Next Article in Journal
Identification of Cerebrospinal Fluid Metabolites as Biomarkers for Enterovirus Meningitis
Next Article in Special Issue
Transcriptome Analysis of Chinese Chestnut (Castanea mollissima Blume) in Response to Dryocosmus kuriphilus Yasumatsu Infestation
Previous Article in Journal
Targeting of LRRC59 to the Endoplasmic Reticulum and the Inner Nuclear Membrane
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
IJMS
Volume 20
Issue 2
10.3390/ijms20020335
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

Evolution of Disease Defense Genes and Their Regulators in Plants

by
Rongzhi Zhang
1,†,
Fengya Zheng
2,†,
Shugen Wei
3,†,
Shujuan Zhang
1,
Genying Li
1,
Peijian Cao
4,* and
Shancen Zhao
2,4,*
1
Institute of Crop Science, Shandong Academy of Agricultural Sciences, Key Laboratory of Wheat Biology & Genetic Improvement on North Yellow & Huai River Valley, Ministry of Agriculture, National Engineering Laboratory for Wheat & Maize, Jinan 250100, China
2
BGI Institute of Applied Agriculture, BGI-Agro, Shenzhen 518083, China
3
Guangxi Botanical Garden of Medicinal Plants, Nanning 530023, China
4
China Tobacco Gene Research Center, Zhengzhou Tobacco Research Institute of CNTC, Zhengzhou 450001, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Int. J. Mol. Sci. 2019, 20(2), 335; https://doi.org/10.3390/ijms20020335
Submission received: 4 December 2018 / Revised: 28 December 2018 / Accepted: 10 January 2019 / Published: 15 January 2019
(This article belongs to the Special Issue Signal Transduction Pathways in Plants for Resistance Against Plant Pathogens 2019)
Browse Figures
Versions Notes

Abstract

:
Biotic stresses do damage to the growth and development of plants, and yield losses for some crops. Confronted with microbial infections, plants have evolved multiple defense mechanisms, which play important roles in the never-ending molecular arms race of plant–pathogen interactions. The complicated defense systems include pathogen-associated molecular patterns (PAMP) triggered immunity (PTI), effector triggered immunity (ETI), and the exosome-mediated cross-kingdom RNA interference (CKRI) system. Furthermore, plants have evolved a classical regulation system mediated by miRNAs to regulate these defense genes. Most of the genes/small RNAs or their regulators that involve in the defense pathways can have very rapid evolutionary rates in the longitudinal and horizontal co-evolution with pathogens. According to these internal defense mechanisms, some strategies such as molecular switch for the disease resistance genes, host-induced gene silencing (HIGS), and the new generation of RNA-based fungicides, have been developed to control multiple plant diseases. These broadly applicable new strategies by transgene or spraying ds/sRNA may lead to reduced application of pesticides and improved crop yield.

1. Introduction

The arms race of plants and host-pathogens seems never to stop, and sometimes the race is very intense. During the evolutionary process, plants have had to evolve multiple immunity mechanisms to survive danger signals in extracellular and intracellular milieus. Plants are able to enhance disease resistance and increase the food security, as well as to balance the resource allocation between growth and development. The prevalent defense mechanisms are categorized into three defense layers: the preliminary defense, pathogen-associated molecular pattern (PAMP) triggered immunity (PTI) [1], the secondary defense, effector-triggered immunity (ETI) [2], and the additional defense, the exosome-mediated cross-kingdom RNA interference (CKRI) system [3].
It is well-known that PTI functions in basal defense. Using the cell surface-localized pattern recognition receptors (PRR), plants can detect the infection of invaders by recognizing the conserved microbe-associated or pathogen-associated molecular patterns (MAMPs or PAMPs) [1]. Plant PRRs are cell surface localized, and always are receptor-like kinases (RLKs) and receptor like proteins (RLPs). RLKs are comprised of extracellular domains, transmembrane domains, and intracellular kinase domains, which are required for transmitting the signals to the downstream defense responses, whereas RLPs are only comprised of the basic conformation without intracellular kinase domain. PTI with broad-spectrum defense is not sufficient to prevent most pathogens, and if plants have defect in PRRs, they often become more susceptible to microbes [4,5,6,7]. In turn, pathogens employ kinds of virulence effectors to overcome PTI and establish successful infection, termed effector-triggered immunity. Thus, ETI functions in the second defense of elicitor mediated defenses.
Most of the genes involved in ETI pathway contain intracellular nucleotide-binding site and leucine-rich repeat domains (NBS-LRRs or NLRs), which are typically cytoplasmic receptor proteins. NBS-LRR genes can detect or recognize the polymorphic, strain-specific pathogen-secreted virulence effectors, and then transfer the signals to the downstream of defense genes. Thus, ETI-pathways belong to the species-specific disease resistance, and rapidly co-evolve with their pathogens. Plant species in eudicots and dicots have lots of NB-LRR genes. According to the N-terminal features and functions, the NB-LRR proteins in plants can be termed into two classes with the terminal Toll/interleukin-1receptor (TIR) or coiled-coil (CC)/resistance to powdery mildew8 (RPW8) domains [8,9,10]. The TIR, CC or RPW8 domains are crucial in signaling transmit in cellular targets for effector action or downstream signaling components [11]. Although the NB-LRR genes were demonstrated as the ancient and conserved genes in plants, their comparative genomic analyses have shown great structural diversity. For example, the CC domains are prevalent in eudicots and monocots, while the TIR domains are nearly absent in monocots [12]. Cross-kingdom RNA interference (CKRI) functions in the third layer, which protects plants by extracellular vesicles transport small RNAs or microRNAs (miRNAs) to microbial pathogens and then silence the virulence genes [3].
As one kind of typically small non-coding RNAs, miRNAs function in post-transcriptional gene regulation. Small miRNAs play big roles in a variety of biological processes, such as development, hormone responses and stress adaptations [13,14,15,16]. In PTI and ETI pathways, microRNAs as the classical regulators in post-transcript or translation level regulate defense/defense-associated genes [17,18], which can balance the benefits and costs of their targets. Plants employ miRNAs as shields against the pathogen attacks. MiRNAs respond to virus, bacteria and fungi by negatively regulating of mRNAs, which mainly function in both PTI and ETI. Until now, totally 153 disease resistance genes from PRGdb database [19], which involved in the plant immunity to biotic stresses, were validated by experiments in wet labs. Of them, 62.09% (95 from 153) genes, 17.65% (27 from 153) genes, 20.26% (31 from 153) genes were classified as NBS-LRR families, RLP/RLK, and other kinds of genes, respectively (Figure 1).
In regard to defense genes, studies have shown a number of genes/small RNAs linked to anti-pathogen immunity. Here, we mainly summarize the current knowledge of the defense genes and their evolution paths regulated by miRNAs in plants, and then discuss their potential applications in crop improvements in the last section.

2. Three Layers of Defense Mechanisms to Biotic Stresses in Plants

2.1. The First Layer of Defense: Defense Genes in PTI

As one of the most important sensory protein groups, RLKs and RLPs in plants play crucial roles both in cell–cell and the plant–environment communications such as plant–pathogen interaction. In addition, RLKs and RLPs play fundamental roles in plant growth and development. Plants deploy a wide assay of RLKs and RLPs as the first layer of inducible defense to detect microbe- and host- derived molecular patterns (Figure 2A, the first layer) [63]. Numbers of RLKs/RLPs have been cloned in plants [64]. The best classical example is FLAGELLIN-SENSITIVE2 (FLS2), belonging to RLK family, which have been verified to response to Flagellin fragment flg22 of bacteria in Arabidopsis [65], grapevine [66], tobacco [67], rice [68] and tomato [69]. As a “molecular glue”, flg22 induces the activity of the heterodimerization complex FLS2-BAK1 (BRI1-ASSOCIATED RECEPTOR KINASE). In different plant species, FLS2 receptors display different affinities for the conserved part of flagellin from different bacteria, which possibly reflect the coevolution with specific-pathogens [66]. Except FLS2, EF-TU RECEPTOR (EFR), PEP 1 RECEPTOR (PEPR1), PEPR2, RLP23, RLP30 [70], the endogenous AtPep1 [71], NLPs [72], and SCFE1 [73], can also recognize bacterial EF-Tu, respectively. All of them are associated with the regulatory BAK1 that acts as a co-receptor for flg22/EF-Tu/AtPep1/nlp30/SCFE1 of pathogens and are crucial for signaling activation [74].
Long chitin oligomers as bivalent ligands, lead to the homodimerization of CHITIN ELICITOR RECEPTOR KINASE 1 (AtCERK1) and generate an active receptor complex in Arabidopsis, which directly trigger chitin-induced immune signaling [75]. The chitin perception system in rice is significantly different from the one in Arabidopsis. OsCERK1 dimmer does not bind chitin since the single LysM domain, while the dimer elicitor-binding LysM-RLP (OsCEBiP) can bind the chitin by ligand. The OsCERK1-chitin-OsCEBiP then forms a sandwich-type receptor dimerization for chitin oligomers [76].
There are a number of RLKs/RLPs involved in plant immunity, which have been well summarized by Tang et al [63]. After plant sensing of pathogen/microbe-associated molecular patterns, these pattern recognition receptors instantly trigger a number of downstream responses, such as the activation of mitogen-activated protein kinases (MAPKs) (Figure 2A, the first layer), which is one of the earliest signaling events [77]. By phosphorylation to transmit response signals, MAPKKK actives MKK, and then MKK actives MPK [78]. MAPK cascades is involved in multiple signaling defense responses, including the biosynthesis/signaling of plant stress/defense hormones, reactive oxygen species generation, stomatal closure, defense gene activation, phytoalexin biosynthesis, cell wall strengthening, and hypersensitive response (HR) cell death (Figure 2A, the first layer) [77]. The activation of MAPK cascades is essential for plant immunity.
In addition, some transcription factors were found to regulate the defense-related genes that involved in signal transduction in rice. For example, a bZIP gene OsBBI1 in rice, is a major transcription factor to regulate the resistance spectrum for diverse groups of M. oryzae by altering the first level of innate immunity in host plants [79]. WRKY13 as another major regulatory factor was identified to transfer signals from WRKY45 to downstream WRKY42 as functioning WRKY- type transcription factors (TFs) [80]. Following the SA-pathway-dependent disease response mechanism, WRKY13 shows correlation of the defense to M. oryzae and Xoo [81]. By activation of NPR1 protein, the SA pathway plays a crucial role in the systemic acquired resistance response mechanism (Figure 2A, the first layer) [82]. As a result, kinds of genes comprised of cellulase surface disease resistance genes and intracellular transcript factors could function in the complex PTI.

2.2. The Second Layer of Defense: The Defense Genes in ETI

In ETI pathway, plants have developed NBS-LRR proteins to recognize effectors and trigger the ETI response [2], which can cause programmed cell death together with the downstream of WRKY and lead to hypersensitive response (HR) (Figure 2A, the second layer) [97]. NBS-LRRs as an interesting class of disease resistance genes own a larger member in plants. In Table 1, about 1.19–3.48% of total coding genes were defined as NBS-LRR genes. Although NB-LRR genes are abundant in plants, only 93 genes are validated to play important roles in the innate immunity of plants up to now. Of the validated NBS-LRR genes, 65.59% (61 from 93) genes contain the CC domains, while only 19.35% (18 from 93) genes contain the TIR domains, and the others contain only one domain of either NBS, LRR, TIR, CC, or RPW8 (Figure 1). The verified disease resistance genes with CNL or TNL domains are listed in Table 2. For example, seven CNLs and seven TNLs in Arabidopsis thaliana, eleven CNLs in Oryza sativa, five CNLs and one TNL in Solanum lycopersicium, seven CNLs in Triticum aestivum, three CNLs in Hodeum vulgare had been exemplified by experiments. These defense genes in plants can confer the resistance to fungi, oomycetes, bacteria, viruses, nematodes, and insects.
One type of plant disease can be prevented by several genes (Table 2). For example, the bacterial blight in Arabidopsis caused by Pseudomonas syringae/Xanthomonas oryzae, can be defended by RPM1 (CNL) [99], Rps2 (CNL) [100], RPS5 (CNL) [101], SSI4 (TNL) [102], and Rps4 (TNL) genes [103]. The downy mildew of cucurbits that caused by Pseudoperonospora cubensis (Oomycetes) in Arabidopsis, can be resisted by RPP13/RPP8 (CNL/CNL) [104], RPP1/RPP4 (TNL/TNL) [105,106], and RPP5 (TNL) [107,108]. In rice, the famous rice blast disease caused by Magnaporthe grisea or Magnaporthe oryzae, can be defended by 17 CNL type of disease resistance genes including Pi-ta/PIB [109], RGA5 [110], Pi36/Pi9/Pi2 [111,112,113], Piz-t/Pikm1-TS/Pikm2-TS/Pid3/Pi5-1/Pi5-2/Pit/Pikp-2 [113,114,115,116,117], Pia [118], Pi37 [119] and Rpr1 [120]. In barley, the powdery mildew caused by Blumeria graminis, can be resistant by CNL type of genes including MLA10 [121], MLA1 [122], and MLA13 [123]. In Linum usitatissimum, flax rust caused by Melampsora lini (Fungal), can be resistant by TNL type of genes including P2 [124], L6 [125], M [126], L [127], L1-L11 [128,129], P [129,130], and P1 [124]. One disease resistance gene can also confer plants resistant to several plant diseases (Table 3). For example, XA1 (CNL) [131] in rice, can defense to bacterial blight caused by bacterium of Pseudomonas syringae and Xanthomonas oryzae. Rx2 in Solanum acaule, can defense to potato virus X (Virus) and Heterodera schachtii (Nematode) [132].
The disease resistance genes were abundant in the wild resource. In Triticeae for example, the defense genes Sr31 and Sr50 [133] from cereal rye (Secale cereale), can confer the resistance to stem rust disease caused by Puccinia graminis f. sp. tritici (Pgt). Sr35 gene from Triticum monococcum confers the resistance to Ug99 Stem Rust Race Group [134]. In addition, some non-NBS-LRR genes can also provide the defense to pathogens. For example, Stb6 in wheat can directly interacted with the effector AvrStb6 that produced by wheat pathogen Zymoseptoria tritici [135]. The X10 gene, which has four potential transmembrane helices in rice, can be induced by transcription activator–like (TAL) effector AvrXa10. The gene can confer disease resistance to rice bacterial blight by inducing programmed cell death in rice [136,137].
By introgression or transgene strategy, these defense genes confer the disease resistance in plants. For example, by overexpressing Pm3a/c/d/f/g in wheat, all tested transgenic lines showed the significantly more resistance than their respective non-transformed sister lines in field experiments [138]. The T0 and T1 transgenic lines with the Sr50 gene were resistant to Puccinia graminis f. sp. tritici (Pgt), while lines without the transgene were susceptible [133].

