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Comparison of amino acids sequences of AvrRxo1 alleles. The grey text indicates identical sequence, and the deep grey indicates putative motifs. The asterisk indicates the residue that is associated with toxicity. The secondary structures under the sequences were predicted using Jpred 3 software. H indicates the α-helix; E indicates β-strand.
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AvrRxo1, a type III effector from Xanthomonas oryzae pv. oryzicola (Xoc) which causes bacterial leaf streak (BLS) in rice, can be recognised by non-host resistance protein Rxo1. It triggers a hypersensitive response (HR) in maize. Little is known regarding the virulence function of AvrRxo1. In this study, we determined that AvrRxo1 is able to suppr...
Citations
... Several non-TALEs have biological virulence functions in Xoc. For example, XopAJ/ AvrRxo1 functions as an NAD kinase to suppress ROS burst [9,10] and XopC functions as an atypical kinase that phosphorylates OSK1 to suppress stomatal immunity [11]. Most candidate targeted genes for each TALE in sequenced Xoc strains have been predicted [12,13]. ...
Xanthomonas oryzae delivers transcription activator-like effectors (TALEs) into plant cells to facilitate infection. Following economic principles, the redundant TALEs are rarely identified in Xanthomonas. Previously, we identified the Tal2b, which activates the expression of the rice 2-oxoglutarate-dependent dioxygenase gene OsF3H03g to promote infection in the highly virulent strain of X. oryzae pv. oryzicola HGA4. Here, we reveal that another clustered TALE, Tal2c, also functioned as a virulence factor to target rice OsF3H04g, a homologue of OsF3H03g. Transferring Tal2c into RS105 induced expression of OsF3H04g to coincide with increased susceptibility in rice. Overexpressing OsF3H04g caused higher susceptibility and less salicylic acid (SA) production compared to wild-type plants. Moreover, CRISPR–Cas9 system-mediated editing of the effector-binding element in the promoters of OsF3H03g or OsF3H04g was found to specifically enhance resistance to Tal2b- or Tal2c-transferring strains, but had no effect on resistance to either RS105 or HGA4. Furthermore, transcriptome analysis revealed that several reported SA-related and defense-related genes commonly altered expression in OsF3H04g overexpression line compared with those identified in OsF3H03g overexpression line. Overall, our results reveal a functional redundancy mechanism of pathogenic virulence in Xoc in which tandem Tal2b and Tal2c specifically target homologues of host genes to interfere with rice immunity by reducing SA.
... When plants growing in disease-suppressive soil are attacked by plant pathogens, the root system secretes metabolites to recruit beneficial microorganisms that protect the plants (Rosenzweig et al., 2012;Yang et al., 2016). Recently, the root system of Arabidopsis was shown to secrete amino acids, nucleotides, and long-chain organic acids that recruit beneficial microorganisms and make its progeny resistant to plant pathogens Liu et al., 2014;Yuan et al., 2018). Plant-derived nutrients attract probiotics in a specific manner, and this mechanism may be used by pathogens. ...
Soil-borne diseases cause serious economic losses in agriculture. Managing diseases with microbial preparations is an excellent approach to soil-borne disease prevention. However, microbial preparations often exhibit unstable effects, limiting their large-scale application. This review introduces and summarizes disease-suppressive soils, the relationship between carbon sources and the microbial community, and the application of human microbial preparation concepts to plant microbial preparations. We also propose an innovative synthetic microbial community assembly strategy with synergistic prebiotics to promote healthy plant growth and resistance to disease. In this review, a new approach is proposed to improve traditional microbial preparations; provide a better understanding of the relationships among carbon sources, beneficial microorganisms and plants; and lay a theoretical foundation for developing new microbial preparations.
