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1.
Annu Rev Phytopathol ; 57: 505-529, 2019 Aug 25.
Artículo en Inglés | MEDLINE | ID: mdl-31470772

RESUMEN

As primary producers, plants are under constant pressure to defend themselves against potentially deadly pathogens and herbivores. In this review, we describe short- and long-term strategies that enable plants to cope with these stresses. Apart from internal immunological strategies that involve physiological and (epi)genetic modifications at the cellular level, plants also employ external strategies that rely on recruitment of beneficial organisms. We discuss these strategies along a gradient of increasing timescales, ranging from rapid immune responses that are initiated within seconds to (epi)genetic adaptations that occur over multiple plant generations. We cover the latest insights into the mechanistic and evolutionary underpinnings of these strategies and present explanatory models. Finally, we discuss how knowledge from short-lived model species can be translated to economically and ecologically important perennials to exploit adaptive plant strategies and mitigate future impacts of pests and diseases in an increasingly interconnected and changing world.

2.
Plant Cell Environ ; 42(8): 2411-2421, 2019 Aug.
Artículo en Inglés | MEDLINE | ID: mdl-31042812

RESUMEN

Many plant pathogens gain entry to their host via stomata. On sensing attack, plants close these pores to restrict pathogen entry. Here, we show that plants exhibit a second longer term stomatal response to pathogens. Following infection, the subsequent development of leaves is altered via a systemic signal. This reduces the density of stomata formed, thus providing fewer entry points for pathogens on new leaves. Arabidopsis thaliana leaves produced after infection by a bacterial pathogen that infects through the stomata (Pseudomonas syringae) developed larger epidermal pavement cells and stomata and consequently had up to 20% reductions in stomatal density. The bacterial peptide flg22 or the phytohormone salicylic acid induced similar systemic reductions in stomatal density suggesting that they might mediate this effect. In addition, flagellin receptors, salicylic acid accumulation, and the lipid transfer protein AZI1 were all required for this developmental response. Furthermore, manipulation of stomatal density affected the level of bacterial colonization, and plants with reduced stomatal density showed slower disease progression. We propose that following infection, development of new leaves is altered by a signalling pathway with some commonalities to systemic acquired resistance. This acts to reduce the potential for future infection by providing fewer stomatal openings.

3.
ISME J ; 13(7): 1647-1658, 2019 07.
Artículo en Inglés | MEDLINE | ID: mdl-30796337

RESUMEN

The rhizobiome is an important regulator of plant growth and health. Plants shape their rhizobiome communities through production and release of primary and secondary root metabolites. Benzoxazinoids (BXs) are common tryptophan-derived secondary metabolites in grasses that regulate belowground and aboveground biotic interactions. In addition to their biocidal activity, BXs can regulate plant-biotic interactions as semiochemicals or within-plant defence signals. However, the full extent and mechanisms by which BXs shape the root-associated microbiome has remained largely unexplored. Here, we have taken a global approach to examine the regulatory activity of BXs on the maize root metabolome and associated bacterial and fungal communities. Using untargeted mass spectrometry analysis in combination with prokaryotic and fungal amplicon sequencing, we compared the impacts of three genetic mutations in different steps in the BX pathway. We show that BXs regulate global root metabolism and concurrently influence the rhizobiome in a root type-dependent manner. Correlation analysis between BX-controlled root metabolites and bacterial taxa suggested a dominant role for BX-dependent metabolites, particularly flavonoids, in constraining a range of soil microbial taxa, while stimulating methylophilic bacteria. Our study supports a multilateral model by which BXs control root-microbe interactions via a global regulatory function in root secondary metabolism.

