Plant-Microbe Interactions: Pathogenesis & Symbiosis
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Four Arabidopsis berberine‐bridge enzyme‐like proteins are specific oxidases that inactivate the elicitor‐active oligogalacturonides

Recognition of endogenous molecules acting as “damage-associated molecular patterns” (DAMPs) is a key feature of immunity in both animals and plants. Oligogalacturonides (OGs), i.e. fragments derived from the hydrolysis of homogalacturonan, a major component of pectin are a well-known class of DAMPs that activate immunity and protect plants against several microbes. However, hyper-accumulation of OGs severely affects growth, eventually leading to cell death and clearly pointing to OGs as players in the growth-defence trade-off. Here we report a mechanism that may control the homeostasis of OGs avoiding their deleterious hyper-accumulation. By combining affinity chromatography on acrylamide-trapped OGs and other procedures, an Arabidopsis thaliana enzyme that specifically oxidizes OGs was purified and identified. The enzyme was named OG OXIDASE 1 (OGOX1) and shown to be encoded by the gene At4g20830. As a typical flavo-protein, OGOX1 is a sulphite-sensitive H2O2–producing enzyme that displays maximal activity on OGs with a degree of polymerization >4. OGOX1 belongs to a large gene family of mainly apoplastic putative FAD-binding proteins [Berberine-Bridge Enzyme-like (BBE-like); 27 members], whose biochemical and biological function is largely unexplored. We have found that at least four BBE-like enzymes in Arabidopsis are OG oxidases (OGOX1-4). Oxidized OGs display a reduced capability of activating the immune responses and are less hydrolysable by fungal polygalacturonases. Plants overexpressing OGOX1 are more resistant to Botrytis cinerea, pointing to a crucial role of OGOX enzymes in plant immunity.
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Genome-wide transcriptome profiling of transgenic hop (Humulus lupulus L.) constitutively overexpressing HlWRKY1 and HlWDR1 transcription factors | BMC Genomics | Full Text

Background
The hop plant (Humulus lupulus L.) is a valuable source of several secondary metabolites, such as flavonoids, bitter acids, and essential oils. These compounds are widely implicated in the beer brewing industry and are having potential biomedical applications. Several independent breeding programs around the world have been initiated to develop new cultivars with enriched lupulin and secondary metabolite contents but met with limited success due to several constraints. In the present work, a pioneering attempt has been made to overexpress master regulator binary transcription factor complex formed by HlWRKY1 and HlWDR1 using a plant expression vector to enhance the level of prenylflavonoid and bitter acid content in the hop. Subsequently, we performed transcriptional profiling using high-throughput RNA-Seq technology in leaves of resultant transformants and wild-type hop to gain in-depth information about the genome-wide functional changes induced by HlWRKY1 and HlWDR1 overexpression.

Results
The transgenic WW-lines exhibited an elevated expression of structural and regulatory genes involved in prenylflavonoid and bitter acid biosynthesis pathways. In addition, the comparative transcriptome analysis revealed a total of 522 transcripts involved in 30 pathways, including lipids and amino acids biosynthesis, primary carbon metabolism, phytohormone signaling and stress responses were differentially expressed in WW-transformants. It was apparent from the whole transcriptome sequencing that modulation of primary carbon metabolism and other pathways by HlWRKY1 and HlWDR1 overexpression resulted in enhanced substrate flux towards secondary metabolites pathway. The detailed analyses suggested that none of the pathways or genes, which have a detrimental effect on physiology, growth and development processes, were induced on a genome-wide scale in WW-transgenic lines.

Conclusions
Taken together, our results suggest that HlWRKY1 and HlWDR1 simultaneous overexpression positively regulates the prenylflavonoid and bitter acid biosynthesis pathways in the hop and thus these transgenes are presented as prospective candidates for achieving enhanced secondary metabolite content in the hop.
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Contribution of a lectin, LecM, to the quorum sensing signalling pathway of Ralstonia solanacearum strain OE1‐1 - Hayashi - - Molecular Plant Pathology - Wiley Online Library

