9[44]
OsBiP3Endoplasmic reticulum (ER) chaperone, luminal-binding protein 32 Xoo isolates5[45]
OsNPR1BTB/POZ-ankyrin repeat protein1 Mo isolate, 2 Xoo isolates1[46]
OsCRK6Cysteine-rich-receptor-like kinases1 Xoo isolate7[47]
OsCRK10Cysteine-rich-receptor-like kinases1 Xoo isolate7[47]
OsCDPK1Calcium-dependent protein kinasesXoo3[48]
OsILA1Raf-like MAPKKK9 Xoo isolates6[49]
lc7Ferredoxin-dependent glutamate synthase17 Xoo isolates7[50]
OsLYP4Lysin motif-containing proteins1 Mo isolate, 1 Xoo isolate, 1 Xoc isolate9[51]
OsLYP6Lysin motif-containing proteins1 Mo isolate, 1 Xoo isolate, 1 Xoc isolate6[51]
OsWRKY67WRKY transcription factor2 Mo isolates, 2 Xoo isolates5[52]
IPA1Transcription factors12 Mo isolates8[53,54]
OsTFIIAα,Transcription factor IIA subunits10 Xoo isolates, 6 Xoc isolates5[55]
OsTFIIAβTranscription factor IIA subunits10 Xoo isolates, 6 Xoc isolates5[55]
OsGLP2-1Germin-like protein1 Mo isolate, 1 Xoo isolate2[56]
OsSnRK1aSucrose nonfermenting 1-related protein kinase 11 Mo isolate, 1 Xoo isolate, 1 Cm isolate and 1 Rs isolate5[57]
OSK35/OsSnRK1bSucrose nonfermenting 1-related protein kinases1 Mo isolate, 1 Xoo isolate3[58]
OsCPK4Calcium-dependent protein kinase1 Mo isolate, 1 Xoo isolate2[59]
BSR1BIK1-like receptor-like cytoplasmic kinase2 Mo isolates, 3 Xoo isolates, 1 Bg isolate, 1 Cm isolate, rice stripe virus9[60]
OsBAG4Ubiquitin-like and BAG domain1 Mo isolate, 1 Xoo isolate1[61]
EBR1RING-Type E3 Ligase1 Mo isolate, 6 Xoo isolates5[61]
SPIN6Rho GTPase-activating protein (RhoGAP)1 Mo isolate, 1 Xoo isolate7[62]
OsWAK25Wall-associated kinases2 Mo isolates, 1 Xoo isolate3[63]
OsCUL3aCullin 3-based RING E3 ubiquitin ligases1 Mo isolate, 3 Xoo isolates2[64]
OsDRP1EDynamin-related protein1 Mo isolate, 1 Xoo isolate9[65]
SPL33Eukaryotic translation elongation factor 1 alpha (eEF1A)-like protein12 Mo isolates, 11 Xoo isolates1[66]
LMM5.1Eukaryotic translation elongation factor 1A (eEF1A)-like protein6 Mo isolates, 5 Xoo isolates1[67]
LMM5.4Eukaryotic translation elongation factor 1A (eEF1A)-like protein6 Mo isolates, 5 Xoo isolates4[67]
LML1Eukaryotic release factor 1 (eRF1) protein4 Mo isolates, 6 Xoo isolates4[68]
OsABA2Xanthoxin dehydrogenase2 Mo isolates, 4 Xoo isolates3[69]
SPL35CUE (coupling of ubiquitin conjugation to ER degradation) domain-containing protein8 Mo isolates, 4 Xoo isolates3[70]
OsHDT701Histone deacetylase4 Mo isolates, 1 Xoo isolate5[71]
OsMPK15Mitogen-activated protein kinase2 Mo isolates, 2 Xoo isolates11[72]
Bsr-k1Tetratricopeptide repeats (TPRs)containing protein7 Mo isolates, 10 Xoo isolates10[73]
OsALDH2B1Aldehyde dehydrogenase1 Mo isolate, 1 Xoo isolate, 1 Xoc isolate6[74]
OsPAL4Phenylalanine ammonia-lyase1 Mo isolate, 1 Xoo isolate, 1 Xoc isolate2[75]
OsHsfB4dClass B heat-shock factor1 Xoo isolate, 1 Xoc isolate3[76]
OsHsp18.0-CIHeat-shock proteins5 Xoc isolates3[77]
OsPAD4Phytoalexin-deficient 42 Xoo isolates, 1 Xoc isolate11[78]
OsGRXS15Glutaredoxins family proteins1 Xoo isolate, 1 Ff isolate1[79]
OsNH5N16Pathogenesis-related genes 1 homologs (NHs)1 Xoo isolates, 1 Ff isolate11[80]
OsASR2Abscisic acid, stress, and ripening 2 protein1 Xoo isolate, 1 Xoc isolate11[81]
Os2H16Short-chain peptide-encoding protein1 Xoo isolate, 1 Xoc isolate6[82]
OsGF14e14-3-3 protein1 Xoo isolate, 1 Rs isolate2[83]
OsWRKY30WRKY transcription factors1 Mo isolate, 1 Rs isolate8[84]
OsACS21-aminocyclopropane-1-carboxylic acid synthase2 Mo isolates, 1 Rs isolate4[85]
OsMESLMethyl esterase-like protein1 Mo isolate, 1 Xoo isolate, 1 Rs isolate7[86]
OsBON1Copine protein1 Mo isolate, 3 Xoo isolates, 1 Rs isolate2[87]
OsBON3Copine protein1 Mo isolate, 3 Xoo isolates, 1 Rs isolate5[87]
1 The pathogens and number of isolates to which resistance is conferred by the genes in the first colum. Burkholderia glumae, Bg; Cochliobolus miyabeanus, Cm; Magnaporthe oryzae, Mo; Rhizoctonia solani, Rs; Fusarium fujikuroi, Ff; Xanthomonas oryzae pv. oryzae, Xoo; Xanthomonas oryzae pv. oryzicola, Xoc. 2 Chr: chromosome.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Liu, Z.; Zhu, Y.; Shi, H.; Qiu, J.; Ding, X.; Kou, Y. Recent Progress in Rice Broad-Spectrum Disease Resistance. Int. J. Mol. Sci. 2021, 22, 11658. https://doi.org/10.3390/ijms222111658

AMA Style

Liu Z, Zhu Y, Shi H, Qiu J, Ding X, Kou Y. Recent Progress in Rice Broad-Spectrum Disease Resistance. International Journal of Molecular Sciences. 2021; 22(21):11658. https://doi.org/10.3390/ijms222111658

Chicago/Turabian Style

Liu, Zhiquan, Yujun Zhu, Huanbin Shi, Jiehua Qiu, Xinhua Ding, and Yanjun Kou. 2021. "Recent Progress in Rice Broad-Spectrum Disease Resistance" International Journal of Molecular Sciences 22, no. 21: 11658. https://doi.org/10.3390/ijms222111658

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