... While both of these hydrophobic modifications can anchor proteins in membranes, S-palmitoylation confers a stronger membrane association [344]. Much of the evidence for T3SE acylation is indirect, and myristoylation is presumed based on the loss of virulence or avirulence function in glycine-to-alanine substitution mutants of AvrPto, AvrRxo1, HopF2, HopO1-1, HopZ1a, HopZ4, and XopJ [32,46,193,[346][347][348][349]. Additional substitutions at cysteine residues suggest that AvrRpm1, HopAF1, and HopZ1b are also S-palmitoylated near the N-terminus [87,350,351], and AvrPto is predicted to undergo palmitoylation as well [350]. ...
Phytopathogenic bacteria possess an arsenal of effector proteins that enable them to subvert host recognition and manipulate the host to promote pathogen fitness. The type III secretion system (T3SS) delivers type III-secreted effector proteins (T3SEs) from bacterial pathogens such as Pseudomonas syringae, Ralstonia solanacearum, and various Xanthomonas species. These T3SEs interact with and modify a range of intracellular host targets to alter their activity and thereby attenuate host immune signaling. Pathogens have evolved T3SEs with diverse biochemical activities, which can be difficult to predict in the absence of structural data. Interestingly, several T3SEs are activated following injection into the host cell. Here, we review T3SEs with documented enzymatic activities, as well as T3SEs that facilitate virulence-promoting processes either indirectly or through non-enzymatic mechanisms. We discuss the mechanisms by which T3SEs are activated in the cell, as well as how T3SEs modify host targets to promote virulence or trigger immunity. These mechanisms may suggest common enzymatic activities and convergent targets that could be manipulated to protect crop plants from infection.
... As the structured LRR domain is missing in RHR, it fails to recognize the pathogenic protein AvrRXO1 79 . The toxicity of AvrRXO1 includes complete C-terminal of this protein and in addition the putative thiol protease site, while initial 52 amino acids from the Nterminus have no impact on toxicity 80 . ATP/GTP binding site motif A is responsible for HR mediated cell death, cytotoxicity and avirulence 80 . ...
... The toxicity of AvrRXO1 includes complete C-terminal of this protein and in addition the putative thiol protease site, while initial 52 amino acids from the Nterminus have no impact on toxicity 80 . ATP/GTP binding site motif A is responsible for HR mediated cell death, cytotoxicity and avirulence 80 . ...
Proteins are essential in almost all cellular processes. The key characteristic of proteins is their ability to bind with their partner specifically and with varied affinity. Protein-protein interactions (PPIs) are the interactions of high specificity between two or multiple proteins molecules occurring due to electrostatic forces and hydrophobic effects. Critical analysis of such PPIs might give essential information to decipher the molecular mechanism of biological processes. PPIs also play a vital role in commencing host pathogen recognition. This review helps to understand PPIs in deciphering the molecular mechanism of the host-pathogen interaction and the database available for PPIs.
... Rxo1 conditions a typical HR phenotype in maize and rice upon presence of AvrRxo1 (also termed as XopAJ) or its homolog from Burkholderia andropogonis and nonhost bacterial pathogen Xoc or X. euvesicatoria [74]. However, AvrRxo1, a conserved bacterial toxin in Asian Xoc strains and some African Xoc strains, can enhance Xoo/Xoc early proliferation in rice leaves and suppress HR induced by Xoo/Xoc in nonhost N. benthamiana ( Figure 3) [75,76]. The toxicity and virulence contribution of AvrRxo1 might be associated with its nucleotide kinase activity, where AvrRxo1 phosphorylates NAD at the 3 hydroxyl position to produce 3 -NADP [77]. ...
