Plants live in complex environments in which they intimately interact with a broad range of microbial pathogens with different lifestyles and infection strategies. The evolutionary arms race between plants and their attackers provided plants with a highly sophisticated defense system that, like the animal innate immune system, recognizes pathogen molecules and responds by activating specific defenses that are directed against the invader. Recent advances in plant immunity research have provided exciting new insights into the underlying defense signaling network. Diverse small-molecule hormones play pivotal roles in the regulation of this network. Their signaling pathways cross-communicate in an antagonistic or synergistic manner, providing the plant with a powerful capacity to finely regulate its immune response. Pathogens, on the other hand, can manipulate the plant's defense signaling network for their own benefit by affecting phytohormone homeostasis to antagonize the host immune response.Phytohormones are small molecules that are essential for the regulation of plant growth, development, reproduction and survival. They act as signal molecules and occur in low concentrations. Classic phytohormones are abscisic acid (ABA), auxins, cytokinins, ethylene (ET) and gibberellins, but small signaling molecules such as brassinosteroids, jasmonates (JAs) and salicylic acid (SA) are recognized as phytohormones as well 1 . Changes in hormone concentration or sensitivity, which can be triggered under biotic and abiotic stress conditions, mediate a whole range of adaptive plant responses. The importance of SA, JAs and ET as primary signals in the regulation of the plant's immune response is well established 2-6 . More recently, ABA 7,8 , auxins 9,10 , gibberellins 11 , cytokinins 12,13 and brassinosteroids 14,15 emerged as players on the battle field as well (Fig. 1). The involvement of so many plant growth regulators in plant immunity suggests that the control of plant growth, development and defense is interconnected in a complex network of cross-communicating hormone signaling pathways. The great regulatory potential of such a network may allow plants to quickly adapt to their biotic and abiotic environment and to utilize their resources in a cost-efficient manner. It is generally believed that hormone-regulated induced defense responses evolved to save energy under enemy-free conditions, as they only involve costs when defenses are activated upon pathogen or insect attack 16 . These costs arise from the allocation of resources to defense and away from plant growth and development. Trade-offs between plant growth rate and disease resistance have been well documented 16 and support the hypothesis that plant growth and defense are regulated by a network of interconnecting signaling pathways.Upon pathogen attack, the quantity, composition and timing of the phytohormonal blend produced by the plant varies among plant species and depends greatly on the lifestyle and infection strategy of the invading attacker. This 'signal s...
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Summary• Upon appropriate stimulation, plants can develop an enhanced capacity to express infection-induced cellular defense responses, a phenomenon known as the primed state. Colonization of the roots of Arabidopsis thaliana by the beneficial rhizobacterial strain Pseudomonas fluorescens WCS417r primes the leaf tissue for enhanced pathogen-and insect-induced expression of jasmonate (JA)-responsive genes, resulting in an induced systemic resistance (ISR) that is effective against different types of pathogens and insect herbivores.• Here the molecular mechanism of this rhizobacteria-induced priming response was investigated using a whole-genome transcript profiling approach.• Out of the 1879 putative methyl jasmonate (MeJA)-responsive genes, 442 genes displayed a primed expression pattern in ISR-expressing plants. Promoter analysis of ISR-primed, MeJA-responsive genes and ISR-primed, Pseudomonas syringae pv. tomato DC3000 (Pst DC3000)-responsive genes revealed over-representation of the G-box-like motif 5′-CACATG-3′. This motif is a binding site for the transcription factor MYC2, which plays a central role in JA-and abscisic acid-regulated signaling. MYC2 expression was consistently up-regulated in ISR-expressing plants. Moreover, mutants impaired in the JASMONATE-INSENSITIVE1/MYC2 gene (jin1-1 and jin1-2) were unable to mount WCS417r-ISR against Pst DC3000 and the downy mildew pathogen Hyaloperonospora parasitica.• Together, these results pinpoint MYC2 as a potential regulator in priming for enhanced JA-responsive gene expression during rhizobacteria-mediated ISR.
Colonisation of plant roots by selected beneficial Trichoderma fungi or Pseudomonas bacteria can result in the activation of a systemic defence response that is effective against a broad spectrum of pathogens. In Arabidopsis thaliana, induced systemic resistance (ISR) triggered by the rhizobacterial strain Pseudomonas fluorescens WCS417r is regulated by a jasmonic acid‐ and ethylene‐dependent defence signalling pathway. Jasmonic acid and ethylene also play a role in Trichoderma‐induced resistance. To further investigate the similarities between rhizobacteria‐ and Trichoderma‐induced resistance, we studied the response of Arabidopsis to root colonisation by Trichoderma asperellum T34. In many aspects T34‐ISR was similar to WCS417r‐ISR. First, colonisation of the roots by T34 rendered the leaves more resistant to the bacterial pathogen Pseudomonas syringae pv. tomato, the biotrophic oomycete Hyaloperonospora parasitica and the necrotrophic fungus Plectosphaerella cucumerina. Second, treatment of the roots with T34 primed the leaf tissue for enhanced jasmonic acid‐responsive gene expression and increased formation of callose‐containing papillae upon pathogen attack. Third, T34‐ISR was fully expressed in the salicylic acid impaired mutant sid2, but blocked in the defence regulatory mutant npr1. Finally, we show that the root‐specific transcription factor MYB72, which is essential in early signalling steps of WCS417r‐ISR, is also required for T34‐ISR. Together, these results indicate that the defence pathways triggered by beneficial Trichoderma and Pseudomonas spp. strains are highly similar and that MYB72 functions as an early node of convergence in the signalling pathways that are induced by these different beneficial microorganisms.