2.3. The Third Layer of Defense: Cross-Kingdom/Organism RNA Interference

It had been demonstrated that plasmodesmata sRNAs can presumably move from cell to cell, and they systemically travel through vasculature [139]. Remarkably, sRNAs also move and induce their target gene silencing between interacted organisms and hosts. The phenomenon was defined as cross-kingdom/organism RNA interference (CKRI) [20,93,140,141,142]. Pathogens can deliver sRNAs into plants. It was recently discovered as a novel class of pathogen effectors (Figure 2A, the third layer). Botrytis cinerea can deliver small RNAs (Bc-sRNAs) to plant cells to silence host immunity genes [140]. Such small RNA effectors in B. cinerea are mostly produced by Dicer-like protein 1/2 (Bc-DCL1/2). In reverse, over-expressing sRNAs that target Bc-DCL1 and Bc-DCL2 in tomato and Arabidopsis, would silence Bc-DCL genes and inhibit fungal growth and pathogenicity. It exemplified bidirectional CKRI and sRNA trafficking between plants and fungi [93]. The easy traveling phenomenon suggests naturally occurring small RNAs might exchange each other across cross-kingdom/organism.
Conversely, hosts also can transfer naturally occurring small RNAs into pests or pathogens to attenuate their virulence (Figure 2A, the third layer). Recently, two reports have demonstrated that naturally occurring plant small RNAs might be delivered into pathogens to silence their target genes. In response to the infection of Verticillium dahliae, cotton plants increase the dose of miR159 and miR166 in expression level and then export both to the fungal hyphae for specific silencing. Two genes encoding an isotrichodermin C-15 hydroxylase and a Ca2+-dependent cysteine protease, were targeted by miR159 and miR166, respectively. Both of the target genes are essential for fungal virulence [20]. Another example is that host Arabidopsis cells by secreting exosome-like extracellular vesicles can also transfer small RNAs into fungal pathogen Botrytis cinerea. At the infection sites, these sRNA-containing vesicles accumulate and then are taken up by the fungal cells. Delivered host small RNAs induce the silence of fungal genes that is critical for pathogenicity. TAS1c-siR483 target two genes BC1G_10728 and BC1G_10508 from B. cinerea, and TAS2-siR453 targets BC1T_08464. All of the three genes involving in vesicle trafficking pathways are critical for pathogenicity [3]. Of them, BC1G_10728 encodes a vacuolar protein sorting 51 and plays a crucial role in Candida albicans virulence [21]. Thus, Arabidopsis has adapted exosome-mediated CKRI mechanism as part of its immune responses during the evolutionary arms race with the pathogens [3].
Based on the above description, since only two miRNAs and two small RNAs in plants were identified to function in CKRI, data are inefficient to deduce their evolution among species. Thus, in the next section, we only discussed the evolution of disease resistance genes and their regulator miRNAs in PTI and ETI.

3. The Regulation of Disease Resistance Genes by Small RNAs

3.1. The First Layer of Defense Regulation: miRNAs Involved in the PTI Pathway

During pathogen infection, plant small RNAs play key roles in gene regulation level. According to the targets of miRNAs that how to respond to the pathogen infection, miRNAs were divided into active and repressed regulation in basal resistance (Figure 1A, Table 3). In the positive regulation, overexpression of miRNAs conferred the resistance to defense diseases in plants. For example, miR393 in Arabidopsis, was discovered to contribute to the antibacterial resistance by negatively targeting the transcripts of the F-box auxin receptors TIR1 [22]. Repressing auxin signaling through miR393 overexpression increases bacterial resistance; conversely, augmenting auxin signaling through over-expressing a TIR enhances susceptibility to virulent Pto DC3000. miR444/OsMADS directly monitors OsRDR1 transcription, and involves in the rice antiviral response [23]. Overexpression of miR444 enhanced rice resistance against rice stripe virus (RSV) infection by diminishes the repressive roles of OsMADS23, OsMADS27a, and OsMADS57 and concomitant by the up-regulation of OsRDR1 expression. Thus, miR444 can indirectly activate the OsRDR1-dependent antiviral RNA-silencing pathway. Over-expression of osa-miR171b conferred less susceptibility to rice stripe virus infection by regulating the target OsSCL6. OsSCL6-IIa/b/c was down-regulated or up-regulated in plants, where osa-miR171b was over-expressed or interfered [24].
In the negative regulation, overexpression their target genes could confer the resistance to pathogens in plants. miR169 suppresses the expression of NFYA in immunity against the infection of bacterial wilt Ralstonia solanacearum [25] and the blast fungus Magnaporthe oryzae in Arabidopsis and rice, respectively [26]. The transgenic lines of over-expressing miR169a, became hyper-susceptible to pathogens. MiR156 and miR395 regulate apple resistance to Leaf Spot Disease [27]. In apple, Md-miR156ab and Md-miR395 suppress MdWRKYN1 and MdWRKY26 expression, which decreases the expression of some pathogenesis-related genes, and results in susceptibility to Alternaria alternaria f. sp. mali. In Arabidopsis, miR396/GRF module mediates innate immunity against P. cucumerina infection without growth costs. Reduced activity of miR396 (MIM396 plants) was found to improve broad resistance to necrotrophic and hemibiotrophic fungal pathogens [28]. MiR319/TCP module involves in the rice blast disease. Increasing expression level of rice miR319 or decreasing expression level of its target TCP21, LIPOXYGENASE2 (LOX2) and LOX5 can facilitate rice ragged stunt virus (RRSV) infection [29], which caused the decreased endogenous jasmonic acid (JA) [30]. Inhibiting ath-miR773 activity accompanied with up-regulation of its target gene METHYLTRANSFERASE 2 increased resistance to hemibiotrophic (Fusarium oxysporum, Colletototrichum higginianum) and necrotrophic (Plectosphaerrella cucumerina) fungal pathogens in Arabidopsis [31]. By regulating the transcription of GhMKK6 gene in cotton, ghr-miR5272a involved in the immune response. Over-expressing ghr-miR5272a increased sensitivity to Fusarium oxysporum by decreasing the expression of GhMKK6 and the followed disease-resistance genes, which lead a similar phenotype to GhMKK6-silenced cotton [32]. In addition, miRNAs could also be involved in the resistance to nematode invasion. For example, miR827 in Arabidopsis down-regulated the expression of NITROGEN LIMITATION ADAPTATION (NLA) gene. It suppressed the basal defense pathway by enhancing susceptibility to the cyst nematode Heterodera schachtii [33].
Except these miRNAs indirectly regulation the PTI pathway, a few of miRNAs were predicted to directly regulate the receptor-like genes. For example, when osa-miR159a.1 was repressed, the expression of OsLRR-RLK2 was induced, which is responded to Xanthomonas oryzae pv. Oryzae in rice [31]. In future, some miRNAs regulation of pattern recognition receptors (PRR) genes may be validated by experiments.

3.2. The Second Layer of Defense Regulation: The Defense Signal Small RNAs in ETI

In addition to the basal defense, miRNAs are also involved in ETI pathway to directly and indirectly regulate the disease resistance genes (Figure 2A & Table 3). MiR393*, the complementary strand of miR393 within the sRNA duplex, by targeting a protein trafficking gene Membrin 12 promote the secretion of antimicrobial PR proteins, which functions in ETI during infection of Pseudomonas syringae pv. Tomato in Arabidopsis [34]. The miR863-3p is induced by the bacterial pathogen Pseudomonas syringae. During early infection, miR863-3p silences two negative regulators of plant defense, namely atypical receptor-like pseudokinase1 (ARLPK1) and ARLPK2, both of which trigger immunity through mRNA degradation. Later during infection, miR863-3p silences SERRATE, and positively regulates defense. And SERRATE is essential for miR863-3p accumulation by a negative feedback loop. Thus, miR863-3p targets both negative and positive regulators of immunity through two modes of action to fine-tune in the timing and amplitude of defense responses [35].
High expression of plant NBS-LRR defense genes is often lethal to plant cells, which is associated with the fitness costs. Thus, plants develop several mechanisms to regulate the transcript level of NBS-LRR genes. One of the key mechanism is the suppression of regulation network in microRNAs and NBS-LRRs, which may play a crucial role in plant-microbe interactions by sRNA silencing mechanism [18]. NBS-LRR genes confer defense against the pathogen infections in gene dosage dynamic expression level by multiple duplications and diversification, while miRNAs minimized the cost of gene copies by inhibiting their expression [36]. One miRNA can regulate dozens to hundreds of NBS-LRRs by targeting the similar motif sites [37], which make it more economical to balance the benefits and costs of these copies in genome. Until now, a few of miRNAs had been validated to be involved in the regulation of NBS-LRR genes.
The regulation between miRNAs and CC-NB-LRR or TIR-NB-LRR gene classes was mostly characterized in eudicots. In most of the post-transcriptional regulation networks, the miRNA can trigger the 21-nt phased siRNA generation in NB-LRR transcripts, which were processed by RNA-dependent RNA polymerase 6 (RDR6) and DICER-LIKE 4 (DCL4) [38]. For example, in Brassica miR1885 were validated to induce by Turnip Mosaic Virus (TuMV) infection, which cleaved TIR-NB-LRR class genes [39]. In Tobacco, by cleaving TIR-NB-LRR immune receptors, both of nta-miR6020 and nta-miR6019 provide resistance to Tobacco mosaic virus (TMV) [40,41]. In tomato, sl-miR5300 and sl-miR482f controlled NB domain-containing proteins in mRNA stability and translation level, which involved in plant immunity [42]. In Arabidopsis, miR472 modulated the disease resistance genes mediated by RDR6 silencing pathway [43]. In Medicago, miR2109, miR482/miR2118 and miR1507 were found to influence NB-LRR gene family [37]. In legumes, miR482, miR1507, miR1510, and miR2109 suppressed NB-LRR gene class with CC or TIR domains, which were proposed to function in the regulation of defense response or host specificity during rhizobium colonization [38,44]. In addition, miR482/miR2118, miR946, miR950, miR951, miR1311, miR1312, miR3697, miR3701, and miR3709 were also mediated to generate phased siRNAs by targeting NBS-LRR gene class in Norway Spruce [45]. In monocots, miR2009 (also named miR9863 in miRBase) was first predicted in wheat to target the Mla alleles [46]. In barley, the miR9863 family was confirmed to trigger response to the Mla alleles [47].

4. The Evolution of Defense Genes

4.1. The Evolution of Defense Gene in PTI

In land plants, RLKs expanded extensively and fulfilled these diverse roles including perceive growth hormones, environmental/danger signals derived from pathogens [143]. In Arabidopsis, 44 RLK subgroups were defined, and leucine-rich repeat receptor-like kinases (LRR-RLK) belong to the largest receptor-like kinase family and are focused by researchers [144]. According to characters of unique basic gene structures and protein motif compositions, plant LRR-RLKs constitute 19 subfamilies, most of which were derived from the common ancestors in land plants. The proportions of LRR-RLK genes in Lycophytes and moss genome are 0.30% and 0.36%, respectively, while the proportions of LRR-RLK genes in angiosperms are 0.67–1.39% [145], which indicated the special expansion of defense genes in angiosperm genomes. LRR-RLK involved in the defense/resistance-related genes was less conserved than that involved in development. Defense-associated LRR-RLKs undergone many duplication events, and most of them were massively lineage-specific expansion mainly by tandem duplication [143,144]. These discoveries provide important resources for future functional research for these critical signaling genes in PTI.