4.
Elife ; 82019 Jan 04.
Artículo en Inglés | MEDLINE | ID: mdl-30608232

RESUMEN

Variation in DNA methylation enables plants to inherit traits independently of changes to DNA sequence. Here, we have screened an Arabidopsis population of epigenetic recombinant inbred lines (epiRILs) for resistance against Hyaloperonospora arabidopsidis (Hpa). These lines share the same genetic background, but show variation in heritable patterns of DNA methylation. We identified four epigenetic quantitative trait loci (epiQTLs) that provide quantitative resistance without reducing plant growth or resistance to other (a)biotic stresses. Phenotypic characterisation and RNA-sequencing analysis revealed that Hpa-resistant epiRILs are primed to activate defence responses at the relatively early stages of infection. Collectively, our results show that hypomethylation at selected pericentromeric regions is sufficient to provide quantitative disease resistance, which is associated with genome-wide priming of defence-related genes. Based on comparisons of global gene expression and DNA methylation between the wild-type and resistant epiRILs, we discuss mechanisms by which the pericentromeric epiQTLs could regulate the defence-related transcriptome.

5.
Front Plant Sci ; 9: 1493, 2018.
Artículo en Inglés | MEDLINE | ID: mdl-30405655

RESUMEN

Concerns over rising atmospheric CO2 concentrations have led to growing interest in the effects of global change on plant-microbe interactions. As a primary substrate of plant metabolism, atmospheric CO2 influences below-ground carbon allocation and root exudation chemistry, potentially affecting rhizosphere interactions with beneficial soil microbes. In this study, we have examined the effects of different atmospheric CO2 concentrations on Arabidopsis rhizosphere colonization by the rhizobacterial strain Pseudomonas simiae WCS417 and the saprophytic strain Pseudomonas putida KT2440. Rhizosphere colonization by saprophytic KT2440 was not influenced by sub-ambient (200 ppm) and elevated (1,200 ppm) concentrations of CO2, irrespective of the carbon (C) and nitrogen (N) content of the soil. Conversely, rhizosphere colonization by WCS417 in soil with relatively low C and N content increased from sub-ambient to elevated CO2. Examination of plant responses to WCS417 revealed that plant growth and systemic resistance varied according to atmospheric CO2 concentration and soil-type, ranging from growth promotion with induced susceptibility at sub-ambient CO2, to growth repression with induced resistance at elevated CO2. Collectively, our results demonstrate that the interaction between atmospheric CO2 and soil nutritional status has a profound impact on plant responses to rhizobacteria. We conclude that predictions about plant performance under past and future climate scenarios depend on interactive plant responses to soil nutritional status and rhizobacteria.

6.
Sci Rep ; 8(1): 14761, 2018 Oct 03.
Artículo en Inglés | MEDLINE | ID: mdl-30283021

RESUMEN

Progeny of heavily diseased plants develop transgenerational acquired resistance (TAR). In Arabidopsis, TAR can be transmitted over one stress-free generation. Although DNA methylation has been implicated in the regulation of TAR, the relationship between TAR and global DNA methylation remains unknown. Here, we characterised the methylome of TAR-expressing Arabidopsis at different generations after disease exposure. Global clustering of cytosine methylation revealed TAR-related patterns in the F3 generation, but not in the F1 generation. The majority of differentially methylated positions (DMPs) occurred at CG context in gene bodies. TAR in F3 progeny after one initial generation of disease, followed by two stress-free generations, was lower than TAR in F3 progeny after three successive generations of disease. This difference in TAR effectiveness was proportional to the intensity of differential methylation at a sub-set of cytosine positions. Comparison of TAR-related DMPs with previously characterised cytosine methylation in mutation accumulation lines revealed that ancestral disease stress preferentially acts on methylation-labile cytosine positions, but also extends to methylation-stable positions. Thus, the TAR-related impact of ancestral disease extends beyond stochastic variation in DNA methylation. Our study has shown that the Arabidopsis epigenome responds globally to disease in previous generations and we discuss its contribution to TAR.

7.
Nat Plants ; 4(6): 392, 2018 Jun.
Artículo en Inglés | MEDLINE | ID: mdl-29802316

RESUMEN

In the version of this Perspective originally published, 'acidification' was incorrectly spelt as 'adification' in Fig. 4. This has now been corrected.

