Unraveling rhizobacteria- and abscisic acid-induced pathogen resistance in rice (Oryza sativa L.)

Induced disease resistance is the phenomenon by which plants exhibit a heightened level of resistance against pathogen infection after appropriate stimulation. In contrast to the relative wealth of information on inducible resistance responses in dicotyledoneous plants, our current understanding of the molecular machinery governing induced resistance in monocotyledoneous crops is still in its infancy. In light of aforementioned knowledge gap, this dissertation aimed to expand our knowledge on the mechanistic basis of biologically and chemically induced resistance in rice, the world’s most important staple food and a central model for cereal crops. The first part of this work is dedicated to the phenomenon of rhizobacteria-induced systemic resistance (ISR). Using an extensive set of bacterial mutants, we pinpoint the phenazine pigment pyocyanin as a two-faced ISR elicitor capable of inducing resistance against the blast pathogen Magnaporthe oryzae, while promoting susceptibility to the sheath blight pathogen Rhizoctonia solani. In addition, evidence is brought forward demonstrating that the ambivalent role of pyocyanin in Pseudomonas aeruginosa 7NSK2-mediated ISR is due to its ability to modulate the plant’s oxidative machinery. Aiming to further dissect the rhizobacteria-mediated ISR response, we continued exploring the bacterial traits and host immune responses underpinning ISR elicited by the P. fluorescens strain WCS374r. The cumulative results favor a model whereby WCS374r bacteria trigger ISR against M. oryzae via secretion of a pseudobactin-type siderophore, thereby sensitizing naïve leaves for potentiated expression of a salicylic acid-repressible, yet jasmonate/ethylene-dependent multifaceted defence response. The differences and similarities between WCS374r-ISR and blast resistance triggered by the salicylic acid mimic benzothiadiazole are addressed as well. In the second part of this work, attention was shifted to the role of the phytohormone abscisic acid (ABA) in modulating rice pathogen defence. We show that topical application of ABA enhances basal resistance against the brown spot-causing ascomycete Cochliobolus miyabeanus. Pursuing a multidisciplinary approach, evidence is provided supporting ABA-mediated repression of pathogen-induced ethylene signalling as a core resistance mechanism. In addition, we present a novel role for the MAPK OsMPK5 as a critical modulator of this ABA/ET crosstalk, and describe how ABA interferes with the postulated fungal manipulation of the plant

Making sense o fhormone-mediated defense networking: from rice to Arabidopsis

Phytohormones are not only essential for plant growth and development but also play central roles in triggering the plant immune signaling network. Historically, research aimed at elucidating the defense-associated role of hormones has tended to focus on the use of experimentally tractable dicot plants such as Arabidopsis thaliana. Emerging from these studies is a picture whereby complex crosstalk and induced hormonal changes mold plant health and disease, with outcomes largely dependent on the lifestyle and infection strategy of invading pathogens. However, recent studies in monocot plants are starting to provide additional important insights into the immune-regulatory roles of hormones, often revealing unique complexities. In this review, we address the latest discoveries dealing with hormone-mediated immunity in rice, one of the most important food crops and an excellent model for molecular genetic studies in monocots. Moreover, we highlight interactions between hormone signaling, rice defense and pathogen virulence, and discuss the differences and similarities with findings in Arabidopsis. Finally, we present a model for hormone defense networking in rice and describe how detailed knowledge of hormone crosstalk mechanisms can be used for engineering durable rice disease resistance

Abscisic acid promotes susceptibility to the rice leaf blight pathogen Xanthomonas oryzae pv oryzae by suppressing salicylic acid-mediated defenses

The plant hormone abscisic acid (ABA) is involved in a wide variety of plant processes, including the initiation of stress-adaptive responses to various environmental cues. Recently, ABA also emerged as a central factor in the regulation and integration of plant immune responses, although little is known about the underlying mechanisms. Aiming to advance our understanding of ABA-modulated disease resistance, we have analyzed the impact, dynamics and interrelationship of ABA and the classic defense hormone salicylic acid (SA) during progression of rice infection by the leaf blight pathogen Xanthomonas oryzae pv. oryzae (Xoo). Consistent with ABA negatively regulating resistance to Xoo, we found that exogenously administered ABA renders rice hypersusceptible to infection, whereas chemical and genetic disruption of ABA biosynthesis and signaling, respectively, led to enhanced Xoo resistance. In addition, we found successful Xoo infection to be associated with extensive reprogramming of ABA biosynthesis and response genes, suggesting that ABA functions as a virulence factor for Xoo. Interestingly, several lines of evidence indicate that this immune-suppressive effect of ABA is due at least in part to suppression of SA-mediated defenses that normally serve to limit pathogen growth. Resistance induced by the ABA biosynthesis inhibitor fluridone, however, appears to operate in a SA-independent manner and is likely due to induction of non-specific physiological stress. Collectively, our findings favor a scenario whereby virulent Xoo hijacks the rice ABA machinery to cause disease and highlight the importance of ABA and its crosstalk with SA in shaping the outcome of rice-Xoo interactions