4.2. The Evolution of Defense Gene in ETI

NBS-LRR genes as a class of ancient and conserved genes have been detected in gymnosperms, angiosperm plants and animals to ensure immunity [12,146,147]. However, comparative genomic analyses have demonstrated that NBS-LRR genes have a great structural diversity in plants and animals. For example, TIR domains were established in the ancestor plants conifers and mosses, and also in animals shared functionality regarding innate immunity [148,149,150]. TIR genes specially expanded in dicot genomes, but are absent or at least rare in monocot genomes [8,147,151,152,153]. For NBS-LRR genes, tandem duplication in genome is the major expansion mechanism in plants. More than 60% of NBS-LRR genes organized in a general pattern of clusters in plant genomes (Figure 2B) [98]. During whole genome duplication, biased deletions happened in the duplicated paralogous blocks with NB-LRR genes, and it could be possibly compensated by their local tandem duplication mechanism (Figure 2B).
The miRNAs typically target highly duplicated NBS-LRRs, and families of heterogeneous NBS-LRRs were rarely targeted by miRNAs in Brassicaceae and Poaceae genomes [18]. miRNAs/NBS-LRR-genes interactions drove functional diploidization of structurally retained NBS-LRR genes duplicates by suppression regulation (Figure 2B) [98]. Evolutionary shuffling events such as diploidization and tandem duplication, leaded to copy number variations and presence absence variations in the synteny collapse of NBS-LRR genes [154,155,156,157]. In addition, the polymorphisms often exist in a population [158]. A contrasted conservation of NBS-LRR genes was observed with only 23.8% for monocots and 6.6% for dicots. Thus, NBS-LRR genes as one of the most plastic gene family in plants have less conservation such as synteny erosion or alternatively loss in plants compared with the other coding protein genes [98].

5. The Evolution of microRNAs in the Defense Pathway

5.1. The Evolution of miRNAs in PTI

In the PTI pathway, most of miRNAs were very conserved and directly/indirectly involve multiple biological processes in the development and abiotic/biotic stresses. All of the MiR169, miR171, miR393, miR395, and miR396 were ancient miRNAs present in both dicots and monocots [48]. miR444 was specific in monocots [49], whereas miR773 and miR5272 were lineage-specific in Arabidopsis and Medicago. The miRNAs conserved in plants mostly regulate the important transcript factors. These transcript factors tend to involve multiple biological processes. Take miR169 and miR396 for example, miR169/NFYA in Arabidopsis indirectly affected lateral root initiation [50], nitrogen-starvation [51], drought stress [52], and biotic stress [25,26]. In Arabidopsis roots, miR396/GRF regulates the switch between stem cells and transit-amplifying cells [53], which affects rice yield by shaping inflorescence architecture [54], and biotic stresses [28].
Both of the miRNA/target regulation and their function are very conserved in plants. MiR169/NFYA module influences the Ralstonia solanacearum pathogenicity in Arabidopsis [25] and the resistance to M. oryzae strains in rice [26]. In addition, these conserved miRNAs’ targets were expanded except for their classical miRNA/target model. For example, miRNA156 regulates of the SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) family involve in the timing of vegetative and reproductive phase change, which is highly conserved among phylogenetically distinct plant species [55]. miR395 by targeting a high-affinity sulphate transporter and three ATP sulfurylases involved in the sulfate homeostasis, is also conserved in plants [56,57]. Differently, both miR156 and miR395 regulate apple resistance to leaf spot disease by targeting WRKY. Thus, miRNAs involved in PTI pathway, are conserved in PTI defense pathway and in plant development such as miR393 vs TIR in auxin signal pathway [22] and miR319 vs. TCL in JA pathway [29]. Only few of miRNAs were reported to potentially regulating the RLK/RLP by osa-miR159a.1 [58], MiR5638 and miR1315 [59]. Genes involved in the PTI pathway were relatively conserved compared to these genes involved in ETI pathway. Thus, most of their regulator miRNAs were also conserved miRNAs or neofunctionalization of miRNAs in plants.

5.2. The Evolution of miRNAs in ETI

Although there are many miRNAs regulated NB-LRR genes, the conservation level of miRNAs is lower than the development associated miRNAs or PTI-associated miRNAs. In the eudicots and monocots, there is no conserved miRNAs targeting the NB-LRR genes. Lineage- or species-specific disease resistance-associated miRNAs were continually present and accompanies the continually varied pathogens. And some miRNAs with similar sequences had obvious functional diversity. miR482/miR2118 in eudicots mostly targeted NB-LRR genes, however, it only initiated the generation of 21-nt phased siRNAs in rice, and most of the target transcripts were noncoding sequences and specifically expressed in the rice stamen and the maize premeiotic and meiotic anther [60,61,62]. It clearly concluded that miR2118 initiated the phased siRNA in male reproductive organs. Therefore, a functional switch occurred in miR482/miR2118 between eudicots and dicots. Their expression level also varies in the lineage-related species. Tae-miR3117 was predicted to target the numbers of NBS-LRRs with higher expression in the tetraploid and hexaploid Triticum seedlings, while it had lower expression levels in Aegilops tauschii (not published data). And in rice, maize, and sorghum, miR3117 also displayed lower expression levels.
Diverse miRNAs, as negative transcriptional regulators, inhibit NBS-LRRs in plants. The highly duplicated NBS-LRRs were typically targeted by miRNAs (Figure 2B), while families of heterogeneous NBS-LRR genes were rarely regulated by miRNAs such as in Poaceae and Brassicaceae genomes. For example, some miRNAs also have a high duplication rate such as miR482/miR2118 in tandem duplication in genomes [60,61,62], which may enhance the expression dosage.
Newly emerged miRNAs were periodically derived from duplicated/redundant NBS-LRRs from different gene families. And most of these new birth miRNAs target these NBS-LRR gene regions of conserved, encoded protein motif, which follow in the convergent evolution model (Figure 2B). The miRNAs may drive the rapid diploidization of these NBS-LRR genes in polyploid plants. These NBS-LRR associated miRNAs had a rapid diversity. The nucleotide diversity of the target site region in the wobble position of the codons drives the diversification of miRNAs. These characters of high duplication rate and rapid diversity were similar to their target genes. The co-evolutionary model between NBS-LRRs and miRNAs in plants makes the plants balance the costs and benefits of disease resistance [18].

6. The Strategies of Defense Pathogens in plants

6.1. The First Strategy: Utilize the Disease Resistance Genes by a Molecular Switch

Up to now, a number of genes were exemplified to be involved in plant immunity defense. By over-expressing such defense genes can dramatically enhance disease resistance in plants, while is often associated with significant penalties to fitness and make the resulting products undesirable. Thus, it is difficult in agricultural applications. Recently, it has been developed a strategy to utilize these disease defense genes from the angle of plant genes or their regulators [83]. The strategy is to introduce immunity-inducible promoter and other two pathogen-responsive upstream open reading frames of the TBF1 gene. It is called uORFsTBF1, which is a key immune regulator and its translation is transiently and rapidly induced upon pathogen challenge (Figure 2C, uORF). It has been demonstrated that inclusion of the uORFsTBF1-mediated translational control over the production of AtNPR1 in rice and an auto-activated immunity receptor snc1-1 in Arabidopsis did not reduce the plant fitness in the laboratory or in the field [83]. This strategy using a molecular switch enables us to engineer more broad-spectrum disease resistance genes with minimal adverse effects on plant growth and development in the agriculture application.

6.2. The Second Strategy: Host-Induced Gene Silencing (HIGS)

Transgene-derived artificial sRNAs in plants can induce the target gene silencing in certain interacting insects [84,85], nematodes [86], fungi [87,88,89,90], oomycetes [91,92], and even plants–plants [141]. The phenomenon was called host-induced gene silencing (HIGS). The artificial sRNAs can travel from host plants to pathogens or pests and then function in trans (Figure 2C, HIGS). It had been well used in many plants in the decades. By plant RNAi suppressing a bollworm P450 monooxygenase gene of cotton impaired larval tolerance of gossypol [85]. In transgenic plants, by RNAi silencing of a conserved and essential root-knot nematode parasitism gene engineered broad root-knot resistance [86]. HIGS of nematode fitness and reproductive genes decreases fecundity of Heterodera glycines Ichinohe. Double-stranded RNA complementary to cytochrome P450 lanosterol C14 alpha-demethylase-encoding genes of Fusarium in Arabidopsis and barley contributes to strong resistance to Fusarium species [90]. HIGS to the MAPKK gene PsFUZ7 in wheat enhance stable resistance to wheat stripe rust [159]. HIGS of an important pathogenicity factor PsCPK1 in Puccinia striiformis f. sp. tritici conferred resistance of wheat to stripe rust [160]. By transgene-mediated cross-kingdome RNAi mechanism, HIGS by transgene is a good and effect strategy to improve the crop disease resistance in a broad spectrum.

6.3. The Third Strategy: Spray-Induced Gene Silencing (SIGS)

The pathogens and pests are capable to take up the double RNAs or small RNAs from the plants or the environments [93]. Based on this and according to the mechanism of cross-kingdom/organism RNA interference, researchers have developed a strategy to control crop disease. It is spray-induced gene silencing (SIGS) that spraying dsRNAs and sRNAs on plant surfaces can target pathogen genes to repression pathogen virulence (Figure 2C, SIGS). For modern crop protection strategies, it is a natural blueprint. Evidences suggest that nematodes [94], insects [84] and fungi [95] could uptake up the environmental dsRNA or sRNAs. Directly spraying the dsRNAs that target the fungal cytochrome P450 lanosterol C-14alpha-demethylases of fungal gene can suppress fungal growth [95]. On barley leaves, spraying CYP51-targeting dsRNA at a concentration range of 1–20 ng/mL, inhibited growth of Fusarium species [3]. It has been demonstrated that spraying naked sRNAs and dsRNA on plants was successful to protect fruits and vegetables against pathogens. However, pesticide effect of the naked sRNAs and dsRNAs can only last 5–8 days. Mitter, et al. developed a method to load dsRNAs on designer, non-toxic, degradable, layered double hydroxide (LDH) clay nanosheets. This LDH made the dsRNA does not be wash off, and can be sustained released for 30 days [96]. This SIGS broadly application of new strategy may contribute to reduced use of chemical pesticides and lightening of selective pressure for resistant pathogens. The new-generation of RNA-based fungicides and pesticides are powerful, eco-friendly, which can be easily adapted to control multiple plant diseases simultaneously.

7. Conclusions

Plants deployed PTI, ETI, and CKRI innate immune systems to arm race with different pathogen stresses. Pathogens developed more advanced effectors to defeat plant defense immunity. A number of genes have been exemplified to play important role between the host-pathogen interactions in plants. These signaling genes will be helpful to improve plant disease resistance against various pathogens. The sustainable and broaden spectrum resistance genes and their regulators such as miRNAs will be applied in developing crop varieties by introducing the molecular switch. From the cross-kingdom angle, the HIGS can also be used to crop breeding by transgenic approach, which can also confer the broaden spectrum resistance to hosts. The SIGS can also make plants yield the broaden spectrum resistance by spraying the designed dsRNAs/sRNA. Further function studies in plants will dissect more and more defense genes and hopefully unravel the intricate defense regulation network. More and more molecular technologies will be invented and adapted to help develop the eco-friendly disease-resistance cultivars.

Author Contributions

S.Z. and R.Z. conceived and designed the project. F.Z., R.Z., S.Z., S.W., and P.C. downloaded the data and analyzed the data. R.Z., F.Z., and G.L. prepared and drafted the manuscript. S.Z. and P.C. revised the manuscript. All the authors read and approved the final manuscript.

Acknowledgments

This work was mainly supported by the Young Elite Scientists Sponsorship Program By CAST (2016QNRC001), the National Natural Science Foundation of China (31501312, 31601301 from SAAS), and the Natural Science Foundation of Shandong Province (ZR2014CM006 from SAAS) for the design of the study. Collection of data was supported by the Agricultural Science and Technology Innovation Project of Shandong Academy of Agricultural Sciences (CXGC2016C09 from SAAS), the Youth Talent Program of Shandong Academy of Agricultural Sciences from SAAS. Data analysis, organization, and interpretation were supported by the Ministry of Agriculture of China (2018ZX08009-10B from SAAS), the Youth Foundation of Shandong Academy of Agricultural Sciences (2016YQN01 from SAAS), the Ministry of Science and Technology of China (2016YFD0100500 from SAAS) and Key R&D Programme of Shandong Province (2017GNC10113 from SAAS), the National Science and Technology Major Project of Breeding New Varieties of Genetically Modified Organisms (2018ZX0800910B from SAAS), and Projects of ENCODE of Tobacco Genome (110201601033(JY-07)).

Conflicts of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as potential conflicts of interest.