8.
Nat Plants ; 4(3): 138-147, 2018 Mar.
Artículo en Inglés | MEDLINE | ID: mdl-29459727

RESUMEN

The magnitude of future climate change could be moderated by immediately reducing the amount of CO2 entering the atmosphere as a result of energy generation and by adopting strategies that actively remove CO2 from it. Biogeochemical improvement of soils by adding crushed, fast-reacting silicate rocks to croplands is one such CO2-removal strategy. This approach has the potential to improve crop production, increase protection from pests and diseases, and restore soil fertility and structure. Managed croplands worldwide are already equipped for frequent rock dust additions to soils, making rapid adoption at scale feasible, and the potential benefits could generate financial incentives for widespread adoption in the agricultural sector. However, there are still obstacles to be surmounted. Audited field-scale assessments of the efficacy of CO2 capture are urgently required together with detailed environmental monitoring. A cost-effective way to meet the rock requirements for CO2 removal must be found, possibly involving the recycling of silicate waste materials. Finally, issues of public perception, trust and acceptance must also be addressed.

9.
New Phytol ; 218(3): 1205-1216, 2018 May.
Artículo en Inglés | MEDLINE | ID: mdl-29465773

RESUMEN

ß-Aminobutyric acid (BABA) induces broad-spectrum disease resistance, but also represses plant growth, which has limited its exploitation in crop protection. BABA perception relies on binding to the aspartyl-tRNA synthetase (AspRS) IBI1, which primes the enzyme for secondary defense activity. This study aimed to identify structural BABA analogues that induce resistance without stunting plant growth. Using site-directed mutagenesis, we demonstrate that the (l)-aspartic acid-binding domain of IBI1 is critical for BABA perception. Based on interaction models of this domain, we screened a small library of structural BABA analogues for growth repression and induced resistance against biotrophic Hyaloperonospora arabidopsidis (Hpa). A range of resistance-inducing compounds were identified, of which (R)-ß-homoserine (RBH) was the most effective. Surprisingly, RBH acted through different pathways than BABA. RBH-induced resistance (RBH-IR) against Hpa functioned independently of salicylic acid, partially relied on camalexin, and was associated with augmented cell wall defense. RBH-IR against necrotrophic Plectosphaerella cucumerina acted via priming of ethylene and jasmonic acid defenses. RBH-IR was also effective in tomato against Botrytis cinerea. Metabolic profiling revealed that RBH, unlike BABA, does not majorly affect plant metabolism. RBH primes distinct defense pathways against biotrophic and necrotrophic pathogens without stunting plant growth, signifying strong potential for exploitation in crop protection.

10.
New Phytol ; 218(2): 752-761, 2018 Apr.
Artículo en Inglés | MEDLINE | ID: mdl-29424932

RESUMEN

The impacts of rising atmospheric CO2 concentrations on plant disease have received increasing attention, but with little consensus emerging on the direct mechanisms by which CO2 shapes plant immunity. Furthermore, the impact of sub-ambient CO2 concentrations, which plants have experienced repeatedly over the past 800 000 yr, has been largely overlooked. A combination of gene expression analysis, phenotypic characterisation of mutants and mass spectrometry-based metabolic profiling was used to determine development-independent effects of sub-ambient CO2 (saCO2 ) and elevated CO2 (eCO2 ) on Arabidopsis immunity. Resistance to the necrotrophic Plectosphaerella cucumerina (Pc) was repressed at saCO2 and enhanced at eCO2 . This CO2 -dependent resistance was associated with priming of jasmonic acid (JA)-dependent gene expression and required intact JA biosynthesis and signalling. Resistance to the biotrophic oomycete Hyaloperonospora arabidopsidis (Hpa) increased at both eCO2 and saCO2 . Although eCO2 primed salicylic acid (SA)-dependent gene expression, mutations affecting SA signalling only partially suppressed Hpa resistance at eCO2 , suggesting additional mechanisms are involved. Induced production of intracellular reactive oxygen species (ROS) at saCO2 corresponded to a loss of resistance in glycolate oxidase mutants and increased transcription of the peroxisomal catalase gene CAT2, unveiling a mechanism by which photorespiration-derived ROS determined Hpa resistance at saCO2 . By separating indirect developmental impacts from direct immunological effects, we uncover distinct mechanisms by which CO2 shapes plant immunity and discuss their evolutionary significance.