Differential effectiveness of Serratia plymuthica IC1270-induced systemic resistance against hemibiotrophic and necrotrophic leaf pathogens in rice

<p>Abstract</p> <p>Background</p> <p>Induced resistance is a state of enhanced defensive capacity developed by a plant reacting to specific biotic or chemical stimuli. Over the years, several forms of induced resistance have been characterized, including systemic acquired resistance, which is induced upon localized infection by an avirulent necrotizing pathogen, and induced systemic resistance (ISR), which is elicited by selected strains of nonpathogenic rhizobacteria. However, contrary to the relative wealth of information on inducible defense responses in dicotyledoneous plants, our understanding of the molecular mechanisms underlying induced resistance phenomena in cereal crops is still in its infancy. Using a combined cytomolecular and pharmacological approach, we analyzed the host defense mechanisms associated with the establishment of ISR in rice by the rhizobacterium <it>Serratia plymuthica </it>IC1270.</p> <p>Results</p> <p>In a standardized soil-based assay, root treatment with IC1270 rendered foliar tissues more resistant to the hemibiotrophic pathogen <it>Magnaporthe oryzae</it>, causal agent of the devastating rice blast disease. Analysis of the cytological and biochemical alterations associated with restriction of fungal growth in IC1270-induced plants revealed that IC1270 primes rice for enhanced attacker-induced accumulation of reactive oxygen species (ROS) and autofluorescent phenolic compounds in and near epidermal cells displaying dense cytoplasmic granulation. Similar, yet more abundant, phenotypes of hypersensitively dying cells in the vicinity of fungal hyphae were evident in a gene-for-gene interaction with an avirulent <it>M. oryzae </it>strain, suggesting that IC1270-inducible ISR and R protein conditioned effector-triggered immunity (ETI) target similar defense mechanisms. Yet, this IC1270-inducible ISR response seems to act as a double-edged sword within the rice defense network as induced plants displayed an increased vulnerability to the necrotrophic pathogens <it>Rhizoctonia solani </it>and <it>Cochliobolus miyabeanus</it>. Artificial enhancement of ROS levels in inoculated leaves faithfully mimicked the opposite effects of IC1270 bacteria on aforementioned pathogens, suggesting a central role for oxidative events in the IC1270-induced resistance mechanism.</p> <p>Conclusion</p> <p>Besides identifying ROS as modulators of antagonistic defense mechanisms in rice, this work reveals the mechanistic similarities between <it>S. plymuthica</it>-mediated ISR and R protein-dictated ETI and underscores the importance of using appropriate innate defense mechanisms when breeding for broad-spectrum rice disease resistance.</p

Modulating plant primary amino acid metabolism as a necrotrophic virulence strategy : the immune-regulatory role of asparagine synthetase in Botrytis cinerea-tomato interaction

The fungal plant pathogen Botrytis cinerea is the causal agent of the “gray mold” disease on a broad range of hosts. As an archetypal necrotroph, B. cinerea has evolved multiple virulence strategies for inducing cell death in its host. Moreover, progress of B. cinerea colonization is commonly associated with induction of senescence in the host tissue, even in non-invaded regions. In a recent study, we showed that abscisic acid deficiency in the sitiens tomato mutant culminates in an anti-senescence defense mechanism which effectively contributes to resistance against B. cinerea infection. Conversely, in susceptible wild-type tomato a strong induction of senescence could be observed following B. cinerea infection. Building upon this earlier work, we here discuss the immune-regulatory role of a key senescence-associated protein, asparagine synthetase. We found that infection of wild-type tomato leads to a strong transcriptional upregulation of asparagine synthetase, followed by a severe depletion of asparagine titers. In contrast, resistant sitiens plants displayed a strong induction of asparagine throughout the course of infection. We hypothesize that rapid activation of asparagine synthetase in susceptible tomato may play a dual role in promoting Botrytis cinerea pathogenesis by providing a rich source of N for the pathogen, on the one hand, and facilitating pathogen-induced host senescence, on the other