The soil‐borne bacterium Ralstonia solanacearum invades the roots and colonizes the intercellular species and then the xylem. The expression of lecM, encoding a lectin LecM, is induced by an OmpR family response regulator HrpG in R. solanacearum strain OE1‐1. LecM contributes to the attachment of strain OE1‐1 to host cells of intercellular spaces. OE1‐1 produces methyl 3‐hydroxymyristate (3‐OH MAME) through a methyltransferase (PhcB) and extracellularly secretes the chemical as a quorum‐sensing (QS) signal, which activates QS. The expression of lecM is also induced by PhcA virulence regulator functioning through QS, and the resultant LecM is implicated in the QS‐dependent production of major exopolysaccharide EPS I and the aggregation of OE1‐1 cells. To investigate LecM functions in QS, we analysed the transcriptome of R. solanacearum strains generated by RNA sequencing technology. In the lecM mutant, the expression of positively QS‐regulated genes (by > 90%) and the expression of negatively QS‐regulated genes (by ~60%) was downregulated and upregulated, respectively. However, phcB and phcA in the lecM mutant were expressed at levels similar to those in strain OE1‐1. The lecM mutant produced significantly less ralfuranone and exhibited a significantly greater swimming motility, which are positively and negatively regulated by QS, respectively. In addition, the extracellular 3‐OH MAME content of lecM mutant was significantly lower than that of OE1‐1. The application of 3‐OH MAME increased more EPS I production in the phcB‐deleted mutant and strain OE1‐1 than in the lecM mutant. Thus, QS‐dependent produced LecM contributes to the QS signalling pathway.

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Role of a receptor-like kinase K1 in pea Rhizobium symbiosis development

The ability of the crop legume Pisum sativum L. to perceive the Nod factor rhizobial signals may depend on several receptors that differ in ligand structure specificity. Identification of pea mutants defective in two types of LysM receptor-like kinases (LysM-RLKs), SYM10 and SYM37, featuring different phenotypic manifestations and impaired at various stages of symbiosis development, corresponds well to this assumption. There is evidence that one of the receptor proteins involved in symbiosis initiation, SYM10, has an inactive kinase domain. This implies the presence of an additional component in the receptor complex, together with SYM10, that remains unknown. Here, we describe a new LysM-RLK, K1, which may serve as an additional component of the receptor complex in pea. To verify the function of K1 in symbiosis, several P. sativum non-nodulating mutants in the k1 gene were identified using the TILLING approach. Phenotyping revealed the blocking of symbiosis development at an appropriately early stage, strongly suggesting the importance of LysM-RLK K1 for symbiosis initiation. Moreover, the analysis of pea mutants with weaker phenotypes provides evidence for the additional role of K1 in infection thread distribution in the cortex and rhizobia penetration. The interaction between K1 and SYM10 was detected using transient leaf expression in Nicotiana benthamiana and in the yeast two-hybrid system. Since the possibility of SYM10/SYM37 complex formation was also shown, we tested whether the SYM37 and K1 receptors are functionally interchangeable using a complementation test. The interaction between K1 and other receptors is discussed.
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Subfamily-specific specialization of RGH1/MLA immune receptors in wild barley | Molecular Plant-Microbe Interactions

The barley disease resistance (R) gene locus Mildew Locus A (Mla) provides isolate-specific resistance against the powdery mildew fungus Blumeria graminis hordei (Bgh) and has been introgressed into modern cultivars from diverse germplasms, including the wild relative Hordeum spontaneum. Known Mla disease resistance specificities to Bgh appear to encode allelic variants of the R Gene Homolog 1 (RGH1) family of nucleotide-binding domain and leucine-rich repeat (NLR) proteins. We here sequenced and assembled the transcriptomes of 50 H. spontaneum accessions representing nine populations distributed throughout the Fertile Crescent. The assembled Mla transcripts exhibited rich sequence diversity, linked neither to geographic origin nor population structure and could be grouped into two similar-sized subfamilies based on two major N-terminal coiled-coil signaling domains that are both capable of eliciting cell death. The presence of positively selected sites, located mainly in the C-terminal leucine-rich repeats of both MLA subfamilies, together with the fact that both coiled-coil signaling domains mediate cell death, implies that the two subfamilies are actively maintained in the population. Unexpectedly, known MLA receptor variants that confer Bgh resistance belong exclusively to one subfamily. Thus, signaling domain divergence, potentially as adaptation to distinct pathogen populations, is an evolutionary signature of functional diversification of an immune receptor.
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Regulation of plant immune signaling by calcium-dependent protein kinases | Molecular Plant-Microbe Interactions