References

  1. Monaghan, J.; Zipfel, C. Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 2012, 15, 349–357. [Google Scholar] [CrossRef] [PubMed]
  2. Eitas, T.K.; Dangl, J.L. NB-LRR proteins: Pairs, pieces, perception, partners, and pathways. Curr. Opin. Plant Biol. 2010, 13, 472–477. [Google Scholar] [CrossRef] [PubMed]
  3. Cai, Q.; Qiao, L.; Wang, M.; He, B.; Lin, F.M.; Palmquist, J.; Huang, H.D.; Jin, H. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science 2018. [Google Scholar] [CrossRef]
  4. Shi, H.; Shen, Q.; Qi, Y.; Yan, H.; Nie, H.; Chen, Y.; Zhao, T.; Katagiri, F.; Tang, D. BR-SIGNALING KINASE1 physically associates with FLAGELLIN SENSING2 and regulates plant innate immunity in Arabidopsis. Plant Cell 2013, 25, 1143–1157. [Google Scholar] [CrossRef] [PubMed]
  5. Yeh, Y.H.; Panzeri, D.; Kadota, Y.; Huang, Y.C.; Huang, P.Y.; Tao, C.N.; Roux, M.; Chien, H.C.; Chin, T.C.; Chu, P.W.; et al. The Arabidopsis Malectin-Like/LRR-RLK IOS1 Is Critical for BAK1-Dependent and BAK1-Independent Pattern-Triggered Immunity. Plant Cell 2016, 28, 1701–1721. [Google Scholar] [CrossRef] [PubMed]
  6. Shen, Q.; Bourdais, G.; Pan, H.; Robatzek, S.; Tang, D. Arabidopsis glycosylphosphatidylinositol-anchored protein LLG1 associates with and modulates FLS2 to regulate innate immunity. Proc. Natl. Acad. Sci. USA 2017, 114, 5749–5754. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  7. Erwig, J.; Ghareeb, H.; Kopischke, M.; Hacke, R.; Matei, A.; Petutschnig, E.; Lipka, V. Chitin-induced and CHITIN ELICITOR RECEPTOR KINASE1 (CERK1) phosphorylation-dependent endocytosis of Arabidopsis thaliana LYSIN MOTIF-CONTAINING RECEPTOR-LIKE KINASE5 (LYK5). New Phytol. 2017, 215, 382–396. [Google Scholar] [CrossRef] [PubMed]
  8. Meyers, B.C.; Kozik, A.; Griego, A.; Kuang, H.; Michelmore, R.W. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 2003, 15, 809–834. [Google Scholar] [CrossRef]
  9. Xiao, S.; Ellwood, S.; Calis, O.; Patrick, E.; Li, T.; Coleman, M.; Turner, J.G. Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 2001, 291, 118–120. [Google Scholar] [CrossRef]
  10. Shao, Z.Q.; Xue, J.Y.; Wu, P.; Zhang, Y.M.; Wu, Y.; Hang, Y.Y.; Wang, B.; Chen, J.Q. Large-Scale Analyses of Angiosperm Nucleotide-Binding Site-Leucine-Rich Repeat Genes Reveal Three Anciently Diverged Classes with Distinct Evolutionary Patterns. Plant Physiol. 2016, 170, 2095–2109. [Google Scholar] [CrossRef] [Green Version]
  11. Mukhtar, M.S.; Carvunis, A.R.; Dreze, M.; Epple, P.; Steinbrenner, J.; Moore, J.; Tasan, M.; Galli, M.; Hao, T.; Nishimura, M.T.; et al. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 2011, 333, 596–601. [Google Scholar] [CrossRef] [PubMed]
  12. Meyers, B.C.; Dickerman, A.W.; Michelmore, R.W.; Sivaramakrishnan, S.; Sobral, B.W.; Young, N.D. Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J. Cell Mol. Biol. 1999, 20, 317–332. [Google Scholar] [CrossRef]
  13. Voinnet, O. Origin, biogenesis, and activity of plant microRNAs. Cell 2009, 136, 669–687. [Google Scholar] [CrossRef] [PubMed]
  14. Alptekin, B.; Langridge, P.; Budak, H. Abiotic stress miRNomes in the Triticeae. Funct. Integr. Genom. 2017, 17, 145–170. [Google Scholar] [CrossRef] [PubMed]
  15. Budak, H.; Kantar, M. Harnessing NGS and Big Data Optimally: Comparison of miRNA Prediction from Assembled versus Non-assembled Sequencing Data—The Case of the Grass Aegilops tauschii Complex Genome. Omics J. Integr. Biol. 2015, 19, 407–415. [Google Scholar] [CrossRef] [PubMed]
  16. Budak, H.; Kantar, M.; Bulut, R.; Akpinar, B.A. Stress responsive miRNAs and isomiRs in cereals. Plant Sci. Int. J. Exp. Plant Biol. 2015, 235, 1–13. [Google Scholar] [CrossRef] [PubMed]
  17. Li, Y.; Zhang, Q.; Zhang, J.; Wu, L.; Qi, Y.; Zhou, J.M. Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiol. 2010, 152, 2222–2231. [Google Scholar] [CrossRef]
  18. Zhang, Y.; Xia, R.; Kuang, H.; Meyers, B.C. The Diversification of Plant NBS-LRR Defense Genes Directs the Evolution of MicroRNAs That Target Them. Mol. Biol. Evol. 2016, 33, 2692–2705. [Google Scholar] [CrossRef]
  19. Osuna-Cruz, C.M.; Paytuvi-Gallart, A.; Di Donato, A.; Sundesha, V.; Andolfo, G.; Aiese Cigliano, R.; Sanseverino, W.; Ercolano, M.R. PRGdb 3.0: A comprehensive platform for prediction and analysis of plant disease resistance genes. Nucleic Acids Res. 2018, 46, D1197–D1201. [Google Scholar] [CrossRef]
  20. Zhang, T.; Zhao, Y.L.; Zhao, J.H.; Wang, S.; Jin, Y.; Chen, Z.Q.; Fang, Y.Y.; Hua, C.L.; Ding, S.W.; Guo, H.S. Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen. Nat. Plants 2016, 2, 16153. [Google Scholar] [CrossRef]
  21. Liu, Y.; Mittal, R.; Solis, N.V.; Prasadarao, N.V.; Filler, S.G. Mechanisms of Candida albicans trafficking to the brain. PLoS Pathog. 2011, 7, e1002305. [Google Scholar] [CrossRef] [PubMed]
  22. Navarro, L.; Dunoyer, P.; Jay, F.; Arnold, B.; Dharmasiri, N.; Estelle, M.; Voinnet, O.; Jones, J.D. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 2006, 312, 436–439. [Google Scholar] [CrossRef] [PubMed]
  23. Wang, H.; Jiao, X.; Kong, X.; Hamera, S.; Wu, Y.; Chen, X.; Fang, R.; Yan, Y. A Signaling Cascade from miR444 to RDR1 in Rice Antiviral RNA Silencing Pathway. Plant Physiol. 2016, 170, 2365–2377. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Tong, A.; Yuan, Q.; Wang, S.; Peng, J.; Lu, Y.; Zheng, H.; Lin, L.; Chen, H.; Gong, Y.; Chen, J.; et al. Altered accumulation of osa-miR171b contributes to rice stripe virus infection by regulating disease symptoms. J. Exp. Bot. 2017, 68, 4357–4367. [Google Scholar] [CrossRef] [PubMed]
  25. Hanemian, M.; Barlet, X.; Sorin, C.; Yadeta, K.A.; Keller, H.; Favery, B.; Simon, R.; Thomma, B.P.; Hartmann, C.; Crespi, M.; et al. Arabidopsis CLAVATA1 and CLAVATA2 receptors contribute to Ralstonia solanacearum pathogenicity through a miR169-dependent pathway. New Phytol. 2016, 211, 502–515. [Google Scholar] [CrossRef] [PubMed]
  26. Li, Y.; Zhao, S.L.; Li, J.L.; Hu, X.H.; Wang, H.; Cao, X.L.; Xu, Y.J.; Zhao, Z.X.; Xiao, Z.Y.; Yang, N.; et al. Osa-miR169 Negatively Regulates Rice Immunity against the Blast Fungus Magnaporthe oryzae. Front. Plant Sci. 2017, 8, 2. [Google Scholar] [CrossRef] [PubMed]
  27. Zhang, Q.; Li, Y.; Zhang, Y.; Wu, C.; Wang, S.; Hao, L.; Wang, S.; Li, T. Md-miR156ab and Md-miR395 Target WRKY Transcription Factors to Influence Apple Resistance to Leaf Spot Disease. Front. Plant Sci. 2017, 8, 526. [Google Scholar] [CrossRef] [PubMed]
  28. Soto-Suarez, M.; Baldrich, P.; Weigel, D.; Rubio-Somoza, I.; San Segundo, B. The Arabidopsis miR396 mediates pathogen-associated molecular pattern-triggered immune responses against fungal pathogens. Sci. Rep. 2017, 7, 44898. [Google Scholar] [CrossRef] [Green Version]
  29. Zhang, C.; Ding, Z.; Wu, K.; Yang, L.; Li, Y.; Yang, Z.; Shi, S.; Liu, X.; Zhao, S.; Yang, Z.; et al. Suppression of Jasmonic Acid-Mediated Defense by Viral-Inducible MicroRNA319 Facilitates Virus Infection in Rice. Mol. Plant 2016, 9, 1302–1314. [Google Scholar] [CrossRef]
  30. Zhang, X.; Bao, Y.; Shan, D.; Wang, Z.; Song, X.; Wang, Z.; Wang, J.; He, L.; Wu, L.; Zhang, Z.; et al. Magnaporthe oryzae Induces the Expression of a MicroRNA to Suppress the Immune Response in Rice. Plant Physiol. 2018, 177, 352–368. [Google Scholar] [CrossRef]
  31. Salvador-Guirao, R.; Baldrich, P.; Weigel, D.; Rubio-Somoza, I.; San Segundo, B. The microRNA miR773 is involved in the Arabidopsis immune response to fungal pathogens. Mol. Plant Microbe Interact. 2017. [Google Scholar] [CrossRef]
  32. Wang, C.; He, X.; Wang, X.; Zhang, S.; Guo, X. ghr-miR5272a-mediated regulation of GhMKK6 gene transcription contributes to the immune response in cotton. J. Exp. Bot. 2017. [Google Scholar] [CrossRef] [PubMed]
  33. Hewezi, T.; Piya, S.; Qi, M.; Balasubramaniam, M.; Rice, J.H.; Baum, T.J. Arabidopsis miR827 mediates post-transcriptional gene silencing of its ubiquitin E3 ligase target gene in the syncytium of the cyst nematode Heterodera schachtii to enhance susceptibility. Plant J. Cell Mol. Biol. 2016, 88, 179–192. [Google Scholar] [CrossRef] [PubMed]
  34. Zhang, X.; Zhao, H.; Gao, S.; Wang, W.C.; Katiyar-Agarwal, S.; Huang, H.D.; Raikhel, N.; Jin, H. Arabidopsis Argonaute 2 regulates innate immunity via miRNA393(*)-mediated silencing of a Golgi-localized SNARE gene, MEMB12. Mol. Cell 2011, 42, 356–366. [Google Scholar] [CrossRef] [PubMed]
  35. Niu, D.; Lii, Y.E.; Chellappan, P.; Lei, L.; Peralta, K.; Jiang, C.; Guo, J.; Coaker, G.; Jin, H. miRNA863-3p sequentially targets negative immune regulator ARLPKs and positive regulator SERRATE upon bacterial infection. Nat. Commun. 2016, 7, 11324. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Tian, D.; Traw, M.B.; Chen, J.Q.; Kreitman, M.; Bergelson, J. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 2003, 423, 74–77. [Google Scholar] [CrossRef] [PubMed]
  37. Zhai, J.; Jeong, D.H.; De Paoli, E.; Park, S.; Rosen, B.D.; Li, Y.; Gonzalez, A.J.; Yan, Z.; Kitto, S.L.; Grusak, M.A.; et al. MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev. 2011, 25, 2540–2553. [Google Scholar] [CrossRef] [Green Version]
  38. Fei, Q.; Xia, R.; Meyers, B.C. Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell 2013, 25, 2400–2415. [Google Scholar] [CrossRef]
  39. He, X.F.; Fang, Y.Y.; Feng, L.; Guo, H.S. Characterization of conserved and novel microRNAs and their targets, including a TuMV-induced TIR-NBS-LRR class R gene-derived novel miRNA in Brassica. FEBS Lett. 2008, 582, 2445–2452. [Google Scholar] [CrossRef]
  40. Li, F.; Pignatta, D.; Bendix, C.; Brunkard, J.O.; Cohn, M.M.; Tung, J.; Sun, H.; Kumar, P.; Baker, B. MicroRNA regulation of plant innate immune receptors. Proc. Natl. Acad. Sci. USA 2012, 109, 1790–1795. [Google Scholar] [CrossRef] [Green Version]
  41. Deng, Y.; Wang, J.; Tung, J.; Liu, D.; Zhou, Y.; He, S.; Du, Y.; Baker, B.; Li, F. A role for small RNA in regulating innate immunity during plant growth. PLoS Pathog. 2018, 14, e1006756. [Google Scholar] [CrossRef] [PubMed]
  42. Ouyang, S.; Park, G.; Atamian, H.S.; Han, C.S.; Stajich, J.E.; Kaloshian, I.; Borkovich, K.A. MicroRNAs suppress NB domain genes in tomato that confer resistance to Fusarium oxysporum. PLoS Pathog. 2014, 10, e1004464. [Google Scholar] [CrossRef] [PubMed]
  43. Boccara, M.; Sarazin, A.; Thiebeauld, O.; Jay, F.; Voinnet, O.; Navarro, L.; Colot, V. The Arabidopsis miR472-RDR6 silencing pathway modulates PAMP- and effector-triggered immunity through the post-transcriptional control of disease resistance genes. PLoS Pathog. 2014, 10, e1003883. [Google Scholar] [CrossRef] [PubMed]
  44. Arikit, S.; Xia, R.; Kakrana, A.; Huang, K.; Zhai, J.; Yan, Z.; Valdes-Lopez, O.; Prince, S.; Musket, T.A.; Nguyen, H.T.; et al. An atlas of soybean small RNAs identifies phased siRNAs from hundreds of coding genes. Plant Cell 2014, 26, 4584–4601. [Google Scholar] [CrossRef] [PubMed]
  45. Xia, R.; Xu, J.; Arikit, S.; Meyers, B.C. Extensive Families of miRNAs and PHAS Loci in Norway Spruce Demonstrate the Origins of Complex phasiRNA Networks in Seed Plants. Mol. Biol. Evol. 2015, 32, 2905–2918. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Wei, B.; Cai, T.; Zhang, R.; Li, A.; Huo, N.; Li, S.; Gu, Y.Q.; Vogel, J.; Jia, J.; Qi, Y.; et al. Novel microRNAs uncovered by deep sequencing of small RNA transcriptomes in bread wheat (Triticum aestivum L.) and Brachypodium distachyon (L.) Beauv. Funct. Integr. Genom. 2009, 9, 499–511. [Google Scholar] [CrossRef] [PubMed]
  47. Liu, J.; Cheng, X.; Liu, D.; Xu, W.; Wise, R.; Shen, Q.H. The miR9863 family regulates distinct Mla alleles in barley to attenuate NLR receptor-triggered disease resistance and cell-death signaling. PLoS Genet. 2014, 10, e1004755. [Google Scholar] [CrossRef]
  48. Zhang, B.; Pan, X.; Cannon, C.H.; Cobb, G.P.; Anderson, T.A. Conservation and divergence of plant microRNA genes. Plant J. Cell Mol. Biol. 2006, 46, 243–259. [Google Scholar] [CrossRef]
  49. Sunkar, R.; Jagadeeswaran, G. In silico identification of conserved microRNAs in large number of diverse plant species. BMC Plant Biol. 2008, 8, 37. [Google Scholar] [CrossRef]
  50. Sorin, C.; Declerck, M.; Christ, A.; Blein, T.; Ma, L.; Lelandais-Briere, C.; Njo, M.F.; Beeckman, T.; Crespi, M.; Hartmann, C. A miR169 isoform regulates specific NF-YA targets and root architecture in Arabidopsis. New Phytol. 2014, 202, 1197–1211. [Google Scholar] [CrossRef] [Green Version]
  51. Zhao, M.; Ding, H.; Zhu, J.K.; Zhang, F.; Li, W.X. Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. New Phytol. 2011, 190, 906–915. [Google Scholar] [CrossRef] [PubMed]
