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This review summarizes recent progress in our current understanding of the mechanisms underlying the cell death pathways in bryophytes, focusing on conserved pathways and particularities in comparison to angiosperms. Regulated cell death (RCD) plays key roles during essential processes along the plant life cycle. It is part of specific developmental programmes and maintains homeostasis of the organism in response to unfavourable environments. Bryophytes could provide valuable models to study developmental RCD processes as well as those triggered by biotic and abiotic stresses. Some pathways analogous to those present in angiosperms occur in the gametophytic haploid generation of bryophytes, allowing direct genetic studies. In this review, we focus on such RCD programmes, identifying core conserved mechanisms and raising new key questions to analyse RCD from an evolutionary perspective.

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Plants evolved, over millions of years, complex defense systems against pathogens. Once infected, the interaction between pathogen effector molecules and host receptors triggers plant immune responses, which include apoptosis, systemic immune response, among others. An important protein family responsible for pathogen effector recognition is the nucleotide binding site-leucine repeat rich (NBS-LRR) proteins. The NBS-LRR gene family is the largest disease resistance gene class in plants. These proteins are widely distributed in vascular plants and have a complex multigenic cluster distribution in plant genomes. To counteract the genetic load of such a large gene family on fitness cost, plants evolved a mechanism using post transcriptional gene silencing induced by small RNAs, particularly microRNAs. For the NBS-LRR gene family, the small RNAs involved in this silencing mechanism are mainly the microRNA482/2118 superfamily. This suppression mechanism is relieved upon pathogen infection, thus allowing increased NBS-LRR expression and triggering plant immunity. In this review, we will discuss the biogenesis of microRNAs and secondary RNAs involved in this silencing mechanism, biochemical and structural features of NBS-LRR proteins in response to pathogen effectors and the evolution of microRNA-based silencing mechanism with a focus on the miR482/2118 family. Furthermore, the biotechnological manipulation of microRNA expression, using both transgenic or genome editing approaches to improve cultivated plants will be discussed, with a focus on the miR482/2118 family in soybean.

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MAIN CONCLUSION: This review provides valuable insights into plant molecular regulatory mechanisms during fungus attacks, highlighting potential miRNA candidates for future disease management. Plant defense responses to biotic stress involve intricate regulatory mechanisms, including post-transcriptional regulation of genes mediated by microRNAs (miRNAs). These small RNAs play a vital role in the plant's innate immune system, defending against viral, bacterial, and fungal attacks. Among the plant pathogenic fungi, Colletotrichum spp. are notorious for causing anthracnose, a devastating disease affecting economically important crops worldwide. Understanding the molecular machinery underlying the plant immune response to Colletotrichum spp. is crucial for developing tools to reduce production losses. In this comprehensive review, we examine the current understanding of miRNAs associated with plant defense against Colletotrichum spp. We summarize the modulation patterns of miRNAs and their respective target genes. Depending on the function of their targets, miRNAs can either contribute to host resistance or susceptibility. We explore the multifaceted roles of miRNAs during Colletotrichum infection, including their involvement in R-gene-dependent immune system responses, hormone-dependent defense mechanisms, secondary metabolic pathways, methylation regulation, and biosynthesis of other classes of small RNAs. Furthermore, we employ an integrative approach to correlate the identified miRNAs with various strategies and distinct phases of fungal infection. This study provides valuable insights into the current understanding of plant miRNAs and their regulatory mechanisms during fungus attacks.

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Despite the positive results of using elicitors to induce resistance against plant diseases, some factors have inhibited the popularization of their use in agriculture. There is an energetic cost related to the elicitors' induced response which can cause undesired effects on growth under low-pressure disease conditions. Elicitors can create phytotoxicity and show high variation in their efficiency between different genotypes within the same crop; in addition, the positive results related to the induced resistance may not repeat in field treatments, adding to the possibility that they are not economically viable. Thus, we carried out two experiments to investigate the technical and economic efficiency of acibenzolar-S-methyl (ASM) and its association with fungicides in the control of leaf diseases of susceptible and resistant wheat varieties, and as how it reflects on the photosynthetic and production performance of wheat. This study showed the limitations of incorporating ASM into foliar fungal disease control in economic terms. However, it was evident that ASM effectively induced plant resistance against Leaf Rust and Powdery Mildew in the field and can be considered a sustainable option for wheat cultivation. Even though its association with chemical control was not the best economic strategy the use of ASM is a tool that can be incorporated into wheat cultivation to minimize the emergence of fungicide-resistant pathogens due to the diversification of modes of action employed and reduce the toxic residue deposition to the environment and human health.