Colonization of Arabidopsis thaliana roots by nonpathogenic Pseudomonas fluorescens WCS417r bacteria triggers a jasmonate/ ethylene-dependent induced systemic resistance (ISR) that is effective against a broad range of pathogens. Microarray analysis revealed that the R2R3-MYB-like transcription factor gene MYB72 is specifically activated in the roots upon colonization by WCS417r. Here, we show that T-DNA knockout mutants myb72-1 and myb72-2 are incapable of mounting ISR against the pathogens Pseudomonas syringae pv tomato, Hyaloperonospora parasitica, Alternaria brassicicola, and Botrytis cinerea, indicating that MYB72 is essential to establish broad-spectrum ISR. Overexpression of MYB72 did not result in enhanced resistance against any of the pathogens tested, demonstrating that MYB72 is not sufficient for the expression of ISR. Yeast two-hybrid analysis revealed that MYB72 physically interacts in vitro with the ETHYLENE INSENSITIVE3 (EIN3)-LIKE3 transcription factor EIL3, linking MYB72 function to the ethylene response pathway. However, WCS417r activated MYB72 in ISR-deficient, ethyleneinsensitive ein2-1 plants. Moreover, exogenous application of the ethylene precursor 1-aminocyclopropane-1-carboxylate induced wild-type levels of resistance in myb72-1, suggesting that MYB72 acts upstream of ethylene in the ISR pathway. Collectively, this study identified the transcriptional regulator MYB72 as a novel ISR signaling component that is required in the roots during early signaling steps of rhizobacteria-mediated ISR.
Cadmium (Cd) is a widespread, naturally occurring element present in soil, rock, water, plants and animals. Cd is a non-essential element for plants and is toxic at higher concentrations. Transcript profiles of roots of Arabidopsis thaliana (Arabidopsis) and Thlaspi caerulescens plants exposed to Cd and zinc (Zn) are examined, with the main aim to determine the differences in gene expression between the Cd-tolerant Zn-hyperaccumulator T. caerulescens and the Cd-sensitive non-accumulator Arabidopsis. This comparative transcriptional analysis emphasized the role of genes involved in lignin, glutathione and sulphate metabolism. Furthermore the transcription factors MYB72 and bHLH100 were studied for their involvement in metal homeostasis, as they showed an altered expression after exposure to Cd. The Arabidopsis myb72 knockout mutant was more sensitive to excess Zn or iron (Fe) deficiency than wild type, while Arabidopsis transformants overexpressing bHLH100 showed increased tolerance to high Zn and nickel (Ni) compared to wild-type plants, confirming their role in metal homeostasis in Arabidopsis.
Summary• Pseudomonas fluorescens WCS417r bacteria and β-aminobutyric acid can induce disease resistance in Arabidopsis, which is based on priming of defence.• In this study, we examined the differences and similarities of WCS417r-and β-aminobutyric acid-induced priming.• Both WCS417r and β-aminobutyric acid prime for enhanced deposition of callose-rich papillae after infection by the oomycete Hyaloperonospora arabidopsis. This priming is regulated by convergent pathways, which depend on phosphoinositideand ABA-dependent signalling components. Conversely, induced resistance by WCS417r and β-aminobutyric acid against the bacterial pathogen Pseudomonas syringae are controlled by distinct NPR1-dependent signalling pathways. As WCS417r and β-aminobutyric acid prime jasmonate-and salicylate-inducible genes, respectively, we subsequently investigated the role of transcription factors. A quantitative PCR-based genome-wide screen for putative WCS417r-and β-aminobutyric acid-responsive transcription factor genes revealed distinct sets of priming-responsive genes. Transcriptional analysis of a selection of these genes showed that they can serve as specific markers for priming. Promoter analysis of WRKY genes identified a putative cis-element that is strongly over-represented in promoters of 21 NPR1-dependent, β-aminobutyric acid-inducible WRKY genes.• Our study shows that priming of defence is regulated by different pathways, depending on the inducing agent and the challenging pathogen. Furthermore, we demonstrated that priming is associated with the enhanced expression of transcription factors.
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