Activation of Ca2+ signaling is a universal response to stress that allows cells to quickly respond to environmental cues. Fluctuations in cytosolic calcium are decoded in plants by calcium-sensing proteins such as Ca2+-dependent protein kinases (CDPKs). The perception of microbes results in an influx of calcium that activates numerous CDPKs that propagate immune signals required for resistance against disease-causing pathogens. This review describes our current understanding of CDPK activation and regulation, and provides a comprehensive overview of CDPK-mediated immune signaling through interaction with various substrates.
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Ancient plants with ancient fungi

Arbuscular mycorrhizas are widespread in land plants including liverworts, some of the closest living relatives of the first plants to colonize land 500 million years ago (MYA). Previous investigations reported near-exclusive colonization of liverworts by the most recently evolved arbuscular mycorrhizal fungi, the Glomeraceae, indicating a recent acquisition from flowering plants at odds with the widely held notion that arbuscular mycorrhizal-like associations in liverworts represent the ancestral symbiotic condition in land plants. We performed an analysis of symbiotic fungi in 674 globally collected liverworts using molecular phylogenetics and electron microscopy. Here, we show every order of arbuscular mycorrhizal fungi colonizes early-diverging liverworts, with non-Glomeraceae being at least 10 times more common than in flowering plants. Arbuscular mycorrhizal fungi in liverworts and other ancient plant lineages (hornworts, lycopods, and ferns) were delimited into 58 taxa and 36 singletons, of which at least 43 are novel and specific to liverworts. The discovery that early plant lineages are colonized by early-diverging fungi supports the hypothesis that arbuscular mycorrhizas are an ancestral symbiosis for all land plants
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Frontiers | Seed transmission of Epichloë endophytes in Lolium perenne is heavily influenced by host genetics | Plant Science

Vertical transmission of symbiotic Epichloë endophytes from host grasses into progeny seed is the primary mechanism by which the next generation of plants is colonised. This process is often imperfect, resulting in endophyte-free seedlings which may have poor ecological fitness if the endophyte confers protective benefits to its host. In this study, we investigated the influence of host genetics and environment on the vertical transmission of Epichloë festucae var. lolii strain AR37 in the temperate forage grass Lolium perenne. The efficiency of AR37 transmission into the seed of over 500 plant genotypes from five genetically diverse breeding populations was determined. In Populations I-III, which had undergone previous selection for high seed infection by AR37, mean transmission was 88%, 93% and 92%, respectively. However, in Populations IV and V, which had not undergone previous selection, mean transmission was 69% and 70%, respectively. The transmission values, together with single nucleotide polymorphism data obtained using genotyping by sequencing for each host, was used to develop a genomic prediction model for AR37 seed transmission. The predictive ability of the model was estimated at r = 0.54. While host genotype contributed greatly to differences in AR37 seed transmission, undefined environmental variables also contributed significantly to seed transmission across different years and geographic locations. There was evidence for a small host genotype by environment effect, however this was less pronounced than genotype or environment alone. Analysis of endophyte infection levels in parent plants within Populations I and IV revealed a loss of endophyte infection over time in Population IV only. This population also had lower average tiller infection frequencies than Population I, suggesting that AR37 failed to colonise all the daughter tillers and therefore seeds. However, we also observed that infection of seed by AR37 may fail during or after initiation of floral development from plants where all tillers remained endophyte-infected over time. While the effects of environment and host genotype on fungal endophyte transmission have been evaluated previously, this is the first study that quantifies the relative impacts of host genetics and environment on endophyte vertical transmission.
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Medicago AP2-domain Transcription Factor WRI5a Is a Master Regulator of Lipid Biosynthesis and Transfer During Mycorrhizal Symbiosis