  52. Li, W.X.; Oono, Y.; Zhu, J.; He, X.J.; Wu, J.M.; Iida, K.; Lu, X.Y.; Cui, X.; Jin, H.; Zhu, J.K. The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 2008, 20, 2238–2251. [Google Scholar] [CrossRef] [PubMed]
  53. Rodriguez, R.E.; Ercoli, M.F.; Debernardi, J.M.; Breakfield, N.W.; Mecchia, M.A.; Sabatini, M.; Cools, T.; De Veylder, L.; Benfey, P.N.; Palatnik, J.F. MicroRNA miR396 Regulates the Switch between Stem Cells and Transit-Amplifying Cells in Arabidopsis Roots. Plant Cell 2015, 27, 3354–3366. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Gao, F.; Wang, K.; Liu, Y.; Chen, Y.; Chen, P.; Shi, Z.; Luo, J.; Jiang, D.; Fan, F.; Zhu, Y.; et al. Blocking miR396 increases rice yield by shaping inflorescence architecture. Nat. Plants 2015, 2, 15196. [Google Scholar] [CrossRef] [PubMed]
  55. Wang, H.; Wang, H. The miR156/SPL Module, a Regulatory Hub and Versatile Toolbox, Gears up Crops for Enhanced Agronomic Traits. Mol. Plant 2015, 8, 677–688. [Google Scholar] [CrossRef] [PubMed]
  56. Yuan, N.; Yuan, S.; Li, Z.; Li, D.; Hu, Q.; Luo, H. Heterologous expression of a rice miR395 gene in Nicotiana tabacum impairs sulfate homeostasis. Sci. Rep. 2016, 6, 28791. [Google Scholar] [CrossRef] [Green Version]
  57. Liang, G.; Yang, F.; Yu, D. MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant J. Cell Mol. Biol. 2010, 62, 1046–1057. [Google Scholar] [CrossRef]
  58. Zhao, Y.T.; Wang, M.; Wang, Z.M.; Fang, R.X.; Wang, X.J.; Jia, Y.T. Dynamic and Coordinated Expression Changes of Rice Small RNAs in Response to Xanthomonas oryzae pv. oryzae. J. Genet. Genom. 2015, 42, 625–637. [Google Scholar] [CrossRef]
  59. Li, Q.; Deng, C.; Xia, Y.; Kong, L.; Zhang, H.; Zhang, S.; Wang, J. Identification of novel miRNAs and miRNA expression profiling in embryogenic tissues of Picea balfouriana treated by 6-benzylaminopurine. PLoS ONE 2017, 12, e0176112. [Google Scholar] [CrossRef]
  60. Zhai, J.; Zhang, H.; Arikit, S.; Huang, K.; Nan, G.L.; Walbot, V.; Meyers, B.C. Spatiotemporally dynamic, cell-type-dependent premeiotic and meiotic phasiRNAs in maize anthers. Proc. Natl. Acad. Sci. USA 2015, 112, 3146–3151. [Google Scholar] [CrossRef]
  61. Johnson, C.; Kasprzewska, A.; Tennessen, K.; Fernandes, J.; Nan, G.L.; Walbot, V.; Sundaresan, V.; Vance, V.; Bowman, L.H. Clusters and superclusters of phased small RNAs in the developing inflorescence of rice. Genome Res. 2009, 19, 1429–1440. [Google Scholar] [CrossRef] [Green Version]
  62. Song, X.; Li, P.; Zhai, J.; Zhou, M.; Ma, L.; Liu, B.; Jeong, D.H.; Nakano, M.; Cao, S.; Liu, C.; et al. Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J. Cell Mol. Biol. 2012, 69, 462–474. [Google Scholar] [CrossRef]
  63. Tang, D.; Wang, G.; Zhou, J.M. Receptor Kinases in Plant-Pathogen Interactions: More Than Pattern Recognition. Plant Cell 2017, 29, 618–637. [Google Scholar] [CrossRef] [Green Version]
  64. Kourelis, J.; van der Hoorn, R.A.L. Defended to the Nines: 25 Years of Resistance Gene Cloning Identifies Nine Mechanisms for R Protein Function. Plant Cell 2018, 30, 285–299. [Google Scholar] [CrossRef] [PubMed]
  65. Gomez-Gomez, L.; Boller, T. FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 2000, 5, 1003–1011. [Google Scholar] [CrossRef]
  66. Trda, L.; Fernandez, O.; Boutrot, F.; Heloir, M.C.; Kelloniemi, J.; Daire, X.; Adrian, M.; Clement, C.; Zipfel, C.; Dorey, S.; et al. The grapevine flagellin receptor VvFLS2 differentially recognizes flagellin-derived epitopes from the endophytic growth-promoting bacterium Burkholderia phytofirmans and plant pathogenic bacteria. New Phytol. 2014, 201, 1371–1384. [Google Scholar] [CrossRef] [PubMed]
  67. Hao, G.; Pitino, M.; Duan, Y.; Stover, E. Reduced Susceptibility to Xanthomonas citri in Transgenic Citrus Expressing the FLS2 Receptor From Nicotiana benthamiana. Mol. Plant Microbe Interact. 2016, 29, 132–142. [Google Scholar] [CrossRef] [PubMed]
  68. Katsuragi, Y.; Takai, R.; Furukawa, T.; Hirai, H.; Morimoto, T.; Katayama, T.; Murakami, T.; Che, F.S. CD2-1, the C-Terminal Region of Flagellin, Modulates the Induction of Immune Responses in Rice. Mol. Plant Microbe Interact. 2015, 28, 648–658. [Google Scholar] [CrossRef] [PubMed]
  69. Robatzek, S.; Bittel, P.; Chinchilla, D.; Kochner, P.; Felix, G.; Shiu, S.H.; Boller, T. Molecular identification and characterization of the tomato flagellin receptor LeFLS2, an orthologue of Arabidopsis FLS2 exhibiting characteristically different perception specificities. Plant Mol. Biol. 2007, 64, 539–547. [Google Scholar] [CrossRef] [Green Version]
  70. Zipfel, C.; Kunze, G.; Chinchilla, D.; Caniard, A.; Jones, J.D.; Boller, T.; Felix, G. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 2006, 125, 749–760. [Google Scholar] [CrossRef]
  71. Yamaguchi, Y.; Huffaker, A.; Bryan, A.C.; Tax, F.E.; Ryan, C.A. PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 2010, 22, 508–522. [Google Scholar] [CrossRef] [PubMed]
  72. Albert, I.; Bohm, H.; Albert, M.; Feiler, C.E.; Imkampe, J.; Wallmeroth, N.; Brancato, C.; Raaymakers, T.M.; Oome, S.; Zhang, H.; et al. An RLP23-SOBIR1-BAK1 complex mediates NLP-triggered immunity. Nat. Plants 2015, 1, 15140. [Google Scholar] [CrossRef] [PubMed]
  73. Zhang, W.; Fraiture, M.; Kolb, D.; Loffelhardt, B.; Desaki, Y.; Boutrot, F.F.; Tor, M.; Zipfel, C.; Gust, A.A.; Brunner, F. Arabidopsis receptor-like protein30 and receptor-like kinase suppressor of BIR1-1/EVERSHED mediate innate immunity to necrotrophic fungi. Plant Cell 2013, 25, 4227–4241. [Google Scholar] [CrossRef] [PubMed]
  74. Sun, Y.; Li, L.; Macho, A.P.; Han, Z.; Hu, Z.; Zipfel, C.; Zhou, J.M.; Chai, J. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 2013, 342, 624–628. [Google Scholar] [CrossRef] [PubMed]
  75. Liu, T.; Liu, Z.; Song, C.; Hu, Y.; Han, Z.; She, J.; Fan, F.; Wang, J.; Jin, C.; Chang, J.; et al. Chitin-induced dimerization activates a plant immune receptor. Science 2012, 336, 1160–1164. [Google Scholar] [CrossRef]
  76. Hayafune, M.; Berisio, R.; Marchetti, R.; Silipo, A.; Kayama, M.; Desaki, Y.; Arima, S.; Squeglia, F.; Ruggiero, A.; Tokuyasu, K.; et al. Chitin-induced activation of immune signaling by the rice receptor CEBiP relies on a unique sandwich-type dimerization. Proc. Natl. Acad. Sci. USA 2014, 111, E404–E413. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  77. Meng, X.; Zhang, S. MAPK cascades in plant disease resistance signaling. Annu. Rev. Phytopathol. 2013, 51, 245–266. [Google Scholar] [CrossRef]
  78. Bi, G.; Zhou, Z.; Wang, W.; Li, L.; Rao, S.; Wu, Y.; Zhang, X.; Menke, F.L.H.; Chen, S.; Zhou, J.M. Receptor-like Cytoplasmic Kinases Directly Link Diverse Pattern Recognition Receptors to the Activation of Mitogen-activated Protein Kinase Cascades in Arabidopsis. Plant Cell 2018. [Google Scholar] [CrossRef]
  79. 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] [Green Version]
  80. Cheng, H.; Liu, H.; Deng, Y.; Xiao, J.; Li, X.; Wang, S. The WRKY45-2 WRKY13 WRKY42 transcriptional regulatory cascade is required for rice resistance to fungal pathogen. Plant Physiol. 2015, 167, 1087–1099. [Google Scholar] [CrossRef]
  81. Qiu, D.; Xiao, J.; Ding, X.; Xiong, M.; Cai, M.; Cao, Y.; Li, X.; Xu, C.; Wang, S. OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol. Plant Microbe Interact. 2007, 20, 492–499. [Google Scholar] [CrossRef] [PubMed]
  82. Johnson, C.; Boden, E.; Arias, J. Salicylic acid and NPR1 induce the recruitment of trans-activating TGA factors to a defense gene promoter in Arabidopsis. Plant Cell 2003, 15, 1846–1858. [Google Scholar] [CrossRef] [PubMed]
  83. 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] [PubMed] [Green Version]
  84. Baum, J.A.; Bogaert, T.; Clinton, W.; Heck, G.R.; Feldmann, P.; Ilagan, O.; Johnson, S.; Plaetinck, G.; Munyikwa, T.; Pleau, M.; et al. Control of coleopteran insect pests through RNA interference. Nat. Biotechnol. 2007, 25, 1322–1326. [Google Scholar] [CrossRef]
  85. Mao, Y.B.; Cai, W.J.; Wang, J.W.; Hong, G.J.; Tao, X.Y.; Wang, L.J.; Huang, Y.P.; Chen, X.Y. Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat. Biotechnol. 2007, 25, 1307–1313. [Google Scholar] [CrossRef]
  86. Huang, G.; Allen, R.; Davis, E.L.; Baum, T.J.; Hussey, R.S. Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. Proc. Natl. Acad. Sci. USA 2006, 103, 14302–14306. [Google Scholar] [CrossRef] [Green Version]
  87. Pliego, C.; Nowara, D.; Bonciani, G.; Gheorghe, D.M.; Xu, R.; Surana, P.; Whigham, E.; Nettleton, D.; Bogdanove, A.J.; Wise, R.P.; et al. Host-induced gene silencing in barley powdery mildew reveals a class of ribonuclease-like effectors. Mol. Plant Microbe Interact. 2013, 26, 633–642. [Google Scholar] [CrossRef]
  88. Panwar, V.; McCallum, B.; Bakkeren, G. Host-induced gene silencing of wheat leaf rust fungus Puccinia triticina pathogenicity genes mediated by the Barley stripe mosaic virus. Plant Mol. Biol. 2013, 81, 595–608. [Google Scholar] [CrossRef]
  89. Panwar, V.; McCallum, B.; Bakkeren, G. Endogenous silencing of Puccinia triticina pathogenicity genes through in planta-expressed sequences leads to the suppression of rust diseases on wheat. Plant J. Cell Mol. Biol. 2013, 73, 521–532. [Google Scholar] [CrossRef]
  90. Koch, A.; Kumar, N.; Weber, L.; Keller, H.; Imani, J.; Kogel, K.H. Host-induced gene silencing of cytochrome P450 lanosterol C14alpha-demethylase-encoding genes confers strong resistance to Fusarium species. Proc. Natl. Acad. Sci. USA 2013, 110, 19324–19329. [Google Scholar] [CrossRef]
  91. Jahan, S.N.; Asman, A.K.; Corcoran, P.; Fogelqvist, J.; Vetukuri, R.R.; Dixelius, C. Plant-mediated gene silencing restricts growth of the potato late blight pathogen Phytophthora infestans. J. Exp. Bot. 2015, 66, 2785–2794. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  92. Vega-Arreguin, J.C.; Jalloh, A.; Bos, J.I.; Moffett, P. Recognition of an Avr3a homologue plays a major role in mediating nonhost resistance to Phytophthora capsici in Nicotiana species. Mol. Plant Microbe Interact. 2014, 27, 770–780. [Google Scholar] [CrossRef]
  93. Wang, M.; Weiberg, A.; Lin, F.M.; Thomma, B.P.; Huang, H.D.; Jin, H. Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. Nat. Plants 2016, 2, 16151. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  94. Timmons, L.; Court, D.L.; Fire, A. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 2001, 263, 103–112. [Google Scholar] [CrossRef]
  95. Koch, A.; Biedenkopf, D.; Furch, A.; Weber, L.; Rossbach, O.; Abdellatef, E.; Linicus, L.; Johannsmeier, J.; Jelonek, L.; Goesmann, A.; et al. An RNAi-Based Control of Fusarium graminearum Infections Through Spraying of Long dsRNAs Involves a Plant Passage and Is Controlled by the Fungal Silencing Machinery. PLoS Pathog. 2016, 12, e1005901. [Google Scholar] [CrossRef] [PubMed]
  96. Mitter, N.; Worrall, E.A.; Robinson, K.E.; Li, P.; Jain, R.G.; Taochy, C.; Fletcher, S.J.; Carroll, B.J.; Lu, G.Q.; Xu, Z.P. Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Nat. Plants 2017, 3, 16207. [Google Scholar] [CrossRef] [PubMed]
  97. Mur, L.A.; Kenton, P.; Lloyd, A.J.; Ougham, H.; Prats, E. The hypersensitive response; the centenary is upon us but how much do we know? J. Exp. Bot. 2008, 59, 501–520. [Google Scholar] [CrossRef] [PubMed]
  98. Zhang, R.; Murat, F.; Pont, C.; Langin, T.; Salse, J. Paleo-evolutionary plasticity of plant disease resistance genes. BMC Genom. 2014, 15, 187. [Google Scholar] [CrossRef] [PubMed]
  99. El Kasmi, F.; Chung, E.H.; Anderson, R.G.; Li, J.; Wan, L.; Eitas, T.K.; Gao, Z.; Dangl, J.L. Signaling from the plasma-membrane localized plant immune receptor RPM1 requires self-association of the full-length protein. Proc. Natl. Acad. Sci. USA 2017, 114, E7385–E7394. [Google Scholar] [CrossRef] [Green Version]
  100. Ilag, L.L.; Yadav, R.C.; Huang, N.; Ronald, P.C.; Ausubel, F.M. Isolation and characterization of disease resistance gene homologues from rice cultivar IR64. Gene 2000, 255, 245–255. [Google Scholar] [CrossRef] [Green Version]
  101. Qi, D.; DeYoung, B.J.; Innes, R.W. Structure-function analysis of the coiled-coil and leucine-rich repeat domains of the RPS5 disease resistance protein. Plant Physiol. 2012, 158, 1819–1832. [Google Scholar] [CrossRef] [PubMed]
  102. Shirano, Y.; Kachroo, P.; Shah, J.; Klessig, D.F. A gain-of-function mutation in an Arabidopsis Toll Interleukin1 receptor-nucleotide binding site-leucine-rich repeat type R gene triggers defense responses and results in enhanced disease resistance. Plant Cell 2002, 14, 3149–3162. [Google Scholar] [CrossRef] [PubMed]