Bacterial blight (BB) and bacterial leaf streak (BLS), caused by Xanthomonas oryzae pv. oryzae and Xanthomonas oryzae pv. oryzicola, respectively, are two devastating diseases in rice planting areas worldwide. It has been proven that adoption of rice resistance is the most effective, economic, and environment-friendly strategy to avoid yield loss caused by BB and BLS. As a model system for plant—pathogen interaction, the rice—X. oryzae pathosystem has been intensively investigated in the past decade. Abundant studies have shown that the resistance and susceptibility of rice to X. oryzae is determined by molecular interactions between rice genes or their products and various pathogen effectors. In this review, we briefly overviewed the literature regarding the diverse interactions, focusing on recent advances in uncovering mechanisms of rice resistance and X. oryzae virulence. Our analysis and discussions will not only be helpful for getting a better understanding of coevolution of the rice innate immunity and X. oryzae virulence, but it will also provide new insights for application of plant R genes in crop breeding.
... Putative homologs lacking the T3 secretion signal are also found in a variety of environmental bacteria with no known pathogenic role [5]. AvrRxo1 has been implicated in several different T3E functions; it triggers a type III secretion-dependent hypersensitive resistance response (HR) in maize or transgenic rice plants expressing the resistance protein Rxo1 [6,7], enhances virulence of Xanthomonas oryzae on rice [8], and suppresses nonhost resistance to X. oryzae on tobacco [9]. Homologs of AvrRxo1 are always encoded upstream of a gene encoding a small protein binding partner, Arc1. ...
... In addition, the AvrRxo1-dependent molecule was a spectral match to the 3'-NADP standard, confirming its identity as 3'-NADP accumulates upon AvrRxo1 expression in planta and during infection with X. oryzae pv. oryzicola AvrRxo1 is a T3E that has been associated with virulence enhancement and suppression of nonhost resistance when expressed from X. oryzae, and with phytotoxic cell collapse when transiently expressed in planta [8,9]. To determine whether AvrRxo1 phosphorylates NAD in plant cells, HA-AvrRxo1 and HA-AvrRxo1-D193T were transiently expressed in leaves of N. benthamiana. ...
... In addition to enhancing virulence, AvrRxo1 is a suppressor of flg22-mediated innate immunity in Arabidopsis [9,22]. We determined the impact of transient AvrRxo1 expression on generation of the PAMP-triggered burst of reactive oxygen species (ROS), a critical early event in plant defense signaling. ...
Gram-negative bacterial pathogens of plants and animals employ type III secreted effectors to suppress innate immunity. Most characterized effectors work through modification of host proteins or transcriptional regulators, although a few are known to modify small molecule targets. The Xanthomonas type III secreted avirulence factor AvrRxo1 is a structural homolog of the zeta toxin family of sugar-nucleotide kinases that suppresses bacterial growth. AvrRxo1 was recently reported to phosphorylate the central metabolite and signaling molecule NAD in vitro, suggesting that the effector might enhance bacterial virulence on plants through manipulation of primary metabolic pathways. In this study, we determine that AvrRxo1 phosphorylates NAD in planta, and that its kinase catalytic sites are necessary for its toxic and resistance-triggering phenotypes. A global metabolomics approach was used to independently identify 3'-NADP as the sole detectable product of AvrRxo1 expression in yeast and bacteria, and NAD kinase activity was confirmed in vitro. 3'-NADP accumulated upon transient expression of AvrRxo1 in Nicotiana benthamiana and in rice leaves infected with avrRxo1-expressing strains of X. oryzae. Mutation of the catalytic aspartic acid residue D193 abolished AvrRxo1 kinase activity and several phenotypes of AvrRxo1, including toxicity in yeast, bacteria, and plants, suppression of the flg22-triggered ROS burst, and ability to trigger an R gene-mediated hypersensitive response. A mutation in the Walker A ATP-binding motif abolished the toxicity of AvrRxo1, but did not abolish the 3'-NADP production, virulence enhancement, ROS suppression, or HR-triggering phenotypes of AvrRxo1. These results demonstrate that a type III effector targets the central metabolite and redox carrier NAD in planta, and that this catalytic activity is required for toxicity and suppression of the ROS burst.