Most land plants evolve a mutualistic symbiosis with arbuscular mycorrhizal (AM) fungi to improve nutrient acquisition from the soil. In return, up to 20% of host plant photosynthate is transferred to the mycorrhizal fungus in the form of lipids and sugar. Nutrient exchange must be regulated by both partners in order to maintain a reliable symbiotic relationship. However, the mechanisms underlying the regulation of lipid transfer from plant to AM fungus remain elusive. Here, we show that Medicago truncatula AP2/EREBP transcription factor WRI5a, and likely its two homologs WRI5b/Erf1 and WRI5c, are master regulators of AM symbiosis by controlling lipid transfer and periarbuscular membrane formation. We found that WRI5a binds the AW-box cis-regulatory elements in the promoters of STR and MtPT4 in M. truncatula, which encodes a periarbuscular membrane-localized ABC transporter required for lipid transfer from the plant to AM fungi-and a phosphate transporter required for phosphate transfer from AM fungi to the plant, respectively. The M. truncatula wri5a mutant and RNAi composite plants hairy roots displayed impaired arbuscule formation, whereas overexpression of WRI5a resulted in enhanced expression of STR and MtPT4, suggesting that WRI5a regulates bidirectional symbiotic nutrient exchange. Moreover, we found that WRI5a and RAM1 (Required for Arbuscular Mycorrhization symbiosis 1) encoding a GRAS-domain transcription factor regulate each other at the transcriptional level, forming a positive feedback loop for regulating AM symbiosis. Our data suggest a role for WRI5a in controlling lipid transfer and periarbuscular membrane formation via the regulation of genes for the biosynthesis and supply of fatty acids and phosphate uptake in arbuscule-containing cells.
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Verticillium dahliae Alt a 1-like protein PevD1 targets cotton PR5-like protein and contributes to fungal infection | Journal of Experimental Botany | Oxford Academic

Alt a 1 family proteins (AA1s) have only been observed in the Dothideomycetes and Sordariomycetes classes of fungi, and their biological functions have been poorly understood to date. Verticillium dahliae, a soil-borne pathogen that causes plant verticillium wilt disease, secretes hundreds of proteins during the process of pathogenic infection, including the AA1s member PevD1. The pevd1 transcript was present in all of the hosts studied and showed elevated expression throughout the infection process. Furthermore, pevd1 knockout mutants displayed attenuated pathogenicity compared with the wild type (WT) strain and complemented strains in hosts. A partner protein of PevD1, pathogenesis-related protein 5 (PR5)-like protein GhPR5, was isolated from cotton plants by co-purification assays, and the PevD1-GhPR5 interaction was further confirmed by a pull-down assay. The GhPR5-interacting region of PevD1 was determined to be located in the C-terminus (PevD1b, amino acids residues 113–155) via pull-down and Y2H techniques. Reintroduction of the pevd1b gene into a pevd1 knockout mutant resulted in restoration of the virulence phenotype to WT levels. Moreover, PevD1b, similar to PevD1, decreased the antifungal activity of GhPR5 in vitro. Our findings highlight a new infection strategy in which V. dahliae secretes PevD1 to inhibit GhPR5 antifungal activity to overcome the host defence system.
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Review: Functional linkages between amino acid transporters and plant responses to pathogens - ScienceDirect

Upon infection, plant pathogens become dependent on their hosts for nutrition. Therefore, the interaction between the two organisms is tightly linked to the availability and flux of nutrients in the plant. The plant’s nitrogen metabolism is reprogrammed during pathogen attack, likely reflecting plant’s response to invasion by the pathogen and active modification by the pathogen to promote feeding. Several lines of evidence indicate that plant-derived amino acids are an important source of nitrogen for diverse pathogens. Moreover, amino acid homeostasis is interconnected with the plant’s immune signaling pathways. Here, we critically examine the knowns and unknowns about connections between plant-encoded amino acid transporters and resistance or susceptibility to pathogens and pests. We use recent insights into sugar transporters to frame a perspective with potential applicability to amino acids and other nutrients. We emphasize different approaches that have provided insight in this topic and we conclude with suggestions to fill gaps in foundational knowledge and explore new avenues for disease control.
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Candidatus Liberibacter asiaticus and its vector, Diaphorina citri, augments the TCA cycle of their host via the GABA shunt and polyamines pathway | Molecular Plant-Microbe Interactions