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Current research in basic and applied knowledge of plant science has aimed to unravel the role of the interaction between environmental factors and the genome in the physiology of plants to confer the ability to overcome challenges in a climate change scenario. Evidence shows that factors causing environmental stress (stressors), whether of biological, chemical, or physical origin, induce eustressing or distressing effects in plants depending on the dose. The latter suggests the induction of the "hormesis" phenomenon. Sustainable crop production requires a better understanding of hormesis, its basic concepts, and the input variables to make its management feasible. This implies that acknowledging hormesis in plant research could allow specifying beneficial effects to effectively manage environmental stressors according to cultivation goals. Several factors have been useful in this regard, which at low doses show beneficial eustressing effects (biostimulant/elicitor), while at higher doses, they show distressing toxic effects. These insights highlight biostimulants/elicitors as tools to be included in integrated crop management strategies for reaching sustainability in plant science and agricultural studies. In addition, compelling evidence on the inheritance of elicited traits in plants unfolds the possibility of implementing stressors as a tool in plant breeding.

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Plants are at risk of attack by various pathogenic organisms. During pathogenesis, microorganisms produce molecules with conserved structures that are recognized by plants that then initiate a defense response. Plants also experience iron deficiency. To address problems caused by iron deficiency, plants use two strategies focused on iron absorption from the rhizosphere. Strategy I is based on rhizosphere acidification and iron reduction, whereas Strategy II is based on iron chelation. Pathogenic defense and iron uptake are not isolated phenomena: the antimicrobial phenols are produced by the plant during defense, chelate and solubilize iron; therefore, the production and secretion of these molecules also increase in response to iron deficiency. In contrast, phytohormone jasmonic acid and salicylic acid that induce pathogen-resistant genes also modulate the expression of genes related to iron uptake. Iron deficiency also induces the expression of defense-related genes. Therefore, in the present review, we address the cross-talk that exists between the defense mechanisms of both Systemic Resistance and Systemic Acquired Resistance pathways and the response to iron deficiency in plants, with particular emphasis on the regulation genetic expression.

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Cell-surface-localized pattern recognition receptors (PRRs) and intracellular nucleotide-binding domain and leucine-rich repeat receptors (NLRs) are plant immune proteins that trigger an orchestrated downstream signaling in response to molecules of microbial origin or host plant origin. Historically, PRRs have been associated with pattern-triggered immunity (PTI), whereas NLRs have been involved with effector-triggered immunity (ETI). However, recent studies reveal that such binary distinction is far from being applicable to the real world. Although the perception of plant pathogens and the final mounting response are achieved by different means, central hubs involved in signaling are shared between PTI and ETI, blurring the zig-zag model of plant immunity. In this review, we not only summarize our current understanding of PRR- and NLR-mediated immunities in plants, but also highlight those signaling components that are evolutionarily conserved across the plant kingdom. Altogether, we attempt to offer an overview of how plants mediate and integrate the induction of the defense responses that comprise PTI and ETI, emphasizing the need for more evolutionary molecular plant-microbe interactions (EvoMPMI) studies that will pave the way to a better understanding of the emergence of the core molecular machinery involved in the so-called evolutionary arms race between plants and microbes.