The energy sensor OsSnRK1a confers broad-spectrum disease resistance in rice

Sucrose non-fermenting-1-related protein kinase-1 (SnRK1) belongs to a family of evolutionary conserved kinases with orthologs in all eukaryotes, ranging from yeasts (SnF1) to mammals (AMP-Activated kinase). These kinases sense energy deficits caused by nutrient limitation or stress and coordinate the required adaptations to maintain energy homeostasis and survival. In plants, SnRK1 is a global regulator of plant metabolism and is also involved in abiotic stress responses. Its role in the response to biotic stress, however, is only starting to be uncovered. Here we studied the effect of altered SnRK1a expression on growth and plant defense in rice. OsSnRK1a overexpression interfered with normal growth and development and increased resistance against both (hemi) biotrophic and necrotrophic pathogens, while OsSnRK1a silencing in RNAi lines increased susceptibility. OsSnRK1a overexpression positively affected the salicylic acid pathway and boosted the jasmonate-mediated defense response after inoculation with the blast fungus Pyricularia oryzae. Together these findings strongly suggest OsSnRK1a to be involved in plant basal immunity and favor a model whereby OsSnRK1a acts as a master switch that regulates growth-immunity trade-offs

Phytohormone-mediated interkingdom signaling shapes the outcome of rice-Xanthomonas oryzae pv. oryzae interactions

Background: Small-molecule hormones are well known to play key roles in the plant immune signaling network that is activated upon pathogen perception. In contrast, little is known about whether phytohormones also directly influence microbial virulence, similar to what has been reported in animal systems. Results: In this paper, we tested the hypothesis that hormones fulfill dual roles in plant-microbe interactions by orchestrating host immune responses, on the one hand, and modulating microbial virulence traits, on the other. Employing the rice-Xanthomonas oryzae pv. oryzae (Xoo) interaction as a model system, we show that Xoo uses the classic immune hormone salicylic acid (SA) as a trigger to activate its virulence-associated quorum sensing (QS) machinery. Despite repressing swimming motility, sodium salicylate (NaSA) induced production of the Diffusible Signal Factor (DSF) and Diffusible Factor (DF) QS signals, with resultant accumulation of xanthomonadin and extracellular polysaccharides. In contrast, abscisic acid (ABA), which favors infection by Xoo, had little impact on DF- and DSF-mediated QS, but promoted bacterial swimming via the LuxR solo protein OryR. Moreover, we found both DF and DSF to influence SA-and ABA-responsive gene expression in planta. Conclusions: Together our findings indicate that the rice SA and ABA signaling pathways cross-communicate with the Xoo DF and DSF QS systems and underscore the importance of bidirectional interkingdom signaling in molding plant-microbe interactions

Jasmonate-induced defense mechanisms in the belowground antagonistic interaction between Pythium arrhenomanes and Meloidogyne graminicola in rice

Next to their essential roles in plant growth and development, phytohormones play a central role in plant immunity against pathogens. In this study we studied the previously reported antagonism between the plant-pathogenic oomycete Pythium arrhenomanes and the root-knot nematode Meloidogyne graminicola, two root pathogens that co-occur in aerobic rice fields. In this manuscript, we investigated if the antagonism is related to imbalances in plant hormone levels, which could be involved in activation of plant defense. Hormone measurements and gene expression analyses showed that the jasmonate (JA) pathway is induced early upon P. arrhenomanes infection. Exogenous application of methyl-jasmonate (MeJA) on the plant confirmed that JA is needed for basal defense against both P. arrhenomanes and M. graminicola in rice. Whereas M. graminicola suppresses root JA levels to increase host susceptibility, Pythium inoculation boosts JA in a manner that prohibits JA repression by the nematode in double-inoculated plants. Exogenous MeJA supply phenocopied the defense-inducing capacity of Pythium against the root-knot nematode, whereas the antagonism was weakened in JA-insensitive mutants. Transcriptome analysis confirmed upregulation of JA biosynthesis and signaling genes upon P. arrhenomanes infection, and additionally revealed induction of genes involved in biosynthesis of diterpenoid phytoalexins, consistent with strong activation of the gene encoding the JA-inducible transcriptional regulator DITERPENOID PHYTOALEXIN FACTOR. Altogether, the here-reported data indicate an important role for JA-induced defense mechanisms in this antagonistic interaction. Next to that, our results provide evidence for induced expression of genes encoding ERF83, and related PR proteins, as well as auxin depletion in P. arrhenomanes infected rice roots, which potentially further contribute to the reduced nematode susceptibility seen in double-infected plants