Huanglongbing, a destructive citrus disease, is associated with Candidatus Liberibacter asiaticus (CLas), which is transmitted by the Asian citrus psyllid, Diaphorina citri. Both CLas and its vector manipulate the host metabolism for their benefit to meet their nutritional needs and neutralize the host defense responses. We used a targeted GC-MS-based method to explore the connection between TCA cycle, γ-aminobutyric acid (GABA)-shunt and polyamines (PAs) pathways in citrus. CLas and D. citri accelerated the conversion of α-ketoglutarate to glutamate, then to GABA, causing an accumulation of GABA in the cytosol. In silico analysis showed that citrus genome possesses a putative GABA permease that connects the GABA-shunt with TCA cycle and supports the accumulation of succinate, fumarate, and citrate. Additionally, the PAs biosynthetic pathway might be connected directly to the TCA cycle through the production of fumarate, or indirectly via enhancement of GABA-shunt. Taken together, we suggest that GABA-shunt and PAs pathway are alternative pathways that contribute to the flux towards succinate rather than an intact TCA cycle in citrus. Both CLas and its vector enhance these pathways. This study provides more insights into citrus responses to the HLB pathosystem, and could be a further step to providing clues for understanding the nutritional needs of CLas, which could help in culturing CLas.
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Frontiers | LysM Receptor-Like Kinase and LysM Receptor-Like Protein families: an update on phylogeny and functional characterization | Plant Science

Members of plant specific families of Receptor-Like Kinases (RLKs) and Receptor-Like Proteins (RLPs), containing 3 extracellular LysMs have been shown to directly bind and/or to be involved in perception of lipo-chitooligosaccharides (LCO), chitooligosaccharides (CO) and peptidoglycan (PGN), three types of GlcNAc-containing molecules produced by microorganisms. These receptors are involved in microorganism perception by plants and can activate different plant responses leading either to symbiosis establishment or to defense responses against pathogens. LysM-RLK/Ps belong to multigenic families. Here, we provide a phylogeny of these families in 8 plant species, including dicotyledons and monocotyledons, and we discuss known or putative biological roles of the members in each of the identified phylogenetic groups. We also report and discuss known biochemical properties functions of the LysM-RLK/Ps.
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FERONIA Receptor Kinase Contributes to Plant Immunity by Suppressing Jasmonic Acid Signaling in Arabidopsis thaliana

FERONIA Receptor Kinase Contributes to Plant Immunity by Suppressing Jasmonic Acid Signaling in Arabidopsis thaliana | Plant-Microbe Interactions: Pathogenesis & Symbiosis | Scoop.it
Bacterial pathogens use effectors and phytotoxins to facilitate infection of host plants. Coronatine (COR) is one of the phytotoxins produced in bacterial pathogens, such as Pseudomonas syringae pv. tomato DC3000 (pst DC3000). COR structurally and functionally mimics the active form of the plant hormone jasmonic acid (JA), JA-isoleucine (JA-Ile), and can hijack the host JA-signaling pathway to achieve host disease susceptibility [1]. COR utilizes the transcription factor MYC2, a master regulator of JA signaling, to activate NAC transcription factors, which functions to inhibit accumulation of salicylic acid (SA) and thus compromise host immunity [2]. It has been demonstrated that SA can antagonize JA signaling through NONEXPRESSOR of PATHOGENESIS-RELATED GENE1 (NPR1) [3] and downstream transcription factors TGAs [4] and WRKYs [5, 6]. However, the detailed mechanism by which host plants counteract COR-mediated susceptibility is largely unknown. Here, we show that the receptor kinase FERONIA (FER) functions to inhibit JA and COR signaling by phosphorylating and destabilizing MYC2, thereby positively regulating immunity. Conversely, the peptide ligand RALF23 acts through FER to stabilize MYC2 and elevate JA signaling, negatively contributing to plant immunity. Our results establish the RALF23-FER-MYC2 signaling module and provide a previously unknown mechanism by which host plants utilize FER signaling to counteract COR-mediated host disease susceptibility.
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Transcriptome analysis reveals the molecular mechanisms of the defense response to gray leaf spot disease in maize | BMC Genomics | Full Text

Background
Gray leaf spot (GLS), which is caused by the necrotrophic fungi Cercospora zeae-maydis and Cercospora zeina, is one of the most impactful diseases in maize worldwide. The aim of the present study is to identify the resistance genes and understand the molecular mechanisms for GLS resistance.