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MAIN CONCLUSION: This review highlights the most relevant and recent updated information available on the defense responses of selected hosts against Xanthomonas spp. Xanthomonas is one of the most important genera of Gram-negative phytopathogenic bacteria, severely affecting the productivity of economically important crops worldwide, colonizing either the vascular system or the mesophyll tissue of the host. Due to its rapid propagation, Xanthomonas poses an enormous challenge to farmers, because it is usually controlled using huge quantities of copper-based chemicals, adversely impacting the environment. Thus, developing new ways of preventing colonization by these bacteria has become essential. Advances in genomic and transcriptomic technologies have significantly elucidated at molecular level interactions between various crops and Xanthomonas species. Understanding how these hosts respond to the infection is crucial if we are to exploit potential approaches for improving crop breeding and cutting productivity losses. This review focuses on our current knowledge of the defense response mechanisms in agricultural crops after Xanthomonas infection. We describe the molecular basis of host-bacterium interactions over a broad spectrum with the aim of improving our fundamental understanding of which genes are involved and how they work in this interaction, providing information that can help to speed up plant breeding programs, namely using gene editing approaches.

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Background: Plant innate immunity relies on a broad repertoire of receptor proteins that can detect pathogens and trigger an effective defense response. Bioinformatic tools based on conserved domain and sequence similarity are within the most popular strategies for protein identification and characterization. However, the multi-domain nature, high sequence diversity and complex evolutionary history of disease resistance (DR) proteins make their prediction a real challenge. Here we present RFPDR, which pioneers the application of Random Forest (RF) for Plant DR protein prediction. Methods: A recently published collection of experimentally validated DR proteins was used as a positive dataset, while 10x10 nested datasets, ranging from 400-4,000 non-DR proteins, were used as negative datasets. A total of 9,631 features were extracted from each protein sequence, and included in a full dimension (FD) RFPDR model. Sequence selection was performed, to generate a reduced-dimension (RD) RFPDR model. Model performances were evaluated using an 80/20 (training/testing) partition, with 10-cross fold validation, and compared to baseline, sequence-based and state-of-the-art strategies. To gain some insights into the underlying biology, the most discriminatory sequence-based features in the RF classifier were identified. Results and Discussion: RD-RFPDR showed to be sensitive (86.4 ± 4.0%) and specific (96.9 ± 1.5%) for identifying DR proteins, while robust to data imbalance. Its high performance and robustness, added to the fact that RD-RFPDR provides valuable information related to DR proteins underlying properties, make RD-RFPDR an interesting approach for DR protein prediction, complementing the state-of-the-art strategies.

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The endoplasmic reticulum (ER) stress response is triggered by any condition that disrupts protein folding and promotes the accumulation of unfolded proteins in the lumen of the organelle. In eukaryotic cells, the evolutionarily conserved unfolded protein response is activated to clear unfolded proteins and restore ER homeostasis. The recovery from ER stress is accomplished by decreasing protein translation and loading into the organelle, increasing the ER protein processing capacity and ER-associated protein degradation activity. However, if the ER stress persists and cannot be reversed, the chronically prolonged stress leads to cellular dysfunction that activates cell death signaling as an ultimate attempt to survive. Accumulating evidence implicates ER stress-induced cell death signaling pathways as significant contributors for stress adaptation in plants, making modulators of ER stress pathways potentially attractive targets for stress tolerance engineering. Here, we summarize recent advances in understanding plant-specific molecular mechanisms that elicit cell death signaling from ER stress. We also highlight the conserved features of ER stress-induced cell death signaling in plants shared by eukaryotic cells.

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BACKGROUND AND AIMS: Plants have evolved complex mechanisms to fight against pathogens. Among these mechanisms, pattern-triggered immunity (PTI) relies on the recognition of conserved microbe- or pathogen-associated molecular patterns (MAMPs or PAMPs, respectively) by membrane-bound receptors. Indeed, PTI restricts virus infection in plants and, in addition, BRI1-associated kinase 1 (BAK1), a central regulator of PTI, plays a role in antiviral resistance. However, the compounds that trigger antiviral defences, along with their molecular mechanisms of action, remain mostly elusive. Herein, we explore the role of a fungal extracellular subtilase named AsES in its capacity to trigger antiviral responses. METHODS: In this study, we obtained AsES by recombinant expression, and evaluated and characterized its capacity to trigger antiviral responses against Tobacco mosaic virus (TMV) by performing time course experiments, analysing gene expression, virus movement and callose deposition. KEY RESULTS: The results of this study provide direct evidence that exogenous treatment with recombinant AsES increases a state of resistance against TMV infection, in both arabidopsis and Nicotiana benthamiana plants. Also, the antiviral PTI response exhibited by AsES in arabidopsis is mediated by the BAK1/SERK3 and BKK1/SERK4 co-receptors. Moreover, AsES requires a fully active salicylic acid (SA) signalling pathway to restrict the TMV movement by inducing callose deposition. Additionally, treatment with PSP1, a biostimulant based on AsES as the active compound, showed an increased resistance against TMV in N. benthamiana and tobacco plants. CONCLUSIONS: AsES is a fungal serine protease which triggers antiviral responses relying on a conserved mechanism by means of the SA signalling pathway and could be exploited as an effective and sustainable biotechnology strategy for viral disease management in plants.