11.
Sci Rep ; 7(1): 16409, 2017 Nov 27.
Artículo en Inglés | MEDLINE | ID: mdl-29180695

RESUMEN

Belowground interactions between plant roots, mycorrhizal fungi and plant growth-promoting rhizobacteria (PGPR) can improve plant health via enhanced nutrient acquisition and priming of the plant immune system. Two wheat cultivars differing in their ability to form mycorrhiza were (co)inoculated with the mycorrhizal fungus Rhizophagus irregularis and the rhizobacterial strain Pseudomonas putida KT2440. The cultivar with high mycorrhizal compatibility supported higher levels of rhizobacterial colonization than the low compatibility cultivar. Those levels were augmented by mycorrhizal infection. Conversely, rhizobacterial colonization of the low compatibility cultivar was reduced by mycorrhizal arbuscule formation. Single inoculations with R. irregularis or P. putida had differential growth effects on both cultivars. Furthermore, while both cultivars developed systemic priming of chitosan-induced callose after single inoculations with R. irregularis or P. putida, only the cultivar with high mycorrhizal compatibility showed a synergistic increase in callose responsiveness following co-inoculation with both microbes. Our results show that multilateral interactions between roots, mycorrhizal fungi and PGPR can have synergistic effects on growth and systemic priming of wheat.

12.
Plant J ; 92(1): 147-162, 2017 Oct.
Artículo en Inglés | MEDLINE | ID: mdl-28742258

RESUMEN

Rhizosphere chemistry is the sum of root exudation chemicals, their breakdown products and the microbial products of soil-derived chemicals. To date, most studies about root exudation chemistry are based on sterile cultivation systems, which limits the discovery of microbial breakdown products that act as semiochemicals and shape microbial rhizosphere communities. Here, we present a method for untargeted metabolic profiling of non-sterile rhizosphere soil. We have developed an experimental growth system that enables the collection and analysis of rhizosphere chemicals from different plant species. High-throughput sequencing of 16SrRNA genes demonstrated that plants in the growth system support a microbial rhizosphere effect. To collect a range of (a)polar chemicals from the system, we developed extraction methods that do not cause detectable damage to root cells or soil-inhabiting microbes, thus preventing contamination with cellular metabolites. Untargeted metabolite profiling by UPLC-Q-TOF mass spectrometry, followed by uni- and multivariate statistical analyses, identified a wide range of secondary metabolites that are enriched in plant-containing soil, compared with control soil without roots. We show that the method is suitable for profiling the rhizosphere chemistry of Zea mays (maize) in agricultural soil, thereby demonstrating the applicability to different plant-soil combinations. Our study provides a robust method for the comprehensive metabolite profiling of non-sterile rhizosphere soil, which represents a technical advance towards the establishment of causal relationships between the chemistry and microbial composition of the rhizosphere.


Asunto(s)
Arabidopsis/metabolismo , Metabolómica/métodos , Microbiota , Exudados de Plantas/análisis , Zea mays/metabolismo , Arabidopsis/química , Raíces de Plantas/química , Raíces de Plantas/metabolismo , Rizosfera , Suelo/química , Zea mays/química
13.
Plant Physiol ; 172(3): 1465-1479, 2016 11.
Artículo en Inglés | MEDLINE | ID: mdl-27621425

RESUMEN

Pyridine nucleotides, such as NAD, are crucial redox carriers and have emerged as important signaling molecules in stress responses. Previously, we have demonstrated in Arabidopsis (Arabidopsis thaliana) that the inducible NAD-overproducing nadC lines are more resistant to an avirulent strain of Pseudomonas syringae pv tomato (Pst-AvrRpm1), which was associated with salicylic acid-dependent defense. Here, we have further characterized the NAD-dependent immune response in Arabidopsis. Quinolinate-induced stimulation of intracellular NAD in transgenic nadC plants enhanced resistance against a diverse range of (a)virulent pathogens, including Pst-AvrRpt2, Dickeya dadantii, and Botrytis cinerea Characterization of the redox status demonstrated that elevated NAD levels induce reactive oxygen species (ROS) production and the expression of redox marker genes of the cytosol and mitochondrion. Using pharmacological and reverse genetics approaches, we show that NAD-induced ROS production functions independently of NADPH oxidase activity and light metabolism but depends on mitochondrial respiration, which was increased at higher NAD. We further demonstrate that NAD primes pathogen-induced callose deposition and cell death. Mass spectrometry analysis reveals that NAD simultaneously induces different defense hormones and that the NAD-induced metabolic profiles are similar to those of defense-expressing plants after treatment with pathogen-associated molecular patterns. We thus conclude that NAD triggers metabolic profiles rather similar to that of pathogen-associated molecular patterns and discuss how signaling cross talk between defense hormones, ROS, and NAD explains the observed resistance to pathogens.