... The virulent Xoc strain RS105, JLB2-24, HNB8-47, HGA1 and HGA2 were grown on polypeptone-sucroseagar medium (10 g l −1 polypeptone, 1 g l −1 glutamic acid, 10 g l −1 sucrose and 15 g l −1 agar) at 28°C for 2 days and then resuspended in sterile 10 mM MgCl 2 to OD 600 = 0.5. More than five newly expanded leaves were infiltrated at three positions with a non-needle syringe at the seedling stage (Liu et al. 2014). The lesion length was scored at 14 days post-inoculation (dpi). ...
Background
The small heat shock proteins represent a large family of proteins that respond to a wide range of abiotic and biotic stresses. OsHsp18.0-CI confers tolerance to salt and cadmium and interacts with viral RNA-dependent RNA polymerase (RdRp). However, the direct function of OsHsp18.0-CI in resistance against biotic stresses remains unclear in rice. ResultsHere, we report that the expression of OsHsp18.0-CI was up-regulated upon inoculation with RS105, a strain of Xanthomonas oryzae pv. oryzicola (Xoc) that causes bacterial leaf streak in rice. In comparison with wild-type, OsHsp18.0-CI overexpression (OE) lines exhibited enhanced resistance to RS105, whereas repression lines exhibited compromised resistance to RS105. In addition, the transcriptional profiles of wild type and OE lines were compared with and without inoculation with RS105. After inoculation with RS105, most of the genes with up-regulated expression were commonly stimulated in the wild type and OE lines, with stronger induction in the OE lines than in wild type. Conclusion
Our study reveals that OsHsp18.0-CI positively regulates resistance to Xoc by mediating an enhanced version of the basal defense response in rice.
... oryzae pv. oryzicola AvrRxo1 induce HR on their respective nonhost plants (Arnold et al. 2001;Kobayashi et al. 1989;Liu et al. 2014;Zhao et al. 2004b). Similarly, Bremia lactucae effector BLG01 carrying a GKLR variant of the RXLR translocation motif induces HR in a backcross inbred line of nonhost Lactuca saligna (Jeuken and Lindhout. ...
Nonhost resistance, a resistance of plant species against all nonadapted pathogens, is considered the most durable and efficient immune system of plants but yet remains elusive. The underlying mechanism of nonhost resistance has been investigated at multiple levels of plant defense for several decades. In this review, we have comprehensively surveyed the latest literature on nonhost resistance in terms of preinvasion, metabolic defense, pattern-triggered immunity, effector-triggered immunity, defense signaling, and possible application in crop protection. Overall, we summarize the current understanding of nonhost resistance mechanisms. Pre- and postinvasion is not much deviated from the knowledge on host resistance, except for a few specific cases. Further insights on the roles of the pattern recognition receptor gene family, multiple interactions between effectors from nonadapted pathogen and plant factors, and plant secondary metabolites in host range determination could expand our knowledge on nonhost resistance and provide efficient tools for future crop protection using combinational biotechnology approaches.
[Formula: see text] Copyright © 2017 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .
... AvrRxo1 is a type III effector that is highly conserved in various Asian X. oryzae pv. oryzicola strains (20,21). It was originally identified as a gene product of this particular pathogen that elicits a non-host HR in maize lines harboring the Rxo1 resistance gene (20). ...
... Hence, AvrRxo1 most likely constitutes a virulence factor that elicits ETS, and the rice Rxo1 homolog does not confer immunity (22). The role of AvrRxo1 as a virulence factor is further supported by the finding that it is toxic when expressed in tobacco and yeast cells (20,21,23). Furthermore, when ectopically expressed in Escherichia coli, AvrRxo1 was shown to inhibit cell growth, a phenotype that could be suppressed by co-expression of AvrRxo2 (19). ...
... AvrRxo1 Shows Phosphotransferase Activity-AvrRxo1 from X. oryzae pv. oryzicola is a multidomain protein consisting of a central potential kinase domain and an N-terminal domain that has been suggested to contain a thiol protease active site (20,21). Whereas the kinase domain is conserved among AvrRxo1 homologs from different plant pathogens (Fig. 1), the N-terminal region is highly divergent, and the potential thiol protease active site is only found in a few Xanthomonas strains. ...