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The facultative biotrophic basidiomycete Sporisorium scitamineum causes smut disease in sugarcane. This study applied an assay to identify S. scitamineum candidate effectors (CEs) with plant immunity suppression activities by delivering them into Nicotiana benthamiana cells via the type-three secretion system of Pseudomonas fluorescens EtHAn. Six CEs were individually cloned into the pEDV6 vector and expressed by P. fluorescens EtHAn for translocation into the plant cells. Three CEs (g1052, g3890, and g5159) could suppress pattern-triggered immunity (PTI) responses with high reproducibility in different coinfiltration experiments with P. syringae pv. tomato DC3000. In addition, three CEs (g1052, g4549, and g5159) were also found to be AvrB-induced suppressors of effector-triggered immunity (ETI), demonstrating for the first time that S. scitamineum can defeat both PTI and ETI responses. A transcriptomic analysis at different stages of infection by the smut fungus of three sugarcane cultivars with contrasting responses to the pathogen revealed that suppressors g1052, g3890, g4549, and g5159 were induced at the early stage of infection. By contrast, the two CEs (g2666 and g6610) that did not exhibit suppression activities expressed only at the late stage of infection. Moreover, genomic structures of the CEs and searches for orthologs in other smut species suggested duplication events and further divergence in CEs evolution of S. scitamineum. Thus, the transient assay applied here demonstrated the potential of pEDV6 and P. fluorescens EtHAn as biological tools for identifying plant immune suppressors from S. scitamineum.

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Plant pathogenesis-related (PR) proteins are a large group of proteins, classified in 17 families, that are induced by pathological conditions. Here, we characterized the soybean PR-1 (GmPR-1) gene repertoire at the sequence, structural and expression levels. We found 24 GmPR-1 genes, clustered in two phylogenetic groups. GmPR-1 genes are under strong purifying selection, particularly those that emerged by tandem duplications. GmPR-1 promoter regions are abundant in cis-regulatory elements associated with major stress-related transcription factor families, namely WRKY, ERF, HD-Zip, C2H2, NAC, and GATA. We observed that 23 GmPR-1 genes are induced by stress conditions or exclusively expressed upon stress. We explored 1972 transcriptome samples, including 26 stress conditions, revealing that most GmPR-1 genes are differentially expressed in a plethora of biotic and abiotic stresses. Our findings highlight stress-responsive GmPR-1 genes with potential biotechnological applications, such as the development of transgenic lines with increased resistance to biotic and abiotic stresses.

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KEY MESSAGE: Chemical defenses are imperative for plant survival, but their production is often associated with growth restrictions. Here we review the most recent theories to explain this complex dilemma of plants. Plants are a nutritional source for a myriad of pests and pathogens that depend on green tissues to complete their life cycle. Rather than remaining passive victims, plants utilize an arsenal of chemical defenses to fend off biotic attack. While the deployment of such barriers is imperative for survival, the production of these chemical defenses is typically associated with negative impacts on plant growth. Here we discuss the most recent theories which explain this highly dynamic growth versus defense dilemma. Firstly, we discuss the hypothesis that the antagonism between the accumulation of chemical defenses and growth is rooted in the evolutionary history of plants and may be a consequence of terrestrialization. Then, we revise the different paradigms available to explain the growth versus chemical defense antagonism, including recent findings that update these into more comprehensive and plausible theories. Finally, we highlight state-of-the-art strategies that are now allowing the activation of growth and the concomitant production of chemical barriers in plants. Growth versus chemical defense antagonism imposes large ecological and economic costs, including increased crop susceptibility to pests and pathogens. In a world where these plant enemies are the main problem to increase food production, we believe that this review will summarize valuable information for future studies aiming to breed highly defensive plants without the typical accompanying penalties to growth.