Asunto(s)
Arabidopsis/inmunología , NAD/metabolismo , Inmunidad de la Planta , Arabidopsis/microbiología , Arabidopsis/efectos de la radiación , Muerte Celular/efectos de la radiación , Análisis Discriminante , Resistencia a la Enfermedad/inmunología , Espacio Intracelular/metabolismo , Análisis de los Mínimos Cuadrados , Luz , Mitocondrias/metabolismo , Mitocondrias/efectos de la radiación , Modelos Biológicos , NADPH Oxidasas/metabolismo , Nucleótidos/metabolismo , Estrés Oxidativo/efectos de la radiación , Patrón Molecular Asociado a Patógenos/metabolismo , Fenotipo , Enfermedades de las Plantas/inmunología , Enfermedades de las Plantas/microbiología , Reguladores del Crecimiento de las Plantas/metabolismo , Inmunidad de la Planta/efectos de la radiación , Hojas de la Planta/citología , Hojas de la Planta/metabolismo , Hojas de la Planta/efectos de la radiación , Piridinas/metabolismo , Especies Reactivas de Oxígeno/metabolismo , Estallido Respiratorio/efectos de la radiación , Ácido Salicílico/metabolismo
14.
Trends Plant Sci ; 21(10): 818-822, 2016 10.
Artículo en Inglés | MEDLINE | ID: mdl-27507609

RESUMEN

Defense priming conditions diverse plant species for the superinduction of defense, often resulting in enhanced pest and disease resistance and abiotic stress tolerance. Here, we propose a guideline that might assist the plant research community in a consistent assessment of defense priming in plants.


Asunto(s)
Resistencia a la Enfermedad/fisiología , Fenómenos Fisiológicos de las Plantas , Epigénesis Genética/fisiología , Plantas/metabolismo , Estrés Fisiológico/fisiología
15.
Plant J ; 88(3): 361-374, 2016 11.
Artículo en Inglés | MEDLINE | ID: mdl-27341062

RESUMEN

DNA methylation is antagonistically controlled by DNA methyltransferases and DNA demethylases. The level of DNA methylation controls plant gene expression on a global level. We have examined impacts of global changes in DNA methylation on the Arabidopsis immune system. A range of hypo-methylated mutants displayed enhanced resistance to the biotrophic pathogen Hyaloperonospora arabidopsidis (Hpa), whereas two hyper-methylated mutants were more susceptible to this pathogen. Subsequent characterization of the hypo-methylated nrpe1 mutant, which is impaired in RNA-directed DNA methylation, and the hyper-methylated ros1 mutant, which is affected in DNA demethylation, revealed that their opposite resistance phenotypes are associated with changes in cell wall defence and salicylic acid (SA)-dependent gene expression. Against infection by the necrotrophic pathogen Plectosphaerella cucumerina, nrpe1 showed enhanced susceptibility, which was associated with repressed sensitivity of jasmonic acid (JA)-inducible gene expression. Conversely, ros1 displayed enhanced resistance to necrotrophic pathogens, which was not associated with increased responsiveness of JA-inducible gene expression. Although nrpe1 and ros1 were unaffected in systemic acquired resistance to Hpa, they failed to develop transgenerational acquired resistance against this pathogen. Global transcriptome analysis of nrpe1 and ros1 at multiple time-points after Hpa infection revealed that 49% of the pathogenesis-related transcriptome is influenced by NRPE1- and ROS1-controlled DNA methylation. Of the 166 defence-related genes displaying augmented induction in nrpe1 and repressed induction in ros1, only 25 genes were associated with a nearby transposable element and NRPE1- and/or ROS1-controlled DNA methylation. Accordingly, we propose that the majority of NRPE1- and ROS1-dependent defence genes are regulated in trans by DNA methylation.