An arsenal of effector proteins is injected by bacterial pathogens into the host cell or its vicinity to increase virulence. The commonly used top-down approaches inferring the toxic mechanism of individual effector proteins from the host's phenotype are often impeded by multiple targets of different effectors as well as by their pleiotropic effects. Here we describe our bottom-up approach, showing that the bacterial type III effector AvrRxo1 of plant pathogens is an authentic phosphotransferase that produces two novel metabolites by phosphorylating nicotinamide / nicotinic acid adenine dinucleotide at the adenosine 3'-hydroxyl group. Both products of AvrRxo1, 3'-NADP and 3'-NAADP, are substantially different from the ubiquitous co-enzyme 2'-NADP and the calcium mobilizer 2'-NAADP. Interestingly, 3'-NADP and 3'-NAADP have previously been used as inhibitors or signaling molecules but were regarded as "artificial" compounds so far. Our findings now necessitate a shift in thinking about the biological importance of 3'-phosphorylated NAD derivatives.
... The other HKG (gmc, lepA, trpB, and phaC) were monomorphic or noninformative (data not shown). In addition to the three HKG, a putative T3S effector gene (Aave_1548) (Eckshtain-Levi et al. 2014) was included, as well as Aave_3810 (a luxR homolog) and Aave_3062 (avrRxo1) (Johnson and Walcott 2013;Liu et al. 2014). These gene designations are according to the AAC00-1 annotation. ...
Bacterial fruit blotch (BFB), caused by the seedborne bacterium Acidovorax citrulli, is an economically important threat to cucurbitaceous crops worldwide. Since the first report of BFB in Brazil in 1990, outbreaks have occurred sporadically on watermelon, and more frequently on melon, resulting in significant yield losses. At present, the genetic diversity and the population structure of A. citrulli strains in Brazil remain unclear. A collection of 74 A. citrulli strains isolated from naturally infected fruits of different hosts in Brazil between 2000 and 2014 and 18 A. citrulli reference strains from other countries were compared by pulsed-field gel electrophoresis (PFGE), multilocus sequence analysis (MLSA) of housekeeping and virulence-associated genes and pathogenicity tests on different cucurbit seedling hosts. The Brazilian population was comprised predominantly of group I strains (98%), regardless of the year of isolation, geographical region or host. Whole genome restriction digestion and PFGE analysis revealed that three unique and previously unreported A. citrulli haplotypes (assigned as haplotypes B22, B23 and B24) occurred in Brazil. The greatest diversity of A. citrulli (4 haplotypes) was found among strains collected from the Northeastern region of Brazil, which accounts for more than 90% of the country`s melon production. MLSA clearly distinguished A. citrulli strains into two well supported clades, in agreement with observations based on PFGE analysis. Five Brazilian A. citrulli strains, representing different group I haplotypes, were moderately aggressive on watermelon seedlings compared to four group II strains that were highly aggressive. In contrast, no significant differences in BFB severity were observed between group I and II A. citrulli strains on melon and squash seedlings. Finally, we observed a differential effect of temperature on in vitro growth of representative group I and II A. citrulli haplotypes. Specifically, out of 18 group II strains tested, all grew at 40°C and 41°C. On the other hand, only three group I strains [haplotypes B8 (P), B3 (K) and B15] out of 15 grew at 40°C. Three strains representing haplotype B8 (P) were the only group I strains that grew at 41°C. These results contribute to a better understanding of the genetic diversity of A. citrulli associated with BFB outbreaks in Brazil, and reinforce the efficiency of MLSA and PFGE analysis for assessing population structure. This study also provides the first evidence to suggest that temperature might be a driver in the ecological adaptation of A. citrulli populations.