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RESUMEN La bacteriosis vascular de la yuca, causada por la bacteria gram negativa Xanthomonas phaseoli pv. manihotis (Xpm), anteriormente conocida como Xanthomonas axonopodis pv. manihotis, es la principal enfermedad bacteriana que compromete su producción. Con la meta de generar una resistencia durable y de amplio espectro a la bacteriosis es posible explotar los mecanismos naturales presentes en plantas no-hospedero. Arabidopsis es una planta modelo extensamente estudiada, la cual es no-hospedero de Xpm. La meta de este estudio fue determinar si la resistencia no-hospedero de Arabidopsis es consecuencia de la presencia de barreras físicas o si esta depende de determinantes genéticos. En este trabajo se evaluó la capacidad de plantas de Arabidopsis de responder a la inoculación con Xpm. Ninguno de los ocho ecotipos de Arabidopsis evaluados mostraron una respuesta hipersensible a la inoculación con ocho diferentes cepas de Xpm. Aunque no se identificó la presencia de especies reactivas de oxígeno si se encontró un bloqueo en el crecimiento de Xpm en las plantas de Arabidopsis. En conjunto, los resultados aquí presentados sugieren que Arabidopsis no está activando una respuesta contra Xpm y que la resistencia observada puede ser consecuencia de las barreras físicas presentes en Arabidopsis que Xpm no es capaz de superar.

ABSTRACT Cassava bacterial blight (CBB), caused by the gram-negative bacteria Xanthomonas phaseoli pv. manihotis (Xpm), previously known as Xanthomonas axonopodis pv. manihotis, is the main bacterial disease compromising cassava production. With the aim to generate durable and broad-spectrum resistance to CBB is possible to exploit the natural mechanism present in non-host plants. Arabidopsis is an extensively studied model plant, which is a non-host of Xpm. The aim of this study was to determinate if the Arabidopsis non-host resistance is a consequence of physical barriers or if it depends on genetic determinants. In this work we evaluated the ability of Arabidopsis plants to respond after Xpm inoculation. None of the eight Arabidopsis ecotypes showed a hypersensitive response after inoculation with eight different Xpm strains. Although reactive oxygen species (ROS) production was not present, impairment in Xpm proliferation was found. These results suggest that Arabidopsis is not activating an immunity response against Xpm and the resistance might be a consequence of physical barriers present in Arabidopsis that Xpm is not able to overcome.

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Large volumes of fruit and vegetable production are lost during postharvest handling due to attacks by necrotrophic fungi. One of the promising alternatives proposed for the control of postharvest diseases is the induction of natural defense responses, which can be activated by recognizing molecules present in pathogens, such as chitin. Chitin is one of the most important components of the fungal cell wall and is recognized through plant membrane receptors. These receptors belong to the receptor-like kinase (RLK) family, which possesses a transmembrane domain and/or receptor-like protein (RLP) that requires binding to another RLK receptor to recognize chitin. In addition, these receptors have extracellular LysM motifs that participate in the perception of chitin oligosaccharides. These receptors have been widely studied in Arabidopsis thaliana (A. thaliana) and Oryza sativa (O. sativa); however, it is not clear how the molecular recognition and plant defense mechanisms of chitin oligosaccharides occur in other plant species or fruits. This review includes recent findings on the molecular recognition of chitin oligosaccharides and how they activate defense mechanisms in plants. In addition, we highlight some of the current advances in chitin perception in horticultural crops.