Asunto(s)
Proteínas de Arabidopsis/metabolismo , Arabidopsis/metabolismo , Arabidopsis/genética , Arabidopsis/inmunología , Proteínas de Arabidopsis/genética , Metilación de ADN/genética , Metilación de ADN/fisiología , Regulación de la Expresión Génica de las Plantas/genética , Regulación de la Expresión Génica de las Plantas/inmunología , Enfermedades de las Plantas/genética , Enfermedades de las Plantas/inmunología , Inmunidad de la Planta/genética , Inmunidad de la Planta/inmunología
16.
Plant Physiol ; 170(4): 2325-39, 2016 04.
Artículo en Inglés | MEDLINE | ID: mdl-26842622

RESUMEN

Necrotrophic and biotrophic pathogens are resisted by different plant defenses. While necrotrophic pathogens are sensitive to jasmonic acid (JA)-dependent resistance, biotrophic pathogens are resisted by salicylic acid (SA)- and reactive oxygen species (ROS)-dependent resistance. Although many pathogens switch from biotrophy to necrotrophy during infection, little is known about the signals triggering this transition. This study is based on the observation that the early colonization pattern and symptom development by the ascomycete pathogen Plectosphaerella cucumerina (P. cucumerina) vary between inoculation methods. Using the Arabidopsis (Arabidopsis thaliana) defense response as a proxy for infection strategy, we examined whether P. cucumerina alternates between hemibiotrophic and necrotrophic lifestyles, depending on initial spore density and distribution on the leaf surface. Untargeted metabolome analysis revealed profound differences in metabolic defense signatures upon different inoculation methods. Quantification of JA and SA, marker gene expression, and cell death confirmed that infection from high spore densities activates JA-dependent defenses with excessive cell death, while infection from low spore densities induces SA-dependent defenses with lower levels of cell death. Phenotyping of Arabidopsis mutants in JA, SA, and ROS signaling confirmed that P. cucumerina is differentially resisted by JA- and SA/ROS-dependent defenses, depending on initial spore density and distribution on the leaf. Furthermore, in situ staining for early callose deposition at the infection sites revealed that necrotrophy by P. cucumerina is associated with elevated host defense. We conclude that P. cucumerina adapts to early-acting plant defenses by switching from a hemibiotrophic to a necrotrophic infection program, thereby gaining an advantage of immunity-related cell death in the host.


Asunto(s)
Arabidopsis/microbiología , Ascomicetos/patogenicidad , Enfermedades de las Plantas/microbiología , Esporas Fúngicas/fisiología , Arabidopsis/metabolismo , Ascomicetos/efectos de los fármacos , Muerte Celular/efectos de los fármacos , Ciclopentanos/farmacología , Resistencia a la Enfermedad/efectos de los fármacos , Redes y Vías Metabólicas , Metaboloma/efectos de los fármacos , Metabolómica , Modelos Biológicos , Oxilipinas/farmacología , Fenotipo , Hojas de la Planta/efectos de los fármacos , Hojas de la Planta/inmunología , Hojas de la Planta/metabolismo , Hojas de la Planta/microbiología , Especies Reactivas de Oxígeno/metabolismo , Ácido Salicílico/farmacología , Esporas Fúngicas/efectos de los fármacos , Tiadiazoles/farmacología
17.
Nat Commun ; 6: 6273, 2015 Feb 16.
Artículo en Inglés | MEDLINE | ID: mdl-25683900

RESUMEN

Herbivore-induced volatile organic compounds prime non-attacked plant tissues to respond more strongly to subsequent attacks. However, the key volatiles that trigger this primed state remain largely unidentified. In maize, the release of the aromatic compound indole is herbivore-specific and occurs earlier than other induced responses. We therefore hypothesized that indole may be involved in airborne priming. Using indole-deficient mutants and synthetic indole dispensers, we show that herbivore-induced indole enhances the induction of defensive volatiles in neighbouring maize plants in a species-specific manner. Furthermore, the release of indole is essential for priming of mono- and homoterpenes in systemic leaves of attacked plants. Indole exposure markedly increases the herbivore-induced production of the stress hormones jasmonate-isoleucine conjugate and abscisic acid, which represents a likely mechanism for indole-dependent priming. These results demonstrate that indole functions as a rapid and potent aerial priming agent that prepares systemic tissues and neighbouring plants for incoming attacks.