  103. Narusaka, M.; Shirasu, K.; Noutoshi, Y.; Kubo, Y.; Shiraishi, T.; Iwabuchi, M.; Narusaka, Y. RRS1 and RPS4 provide a dual Resistance-gene system against fungal and bacterial pathogens. Plant J. Cell Mol. Biol. 2009, 60, 218–226. [Google Scholar] [CrossRef] [PubMed]
  104. Bittner-Eddy, P.D.; Crute, I.R.; Holub, E.B.; Beynon, J.L. RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. Plant J. 2000, 21, 177–188. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  105. Botella, M.A.; Parker, J.E.; Frost, L.N.; Bittner-Eddy, P.D.; Beynon, J.L.; Daniels, M.J.; Holub, E.B.; Jones, J.D. Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants. Plant Cell 1998, 10, 1847–1860. [Google Scholar] [CrossRef] [PubMed]
  106. Van der Biezen, E.A.; Freddie, C.T.; Kahn, K.; Parker, J.E.; Jones, J.D. Arabidopsis RPP4 is a member of the RPP5 multigene family of TIR-NB-LRR genes and confers downy mildew resistance through multiple signalling components. Plant J. Cell Mol. Biol. 2002, 29, 439–451. [Google Scholar] [CrossRef] [Green Version]
  107. Parker, J.E.; Coleman, M.J.; Szabo, V.; Frost, L.N.; Schmidt, R.; van der Biezen, E.A.; Moores, T.; Dean, C.; Daniels, M.J.; Jones, J.D. The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. Plant Cell 1997, 9, 879–894. [Google Scholar] [CrossRef]
  108. Noel, L.; Moores, T.L.; van Der Biezen, E.A.; Parniske, M.; Daniels, M.J.; Parker, J.E.; Jones, J.D. Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell 1999, 11, 2099–2112. [Google Scholar] [CrossRef]
  109. Bryan, G.T.; Wu, K.S.; Farrall, L.; Jia, Y.; Hershey, H.P.; McAdams, S.A.; Faulk, K.N.; Donaldson, G.K.; Tarchini, R.; Valent, B. tA single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta. Plant Cell 2000, 12, 2033–2046. [Google Scholar] [CrossRef]
  110. Cesari, S.; Thilliez, G.; Ribot, C.; Chalvon, V.; Michel, C.; Jauneau, A.; Rivas, S.; Alaux, L.; Kanzaki, H.; Okuyama, Y.; et al. The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. Plant Cell 2013, 25, 1463–1481. [Google Scholar] [CrossRef]
  111. Liu, X.; Lin, F.; Wang, L.; Pan, Q. The in silico map-based cloning of Pi36, a rice coiled-coil nucleotide-binding site leucine-rich repeat gene that confers race-specific resistance to the blast fungus. Genetics 2007, 176, 2541–2549. [Google Scholar] [CrossRef] [PubMed]
  112. Qu, S.; Liu, G.; Zhou, B.; Bellizzi, M.; Zeng, L.; Dai, L.; Han, B.; Wang, G.L. The broad-spectrum blast resistance gene Pi9 encodes a nucleotide-binding site-leucine-rich repeat protein and is a member of a multigene family in rice. Genetics 2006, 172, 1901–1914. [Google Scholar] [CrossRef] [PubMed]
  113. Zhou, B.; Qu, S.; Liu, G.; Dolan, M.; Sakai, H.; Lu, G.; Bellizzi, M.; Wang, G.L. The eight amino-acid differences within three leucine-rich repeats between Pi2 and Piz-t resistance proteins determine the resistance specificity to Magnaporthe grisea. Mol. Plant Microbe Interact. 2006, 19, 1216–1228. [Google Scholar] [CrossRef] [PubMed]
  114. Shang, J.; Tao, Y.; Chen, X.; Zou, Y.; Lei, C.; Wang, J.; Li, X.; Zhao, X.; Zhang, M.; Lu, Z.; et al. Identification of a new rice blast resistance gene, Pid3, by genomewide comparison of paired nucleotide-binding site--leucine-rich repeat genes and their pseudogene alleles between the two sequenced rice genomes. Genetics 2009, 182, 1303–1311. [Google Scholar] [CrossRef] [PubMed]
  115. Lee, S.K.; Song, M.Y.; Seo, Y.S.; Kim, H.K.; Ko, S.; Cao, P.J.; Suh, J.P.; Yi, G.; Roh, J.H.; Lee, S.; et al. Rice Pi5-mediated resistance to Magnaporthe oryzae requires the presence of two coiled-coil-nucleotide-binding-leucine-rich repeat genes. Genetics 2009, 181, 1627–1638. [Google Scholar] [CrossRef]
  116. Kawano, Y.; Akamatsu, A.; Hayashi, K.; Housen, Y.; Okuda, J.; Yao, A.; Nakashima, A.; Takahashi, H.; Yoshida, H.; Wong, H.L.; et al. Activation of a Rac GTPase by the NLR family disease resistance protein Pit plays a critical role in rice innate immunity. Cell Host Microbe 2010, 7, 362–375. [Google Scholar] [CrossRef]
  117. Yuan, B.; Zhai, C.; Wang, W.; Zeng, X.; Xu, X.; Hu, H.; Lin, F.; Wang, L.; Pan, Q. The Pik-p resistance to Magnaporthe oryzae in rice is mediated by a pair of closely linked CC-NBS-LRR genes. Theor. Appl. Genet. 2011, 122, 1017–1028. [Google Scholar] [CrossRef]
  118. Okuyama, Y.; Kanzaki, H.; Abe, A.; Yoshida, K.; Tamiru, M.; Saitoh, H.; Fujibe, T.; Matsumura, H.; Shenton, M.; Galam, D.C.; et al. A multifaceted genomics approach allows the isolation of the rice Pia-blast resistance gene consisting of two adjacent NBS-LRR protein genes. Plant J. Cell Mol. Biol. 2011, 66, 467–479. [Google Scholar] [CrossRef]
  119. Lin, F.; Chen, S.; Que, Z.; Wang, L.; Liu, X.; Pan, Q. The blast resistance gene Pi37 encodes a nucleotide binding site leucine-rich repeat protein and is a member of a resistance gene cluster on rice chromosome 1. Genetics 2007, 177, 1871–1880. [Google Scholar] [CrossRef]
  120. Sakamoto, K.; Tada, Y.; Yokozeki, Y.; Akagi, H.; Hayashi, N.; Fujimura, T.; Ichikawa, N. Chemical induction of disease resistance in rice is correlated with the expression of a gene encoding a nucleotide binding site and leucine-rich repeats. Plant Mol. Biol. 1999, 40, 847–855. [Google Scholar] [CrossRef]
  121. Bai, S.; Liu, J.; Chang, C.; Zhang, L.; Maekawa, T.; Wang, Q.; Xiao, W.; Liu, Y.; Chai, J.; Takken, F.L.; et al. Structure-function analysis of barley NLR immune receptor MLA10 reveals its cell compartment specific activity in cell death and disease resistance. PLoS Pathog. 2012, 8, e1002752. [Google Scholar] [CrossRef] [PubMed]
  122. Zhou, F.; Kurth, J.; Wei, F.; Elliott, C.; Vale, G.; Yahiaoui, N.; Keller, B.; Somerville, S.; Wise, R.; Schulze-Lefert, P. Cell-autonomous expression of barley Mla1 confers race-specific resistance to the powdery mildew fungus via a Rar1-independent signaling pathway. Plant Cell 2001, 13, 337–350. [Google Scholar] [CrossRef] [PubMed]
  123. Hein, I.; Campbell, E.I.; Woodhead, M.; Hedley, P.E.; Young, V.; Morris, W.L.; Ramsay, L.; Stockhaus, J.; Lyon, G.D.; Newton, A.C.; et al. Characterisation of early transcriptional changes involving multiple signalling pathways in the Mla13 barley interaction with powdery mildew (Blumeria graminis f. sp. hordei). Planta 2004, 218, 803–813. [Google Scholar] [CrossRef] [PubMed]
  124. Dodds, P.N.; Lawrence, G.J.; Ellis, J.G. Six amino acid changes confined to the leucine-rich repeat beta-strand/beta-turn motif determine the difference between the P and P2 rust resistance specificities in flax. Plant Cell 2001, 13, 163–178. [Google Scholar] [CrossRef]
  125. Lawrence, G.; Finnegan, J.; Ellis, J. Instability of the L6 gene for rust resistance in flax is correlated with the presence of a linked Ac element. Plant J. Cell Mol. Biol. 1993, 4, 659–669. [Google Scholar] [CrossRef] [Green Version]
  126. Lawrence, G.J.; Anderson, P.A.; Dodds, P.N.; Ellis, J.G. Relationships between rust resistance genes at the M locus in flax. Mol. Plant Pathol. 2010, 11, 19–32. [Google Scholar] [CrossRef]
  127. Ellis, J.G.; Lawrence, G.J.; Luck, J.E.; Dodds, P.N. Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 1999, 11, 495–506. [Google Scholar] [CrossRef] [PubMed]
  128. Ravensdale, M.; Bernoux, M.; Ve, T.; Kobe, B.; Thrall, P.H.; Ellis, J.G.; Dodds, P.N. Intramolecular interaction influences binding of the Flax L5 and L6 resistance proteins to their AvrL567 ligands. PLoS Pathog. 2012, 8, e1003004. [Google Scholar] [CrossRef] [PubMed]
  129. Ellis, J.G.; Lawrence, G.J.; Dodds, P.N. Further analysis of gene-for-gene disease resistance specificity in flax. Mol. Plant Pathol. 2007, 8, 103–109. [Google Scholar] [CrossRef] [PubMed]
  130. Zhang, X.; Farah, N.; Rolston, L.; Ericsson, D.J.; Catanzariti, A.M.; Bernoux, M.; Ve, T.; Bendak, K.; Chen, C.; Mackay, J.P.; et al. Crystal structure of the Melampsora lini effector AvrP reveals insights into a possible nuclear function and recognition by the flax disease resistance protein P. Mol. Plant Pathol. 2018, 19, 1196–1209. [Google Scholar] [CrossRef] [PubMed]
  131. Yoshimura, S.; Yamanouchi, U.; Katayose, Y.; Toki, S.; Wang, Z.X.; Kono, I.; Kurata, N.; Yano, M.; Iwata, N.; Sasaki, T. Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc. Natl. Acad. Sci. USA 1998, 95, 1663–1668. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  132. Bendahmane, A.; Querci, M.; Kanyuka, K.; Baulcombe, D.C. Agrobacterium transient expression system as a tool for the isolation of disease resistance genes: Application to the Rx2 locus in potato. Plant J. Cell Mol. Biol. 2000, 21, 73–81. [Google Scholar] [CrossRef]
  133. Mago, R.; Zhang, P.; Vautrin, S.; Simkova, H.; Bansal, U.; Luo, M.C.; Rouse, M.; Karaoglu, H.; Periyannan, S.; Kolmer, J.; et al. The wheat Sr50 gene reveals rich diversity at a cereal disease resistance locus. Nat. Plants 2015, 1, 15186. [Google Scholar] [CrossRef] [PubMed]
  134. Saintenac, C.; Zhang, W.; Salcedo, A.; Rouse, M.N.; Trick, H.N.; Akhunov, E.; Dubcovsky, J. Identification of wheat gene Sr35 that confers resistance to Ug99 stem rust race group. Science 2013, 341, 783–786. [Google Scholar] [CrossRef] [PubMed]
  135. Kema, G.H.J.; Mirzadi Gohari, A.; Aouini, L.; Gibriel, H.A.Y.; Ware, S.B.; van den Bosch, F.; Manning-Smith, R.; Alonso-Chavez, V.; Helps, J.; Ben M’Barek, S.; et al. Stress and sexual reproduction affect the dynamics of the wheat pathogen effector AvrStb6 and strobilurin resistance. Nat. Genet. 2018, 50, 375–380. [Google Scholar] [CrossRef]
  136. Tian, D.; Wang, J.; Zeng, X.; Gu, K.; Qiu, C.; Yang, X.; Zhou, Z.; Goh, M.; Luo, Y.; Murata-Hori, M.; et al. The rice TAL effector-dependent resistance protein XA10 triggers cell death and calcium depletion in the endoplasmic reticulum. Plant Cell 2014, 26, 497–515. [Google Scholar] [CrossRef]
  137. Wang, J.; Tian, D.; Gu, K.; Yang, X.; Wang, L.; Zeng, X.; Yin, Z. Induction of Xa10-like Genes in Rice Cultivar Nipponbare Confers Disease Resistance to Rice Bacterial Blight. Mol. Plant Microbe Interact. 2017, 30, 466–477. [Google Scholar] [CrossRef]
  138. Brunner, S.; Stirnweis, D.; Diaz Quijano, C.; Buesing, G.; Herren, G.; Parlange, F.; Barret, P.; Tassy, C.; Sautter, C.; Winzeler, M.; et al. Transgenic Pm3 multilines of wheat show increased powdery mildew resistance in the field. Plant Biotechnol. J. 2012, 10, 398–409. [Google Scholar] [CrossRef]
  139. Molnar, A.; Melnyk, C.W.; Bassett, A.; Hardcastle, T.J.; Dunn, R.; Baulcombe, D.C. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 2010, 328, 872–875. [Google Scholar] [CrossRef]
  140. Weiberg, A.; Wang, M.; Lin, F.M.; Zhao, H.; Zhang, Z.; Kaloshian, I.; Huang, H.D.; Jin, H. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 2013, 342, 118–123. [Google Scholar] [CrossRef]
  141. Shahid, S.; Kim, G.; Johnson, N.R.; Wafula, E.; Wang, F.; Coruh, C.; Bernal-Galeano, V.; Phifer, T.; dePamphilis, C.W.; Westwood, J.H.; et al. MicroRNAs from the parasitic plant Cuscuta campestris target host messenger RNAs. Nature 2018, 553, 82–85. [Google Scholar] [CrossRef] [PubMed]
  142. Wang, M.; Thomas, N.; Jin, H. Cross-kingdom RNA trafficking and environmental RNAi for powerful innovative pre- and post-harvest plant protection. Curr. Opin. Plant Biol. 2017, 38, 133–141. [Google Scholar] [CrossRef]
  143. Shiu, S.H.; Karlowski, W.M.; Pan, R.; Tzeng, Y.H.; Mayer, K.F.; Li, W.H. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 2004, 16, 1220–1234. [Google Scholar] [CrossRef] [PubMed]
  144. Fischer, I.; Dievart, A.; Droc, G.; Dufayard, J.F.; Chantret, N. Evolutionary Dynamics of the Leucine-Rich Repeat Receptor-Like Kinase (LRR-RLK) Subfamily in Angiosperms. Plant Physiol. 2016, 170, 1595–1610. [Google Scholar] [CrossRef] [PubMed]
  145. Liu, P.L.; Du, L.; Huang, Y.; Gao, S.M.; Yu, M. Origin and diversification of leucine-rich repeat receptor-like protein kinase (LRR-RLK) genes in plants. BMC Evol. Biol. 2017, 17, 47. [Google Scholar] [CrossRef] [PubMed]
  146. Akita, M.; Valkonen, J.P. A novel gene family in moss (Physcomitrella patens) shows sequence homology and a phylogenetic relationship with the TIR-NBS class of plant disease resistance genes. J. Mol. Evol. 2002, 55, 595–605. [Google Scholar] [CrossRef] [PubMed]
  147. Bertin, J.; Nir, W.J.; Fischer, C.M.; Tayber, O.V.; Errada, P.R.; Grant, J.R.; Keilty, J.J.; Gosselin, M.L.; Robison, K.E.; Wong, G.H.; et al. Human CARD4 protein is a novel CED-4/Apaf-1 cell death family member that activates NF-κB. J. Biol. Chem. 1999, 274, 12955–12958. [Google Scholar] [CrossRef]