Results
Two cultivars, ‘Yayu889’ and ‘Zhenghong532,’ which are distinguished as resistant and susceptible cultivars, respectively, were challenged with the GLS disease and a RNA-seq experiment was conducted on infected plants at 81, 89, 91, and 93 days post planting (dap). Compared with the beginning stage at 81 dap, 4666, 1733, and 1166 differentially expressed genes (DEGs) were identified at 89, 91, and 93 dap, respectively, in ‘Yayu889,’ while relatively fewer, i.e., 4713, 881, and 722 DEGs, were identified in ‘Zhenghong532.’ Multiple pathways involved in the response of maize to GLS, including ‘response to salicylic acid,’ ‘protein phosphorylation,’ ‘oxidation-reduction process,’ and ‘carotenoid biosynthetic process,’ were enriched by combining differential expression analysis and Weighted Gene Co-expression Network Analysis (WGCNA). The expression of 12 candidate resistance proteins in these pathways were quantified by the multiple reaction monitoring (MRM) method. This approach identified two candidate resistance proteins, a calmodulin-like protein and a leucine-rich repeat receptor-like protein kinase with SNPs that were located in QTL regions for GLS resistance. Metabolic analysis showed that, compared with ‘Zhenghong532,’ the amount of salicylic acid (SA) and total carotenoids in ‘Yayu889’ increased, while peroxidase activity decreased during the early infection stages, suggesting that increased levels of SA, carotenoids, and reactive oxygen species (ROS) may enhance the defense response of ‘Yayu889’ to GLS.

Conclusion
By combining transcriptome and proteome analyses with comparisons of resistance QTL regions, calmodulin-like protein and leucine-rich repeat receptor-like protein kinase were identified as candidate GLS resistance proteins. Moreover, we found that the metabolic pathways for ROS, SA, and carotenoids are especially active in the resistant cultivar. These findings could lead to a better understanding of the GLS resistance mechanisms and facilitate the breeding of GLS-resistant maize cultivars.
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A Meloidogyne graminicola C‐type lectin, Mg01965 is secreted into the host apoplast to suppress plant defense and promote parasitism - Zhuo - - Molecular Plant Pathology - Wiley Online Library

C‐type lectins (CTLs), a class of multifunctional proteins, are numerous in nematodes. One CTL gene Mg01965 shown to be expressed in the subventral glands especially in the second‐stage juveniles of the root‐knot nematode Meloidogyne graminicola was further analyzed in this study. In vitro RNA interference targeting Mg01965 in the preparasitic juveniles significantly reduced their ability to infect host plant roots. Immunolocalizations showed that Mg01965 is secreted by M. graminicola into the roots during the early parasitic stages and accumulates in the apoplast. Transient expression of Mg01965 in N. benthamiana and targeting it to the apoplast suppressed the burst of reactive oxygen species triggered by flg22. The CTL Mg01965 suppresses plant innate immunity in the host apoplast, promoting nematode parasitism in the early infection stages.
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OsJAZ9 overexpression improves potassium deficiency tolerance in rice by modulating jasmonic acid levels and signaling

Potassium (K) which makes around 2-10% of plants total dry biomass, when become deficient, makes the plants highly susceptible to both abiotic and biotic stresses. Recent evidences suggest overlapping transcriptional responses to K deficiency and Jasmonate (JA) treatment in plants. However, a link between these responses was missing. Notably, K deficiency and JA application produce similar phenotypic and transcriptional responses. Here, we used molecular, physiological and morphological studies to analyze the role of OsJAZ9 in JA homeostasis, K deficiency and sheath blight resistance. We raised OsJAZ9 overexpression, knockdown, translational reporter and C-terminal deleted translational reporter lines in rice to establish the role of JA signaling in K ion homeostasis and OsJAZ9 as a critical component of JA signaling for K deficiency response. OsJAZ9 overexpression and knockdown provide K deficiency tolerance and sensitivity, respectively, by modulating various K transporters and root system architecture. Furthermore, RNA Seq and JA profiling revealed an elevation of JA responsive genes and JA levels in OsJAZ9 OE lines under K deficiency. Our data provide clear evidence on the crucial role of JAZ repressor, OsJAZ9 in improving K deficiency tolerance in rice by altering JA levels and signaling.
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A Dihydroflavonol-4-reductase-like Protein Interacts with NFR5 and Regulates Rhizobial Infection in Lotus japonicus | Molecular Plant-Microbe Interactions