Asunto(s)
Herbivoria/efectos de los fármacos , Indoles/farmacología , Compuestos Orgánicos Volátiles/farmacología , Zea mays/fisiología , Ácido Abscísico/biosíntesis , Animales , Ciclopentanos/metabolismo , Mutación/genética , Oxilipinas/metabolismo , Reguladores del Crecimiento de las Plantas/farmacología , Terpenos/farmacología , Zea mays/efectos de los fármacos
19.
Front Plant Sci ; 5: 184, 2014.
Artículo en Inglés | MEDLINE | ID: mdl-24847342

RESUMEN

Priming of defense increases the responsiveness of the plant immune system and can provide broad-spectrum protection against disease. Recent evidence suggests that priming of defense can be inherited epigenetically to following generations. However, the mechanisms of long-lasting defense priming within one generation remains poorly understood. Here, we have investigated the mechanistic basis of long-lasting induced resistance after treatment with ß -aminobutyric acid (BABA), an agent that mimics biologically induced resistance phenomena. BABA-induced resistance (BABA-IR) is based on priming of salicylic acid (SA)-dependent and SA-independent defenses. BABA-IR could be detected up to 28 days after treatment of wild-type Arabidopsis. This long-lasting component of the induced resistance response requires the regulatory protein NPR1 and is associated with priming of SA-inducible genes. In contrast, NPR1-independent resistance by BABA was transient and had disappeared by 14 days after treatment. Chromatin immunoprecipitation (ChIP) assays revealed no increased acetylation of histone H3K9 at promoters regions of priming-responsive genes, indicating that this post-translational histone modification is not critical for long-term transcriptional priming. Interestingly, the kyp-6 mutant, which is affected in methyltransferase activity of H3K9, was blocked in long-lasting BABA-IR, indicating a critical requirement of this post-translational histone modification in long-lasting BABA-IR. Considering that KYP suppresses gene transcription through methylation of H3K9 and CpHpG DNA methylation, we propose that KYP enables long-term defense gene priming by silencing suppressor genes of SA/NPR1-dependent genes.

20.
Nat Chem Biol ; 10(6): 450-6, 2014 Jun.
Artículo en Inglés | MEDLINE | ID: mdl-24776930

RESUMEN

Specific chemicals can prime the plant immune system for augmented defense. ß-aminobutyric acid (BABA) is a priming agent that provides broad-spectrum disease protection. However, BABA also suppresses plant growth when applied in high doses, which has hampered its application as a crop defense activator. Here we describe a mutant of Arabidopsis thaliana that is impaired in BABA-induced disease immunity (ibi1) but is hypersensitive to BABA-induced growth repression. IBI1 encodes an aspartyl-tRNA synthetase. Enantiomer-specific binding of the R enantiomer of BABA to IBI1 primed the protein for noncanonical defense signaling in the cytoplasm after pathogen attack. This priming was associated with aspartic acid accumulation and tRNA-induced phosphorylation of translation initiation factor eIF2α. However, mutation of eIF2α-phosphorylating GCN2 kinase did not affect BABA-induced immunity but relieved BABA-induced growth repression. Hence, BABA-activated IBI1 controls plant immunity and growth via separate pathways. Our results open new opportunities to separate broad-spectrum disease resistance from the associated costs on plant growth.


Asunto(s)
Aminobutiratos/farmacología , Arabidopsis/efectos de los fármacos , Aspartato-ARNt Ligasa/genética , Aspartato-ARNt Ligasa/metabolismo , Aminobutiratos/química , Arabidopsis/enzimología , Arabidopsis/genética , Arabidopsis/crecimiento & desarrollo , Genes de Plantas , Mutación , Enfermedades de las Plantas/inmunología , Enfermedades de las Plantas/prevención & control , Inmunidad de la Planta/efectos de los fármacos , Inmunidad de la Planta/genética , Estereoisomerismo
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