  148. Meyers, B.C.; Morgante, M.; Michelmore, R.W. TIR-X and TIR-NBS proteins: Two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes. Plant J. Cell Mol. Biol. 2002, 32, 77–92. [Google Scholar] [CrossRef]
  149. Liu, J.J.; Ekramoddoullah, A.K. Isolation, genetic variation and expression of TIR-NBS-LRR resistance gene analogs from western white pine (Pinus monticola Dougl. ex. D. Don.). Mol. Genet. Genom. 2003, 270, 432–441. [Google Scholar] [CrossRef]
  150. Girardin, S.E.; Sansonetti, P.J.; Philpott, D.J. Intracellular vs extracellular recognition of pathogens--common concepts in mammals and flies. Trends Microbiol. 2002, 10, 193–199. [Google Scholar] [CrossRef]
  151. Bai, J.; Pennill, L.A.; Ning, J.; Lee, S.W.; Ramalingam, J.; Webb, C.A.; Zhao, B.; Sun, Q.; Nelson, J.C.; Leach, J.E.; et al. Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res. 2002, 12, 1871–1884. [Google Scholar] [CrossRef] [PubMed]
  152. Yang, S.; Zhang, X.; Yue, J.X.; Tian, D.; Chen, J.Q. Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol. Genet. Genom. 2008, 280, 187–198. [Google Scholar] [CrossRef] [PubMed]
  153. Porter, B.W.; Paidi, M.; Ming, R.; Alam, M.; Nishijima, W.T.; Zhu, Y.J. Genome-wide analysis of Carica papaya reveals a small NBS resistance gene family. Mol. Genet. Genom. 2009, 281, 609–626. [Google Scholar] [CrossRef] [PubMed]
  154. Luo, S.; Zhang, Y.; Hu, Q.; Chen, J.; Li, K.; Lu, C.; Liu, H.; Wang, W.; Kuang, H. Dynamic nucleotide-binding site and leucine-rich repeat-encoding genes in the grass family. Plant Physiol. 2012, 159, 197–210. [Google Scholar] [CrossRef] [PubMed]
  155. Guo, Y.L.; Fitz, J.; Schneeberger, K.; Ossowski, S.; Cao, J.; Weigel, D. Genome-wide comparison of nucleotide-binding site-leucine-rich repeat-encoding genes in Arabidopsis. Plant Physiol. 2011, 157, 757–769. [Google Scholar] [CrossRef] [PubMed]
  156. Shen, J.; Araki, H.; Chen, L.; Chen, J.Q.; Tian, D. Unique evolutionary mechanism in R-genes under the presence/absence polymorphism in Arabidopsis thaliana. Genetics 2006, 172, 1243–1250. [Google Scholar] [CrossRef] [PubMed]
  157. Yang, S.; Feng, Z.; Zhang, X.; Jiang, K.; Jin, X.; Hang, Y.; Chen, J.Q.; Tian, D. Genome-wide investigation on the genetic variations of rice disease resistance genes. Plant Mol. Biol. 2006, 62, 181–193. [Google Scholar] [CrossRef] [PubMed]
  158. Zheng, F.; Wu, H.; Zhang, R.; Li, S.; He, W.; Wong, F.L.; Li, G.; Zhao, S.; Lam, H.M. Molecular phylogeny and dynamic evolution of disease resistance genes in the legume family. BMC Genom. 2016, 17, 402. [Google Scholar] [CrossRef] [PubMed]
  159. Zhu, X.; Qi, T.; Yang, Q.; He, F.; Tan, C.; Ma, W.; Voegele, R.T.; Kang, Z.; Guo, J. Host-Induced Gene Silencing of the MAPKK Gene PsFUZ7 Confers Stable Resistance to Wheat Stripe Rust. Plant Physiol. 2017, 175, 1853–1863. [Google Scholar] [CrossRef] [PubMed]
  160. Qi, T.; Zhu, X.; Tan, C.; Liu, P.; Guo, J.; Kang, Z.; Guo, J. Host-induced gene silencing of an important pathogenicity factor PsCPK1 in Puccinia striiformis f. sp. tritici enhances resistance of wheat to stripe rust. Plant Biotechnol. J. 2018, 16, 797–807. [Google Scholar] [CrossRef]
Ijms 20 00335 g001 550
Figure 1. Categories of the genes/regulators in the three defense layers in plants. The data was downloaded from PRGdb database and the recent publications [20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62]. PTI: pathogen-associated molecular patterns (PAMP) triggered immunity; ETI: effector-triggered immunity; CRKI: cross-kingdom RNA interference.
Figure 1. Categories of the genes/regulators in the three defense layers in plants. The data was downloaded from PRGdb database and the recent publications [20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62]. PTI: pathogen-associated molecular patterns (PAMP) triggered immunity; ETI: effector-triggered immunity; CRKI: cross-kingdom RNA interference.
Ijms 20 00335 g001
Ijms 20 00335 g002 550
Figure 2. The interaction mechanisms of plants-pathogens from three interacted and miRNA regulation layers. (A) The three defensive layers in plants including the PTI, ETI, and cross-kingdom RNA interference (CKRI), and the three infection layers in pathogens including pattern recognition receptors (PRR), effector and CKRI. (B) The evolution of NBS-LRR genes and their regulator miRNAs. (C) The three strategies of defense to biotic stresses including uORF [83], host-induced gene silencing (HIGS) [84,85,86,87,88,89,90,91,92] and spray-induced gene silencing (SIGS) [3,93,94,95,96] in plants.
Figure 2. The interaction mechanisms of plants-pathogens from three interacted and miRNA regulation layers. (A) The three defensive layers in plants including the PTI, ETI, and cross-kingdom RNA interference (CKRI), and the three infection layers in pathogens including pattern recognition receptors (PRR), effector and CKRI. (B) The evolution of NBS-LRR genes and their regulator miRNAs. (C) The three strategies of defense to biotic stresses including uORF [83], host-induced gene silencing (HIGS) [84,85,86,87,88,89,90,91,92] and spray-induced gene silencing (SIGS) [3,93,94,95,96] in plants.
Ijms 20 00335 g002
Table
Table 1. Disease resistance genes and their regulator miRNAs in plants [98]. Mbp, million base pair; Nb, number; R-gene, disease resistance genes.
Table 1. Disease resistance genes and their regulator miRNAs in plants [98]. Mbp, million base pair; Nb, number; R-gene, disease resistance genes.
SpeciesNb Chr.Size (Mbp)Nb GeneR-Genes
Nb R-Genes(%) 1Nb MiRNA Targets(%) 2
Monocots
Oryza sativa (rice)1237241,04611962.9114412.04
Sorghum bicolor1065934,0086251.8410917.44
Zea mays (maize)10236532,5406732.0700
Brachypodium distachyon527125,5045372.1114927.75
Eudicots
Arabidopsis thaliana511933,1985031.528116.1
Populus trichocarpa1929430,2604461.4738285.65
Carica papaya923419,2052281.1900
Glycine max2094946,16411712.5429024.77
Malusxdomestica (apple)1774258,97920523.4825612.48
1 the percentage of the R-genes from the total coding genes; 2 percentage of the miRNA target genes from the R-genes.
Table
Table 2. The validated disease resistance genes and their pathogens in plants. The data were derived from PRGDB database.
Table 2. The validated disease resistance genes and their pathogens in plants. The data were derived from PRGDB database.
Plant SpeciesDiseasePathogensAvirus GenesTypes of PathogensGenesTypesGenBank Locus
Arabidopsis thalianaWhite rust of crucifersAlbugo candida OomycetesRAC1TNLAY522496
Cucumber Mosaic VirusCucumber mosaic virus VirusRCY1CNLAB087829
Bacterial BlightPseudomonas syringae/Xanthomonas oryzaeavrRpm1; avrRpt2; avrPphB; N; avrRps4BacteriumRPM1; Rps2; RPS5; SSI4; Rps4CNL; CNL; CNL; TNL; TNLNM_111584; NM_118742; NM_101094; AY179750; NM_123893
Downy mildew of cucurbitsPseudoperonospora cubensis OomycetesRPP13/RPP8; RPP1/RPP4; RPP5CNL/CNL; TNL/TNL; TNLNM_114520/NM_123713; NM_114316/NM_117790; NM_117798
Bacterial wilt of potatoRalstonia solanacearum BacteriumRRS1TNLNM_001085246
Turnip crinkle virusTurnip crinkle virus VirusHRTCNLNM_128190
Aegilops tauschiiCereal cyst nematodeHeterodera avenae NematodeCre1CNLAY124651
Capsicum chacoenseBacterial spot of tomatoXanthomonas campestrisAvrBs2BacteriumBs2CNLAF202179
Capsicum chinensePepper mild mottle virusPepper mild mottle virus VirusL3CNLBAJ33559
Cucumis meloFusarium WiltFusarium oxysporum FungalFOM-2CNLDQ287965
Melon aphid diseaseAphis gossypii insectVATCNLAGH33848
zucchini yellow mosaic viruszucchini yellow mosaic virus VirusFOM1TNLAIU36098
Glycine maxSoybean mosaic virussoybean mosaic virus VirusKR1TNLAF327903
Helianthus annuusDowny mildew of sunflowerPlasmopara halstedii OomycetesPl8CNLAY490793
Hordeum vulgarePowdery mildew (barley)Blumeria graminis FungalMLA10/MLA1/MLA13CNLAY266445; GU245961; AF523683
Lactuca sativaDowny mildew of lettuceBremia lactucaeAvr3OomycetesDm3 (RGC2B)CNLAH007213
Linum usitatissimumFlax rustMelampsora lini FungalP2/L6/M; L,L1-L11; P,P1-4TNL; TNL; TNLAF310960/U27081/U73916; AAD25974/AAK28806
Nicotiana glutinosaTobacco Mosaic VirusTobacco mosaic virus VirusNTNLU15605
Oryza sativaRice blast diseaseMagnaporthe griseaAvr-PitaFungalPi-ta/PIBCNLAY196754
Bacterial BlightPseudomonas syringae/Xanthomonas oryzae BacteriumXA1CNLAB002266
Rice blast diseaseMagnaporthe oryzae FungalRGA5CNLEU883792
Oryza sativa Indica GroupRice blast diseaseMagnaporthe grisea FungalPi36/Pi9/Pi2CNLDQ900896/DQ285630/DQ352453
Oryza sativa Japonica GroupRice blast diseaseMagnaporthe grisea FungalPiz-t/Pikm1-TS/Pikm2-TS/Pid3/Pi5-1/Pi5-2/Pit/Pikp-2CNLDQ352040/AB462324/AB462325/FJ773286/EU869185/EU869186/AB379816/HM035360
Rice blast diseaseMagnaporthe oryzae FungalPia; Pi37; Rpr1CNL; CNL; CNLAB604626; DQ923494; AC119670
Solanum acauleLatent mosaic of potato/Beet cyst nematodePotato virus X/Heterodera schachtii Virus/NematodeRx2CNLAJ249448
Solanum bulbocastanumLate Blight of tomatoPhytophthora infestans OomyceteRpi-blb1/Rpi-blb2; RBCNL; CNLAY336128; DQ122125; AY426259
Solanum demissumLate Blight of tomatoPhytophthora infestans OomyceteR1CNLAF447489
Solanum lycopersicumBacterial spot of tomatoXanthomonas campestrisHax4/AvrBs4BacteriumBs4TNLAY438027
Yellow potato cyst nematodeYellow potato cyst nematode NematodeHeroCNLAJ457052
root-knot nematodeMeloidogyne incognita NematodeMi1.2CNLAF039682
Tomato Spotted WiltTomato spotted wilt virus VirusSw-5CNLAY007366
Tobacco Mosaic VirusTobacco mosaic virusMPVirusTm-2a/Tm-2CNLF536201/AF536200
Solanum pimpinellifoliumBacterial Speck of tomatoPseudomonas syringaeAvrPto/AvrPtoBBacteriumPrfCNLAF220602
Late blightPhytophthora infestans OomycetePh-3CNLKJ563933
Solanum tuberosumYellow potato cyst nematodeGlobodera NematodeGpa2CNLAF195939
Late Blight of potatoPhytophthora infestans NematodeGro1.4TNLAY196151
Latent mosaic of potato/Beet cyst nematodePotato virus X/Heterodera schachtii VirusRxCNLAJ011801
Solanum tuberosum subsp andigenaPotato virus YPotato virus Y VirusRY-1TNLAJ300266
Triticum aestivumBrown wheat rust of potatoPuccinia triticina FungalLr10/Lr21/Lr1CNLAY270157/FJ876280/EF439840
powdery mildewBlumeria graminis f. sp. Tritici FungalPm3CNLAY325736
stem rustPuccinia graminis f. sp. Tritici FungalSr33CNLKF031303
Nematode diseaseHeterodera avenae NematodeCre3CNLAF052641
Yellow rustPuccinia striiformis Westend. f.sp. Tritici FungalYr10CNLAF149114
Triticum monococcum subsp. Monococcumstem rustPuccinia graminis f. sp. Tritici FungalSr35CNLAGP75918
Zea maysCommon rust of maizePuccinia sorghi FungalRp1-DCNLAF107293
Table
Table 3. List of regulators involved in the immunity response to pathogens in plants.
Table 3. List of regulators involved in the immunity response to pathogens in plants.
Plant miRNAsImmunity ResponseTargets in Plants or PathogensPositive (+)/Negative (−) RegulatorPathogens
ClassificationPathogen/Plant
miR393PTIF-box auxin receptorsPositiveBacteriaPseudomonas syringae/Arabidopsis
miR160aPTIauxin response factors16PositiveBacteriaPseudomonas syringae/Arabidopsis
miR319PTITCP21NegativeVirusRice ragged stunt virus (RRSV)/RICE
miR773PTIMETHYLTRANSFERASE 2NegativeBacteria; FungulPseudomonas syringae/Arabidopsis; Plectosphaerella cucumerina/Arabidopsis
miR169PTINFYANegativeBacteria; FungulMagnaporthe oryzae/RICE
miR396PTIGRFNegativeFungulPlectosphaerella cucumerina/Arabidopsis
miR156PTIMdWRKYN1NegativeFungulAlternaria alternaria/APPLE
miR395PTIMdWRKY26NegativeFungulAlternaria alternaria/APPLE
miR5272PTIMKK6NegativeFungulFusarium oxysporum/COTTON
MIR398PTICSD2NegativeBacteriaPseudomonas syringae/Arabidopsis
miR164PTINACNegativeFungulMagnaporthe oryzae/RICE
miR393*ETIMEMB12 (Membrin 12)PositiveBacteriaPseudomonas syringae/Arabidopsis
miR444ETIMADSPositiveVirusRice stripe virus (RSV)/RICE
miR171ETIOsSCL6-Iia/b/cPositiveVirusRice stripe virus (RSV)/RICE
miR863-3pETIARLPK1&ARLPK2PositiveBacteriaPseudomonas syringae/Arabidopsis
miR863-3pETISERRATENegativeBacteriaPseudomonas syringae/Arabidopsis
MIR9863ETINBS-LRRNegativeFungulBlumeria graminis/Barley
MIR482ETINBS-LRRNegativeFungulFusarium oxysporum/Tomato
MIR5300ETINBS-LRRNegativeFungulFusarium oxysporum/Tomato
miR1510ETINBS-LRRNegativeFungulPhytophthora sojae/Soybean
miR6019ETINBS-LRRNegativeVirusTobacco mosaic virus/Tobacco
miR6020ETINBS-LRRNegativeVirusTobacco mosaic virus/Tobacco
miR1885ETINBS-LRRNegativeVirusTurnip mosaic virus/Brassica
miR472ETINBS-LRRNegativeBacteriaPseudomonas syringae/Arabidopsis
miR166CKRIClp-1 1PositiveFungulVerticillium dahliae/Cotton
miR159CKRIHiC-15 1PositiveFungulVerticillium dahliae/Cotton
TAS1c-siR483CKRIBc-Vps51&Bc-DCTN1 1PositiveFungulBotrytis cinerea /Arabidopsis
TAS2-siR453CKRIBC1T_08464 1PositiveFungulBotrytis cinerea /Arabidopsis
CKRI: Cross-kingdom RNA interference; 1 Target gene from pathogen.