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Studies show that DNA methylation is associated with plant immunity but little is known as to how this epigenetic mechanism assists plants in adjusting their responses to biotic stress, especially when interacting with an hemibiotrophic pathogen such as citrus Phytophthora. The aim of the present study was to assess the effects of scion-rootstock interaction on plant resistance to P. citrophthora infection and DNA methylation patterns in 'Pera' sweet orange and 'Tahiti' acid lime grafted onto 'Rangpur' lime and 'Tropical' sunki rootstocks reinoculated with P. citrophthora. Results showed that reinoculated plants of the 'Pera' sweet orange/'Rangpur' lime and 'Tahiti' acid lime/'Tropical' sunki combinations with more and less sensitive varieties to Phytophthora, presented smaller stem lesions and increased frequency of full methylation and hemimethylation rates, compared to inoculated plants. In contrast, 'Tahiti' acid lime/'Rangpur' lime, two highly sensitive varieties, and 'Pera'/'Tropical' sunki, two much less sensitive varieties, showed high increases in the frequency of hemimethylation and non-methylation levels. Results suggest that in citrus, both the scion-rootstock interaction and DNA methylation affect the response to P. citrophthora infection. Reinoculated plants, depending on the combination, showed changes in intracellular hyphae growth through the formation of sets of fibers and crystal accumulation in the periderm, cortex, and phloem. In addition, starch grain concentration was higher in reinoculated plants in comparison to inoculated plants. These findings support the assumption that DNA methylation is a plant defense mechanism and therefore may be exploited to improve the response of plants to the gummosis of P. citrophthora in citrus.

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The plant hormone cytokinin (CK) plays central roles in plant development and throughout plant life. The perception of CKs initiating their signaling cascade is mediated by histidine kinase receptors (AHKs). Traditionally thought to be perceived mostly at the endoplasmic reticulum (ER) due to receptor localization, CK was recently reported to be perceived at the plasma membrane (PM), with CK and its AHK receptors being trafficked between the PM and the ER. Some of the downstream mechanisms CK employs to regulate developmental processes are unknown. A seminal report in this field demonstrated that CK regulates auxin-mediated lateral root organogenesis by regulating the endocytic recycling of the auxin carrier PIN1, but since then, few works have addressed this issue. Modulation of the cellular cytoskeleton and trafficking could potentially be a mechanism executing responses downstream of CK signaling. We recently reported that CK affects the trafficking of the pattern recognition receptor LeEIX2, influencing the resultant defense output. We have also recently found that CK affects cellular trafficking and the actin cytoskeleton in fungi. In this work, we take an in-depth look at the effects of CK on cellular trafficking and on the actin cytoskeleton in plant cells. We find that CK influences the actin cytoskeleton and endomembrane compartments, both in the context of defense signaling-where CK acts to amplify the signal-as well as in steady state. We show that CK affects the distribution of FLS2, increasing its presence in the plasma membrane. Furthermore, CK enhances the cellular response to flg22, and flg22 sensing activates the CK response. Our results are in agreement with what we previously reported for fungi, suggesting a fundamental role for CK in regulating cellular integrity and trafficking as a mechanism for controlling and executing CK-mediated processes.

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Powdery mildew causes substantial losses in crop and economic plant yields worldwide. Although powdery mildew infection of rubber trees (Hevea brasiliensis), caused by the biotrophic fungus Erysiphe quercicola, severely threatens natural rubber production, little is known about the mechanism by which E. quercicola adapts to H. brasiliensis to invade the host plant. In barley and Arabidopsis thaliana, lifeguard (LFG) proteins, which have topological similarity to BAX INHIBITOR-1, are involved in host plant susceptibility to powdery mildew infection. In this study, we characterized an H. brasiliensis LFG protein (HbLFG1) with a focus on its function in regulating defense against powdery mildew. HbLFG1 gene expression was found to be upregulated during E. quercicola infection. HbLFG1 showed conserved functions in cell death inhibition and membrane localization. Expression of HbLFG1 in Nicotiana benthamiana leaves and A. thaliana Col-0 was demonstrated to significantly suppress callose deposition induced by conserved pathogen-associated molecular patterns chitin and flg22. Furthermore, we found that overexpression of HbLFG1 in H. brasiliensis mesophyll protoplasts significantly suppressed the chitin-induced burst of reactive oxygen species. Although A. thaliana Col-0 and E. quercicola displayed an incompatible interaction, Col-0 transformants overexpressing HbLFG1 were shown to be susceptible to E. quercicola. Collectively, the findings of this study provide evidence that HbLFG1 acts as a negative regulator of plant immunity that facilitates E. quercicola infection in H. brasiliensis.

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