Share and Cite

MDPI and ACS Style

Zhang, R.; Zheng, F.; Wei, S.; Zhang, S.; Li, G.; Cao, P.; Zhao, S. Evolution of Disease Defense Genes and Their Regulators in Plants. Int. J. Mol. Sci. 2019, 20, 335. https://doi.org/10.3390/ijms20020335

AMA Style

Zhang R, Zheng F, Wei S, Zhang S, Li G, Cao P, Zhao S. Evolution of Disease Defense Genes and Their Regulators in Plants. International Journal of Molecular Sciences. 2019; 20(2):335. https://doi.org/10.3390/ijms20020335

Chicago/Turabian Style

Zhang, Rongzhi, Fengya Zheng, Shugen Wei, Shujuan Zhang, Genying Li, Peijian Cao, and Shancen Zhao. 2019. "Evolution of Disease Defense Genes and Their Regulators in Plants" International Journal of Molecular Sciences 20, no. 2: 335. https://doi.org/10.3390/ijms20020335

APA Style

Zhang, R., Zheng, F., Wei, S., Zhang, S., Li, G., Cao, P., & Zhao, S. (2019). Evolution of Disease Defense Genes and Their Regulators in Plants. International Journal of Molecular Sciences, 20(2), 335. https://doi.org/10.3390/ijms20020335

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