In almost all symbiotic interactions between rhizobia and leguminous plants, host flavonoid-induced synthesis of Nod factors in rhizobia is required to initiate symbiotic response in plants. In this study, we found that Lotus japonicus Nod Factor Receptor 5 (LjNFR5) might directly regulate flavonoid biosynthesis during symbiotic interaction with rhizobia. A yeast two-hybrid analysis revealed that a dihydroflavonol-4-reductase-like protein (LjDFL1) interacts with LjNFR5. The interaction between MtDFL1 and MtNFP, two Medicago truncatula proteins with homology to LjDFL1 and LjNFR5, respectively, was also shown, suggesting that interaction between these two proteins might be conserved in different legumes. LjDFL1 was highly expressed in root hairs and the epidermal cells of root tips. Lotus ljdfl1 mutants and Medicago mtdfl1 mutants produced significantly fewer infection threads (ITs) than the wild-type control plants following rhizobial treatment. Furthermore, the roots of stable transgenic L. japonicus plants overexpressing LjDFL1 formed more ITs than control roots after exposure to rhizobia. These data indicated that LjDFL1 is a positive regulator of symbiotic signaling. However, the expression of LjDFL1 was suppressed by rhizobial treatment, suggesting that a negative feedback loop might be involved in regulation of the symbiotic response in L. japonicus.
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Rpp1 encodes a ULP1-NBS-LRR protein that controls immunity to Phakopsora pachyrhizi in soybean | Molecular Plant-Microbe Interactions

Phakopsora pachyrhizi is the causal agent of Asian soybean rust. Susceptible soybean plants infected by virulent isolates of P. pachyrhizi are characterized by tan-colored lesions and erumpent uredinia on the leaf surface. Germplasm screening and genetic analyses have led to the identification of seven loci, Rpp1 – Rpp7, that provide varying degrees of resistance to P. pachyrhizi (Rpp). Two genes, Rpp1 and Rpp1b, map to the same region on soybean chromosome 18. Rpp1 is unique among the Rpp genes in that it confers an immune response (IR) to avirulent P. pachyrhizi isolates. The IR is characterized by a lack of visible symptoms, whereas resistance provided by Rpp1b – Rpp7 results in red-brown foliar lesions. Rpp1 maps to a region spanning approximately 150 Kb on chromosome 18 between markers Sct_187 and Sat_064 in L85-2378 (Rpp1), an isoline developed from Williams 82 and PI 200492 (Rpp1). To identify Rpp1, we constructed a bacterial artificial chromosome (BAC) library from soybean accession PI 200492. Sequencing of the Rpp1 locus identified three homologous nucleotide binding site-leucine rich repeat (NBS-LRR) candidate resistance genes between Sct_187 and Sat_064. Each candidate gene is also predicted to encode an N-terminal ubiquitin-like protease 1 (ULP1) domain. Co-silencing of the Rpp1 candidates abrogated the immune response in the Rpp1 resistant soybean accession PI 200492, indicating that Rpp1 is a ULP1-NBS-LRR protein and plays a key role in the IR.
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Heterotrimeric G-proteins in unfolded protein response mediate plant growth-defense tradeoffs upstream of steroid and immune signaling

Plants prioritize growth over defense to gain a competitive advantage for limited resources, but change priorities to successfully fight infection and herbivory. Despite the importance of growth-defense tradeoffs in optimizing plant productivity in natural and agricultural populations, the molecular mechanisms that link growth and immunity remain unclear. Here, we demonstrate that growth-defense tradeoffs between pathways activated by BRI1, a steroid receptor, and FLS2, an innate immune receptor, are uncoupled in an Arabidopsis mutant (agg1 agg2) lacking two redundant heterotrimeric G-protein gamma subunits that form stable heterodimers with the Gβ subunit AGB1 to control one arm of the unfolded protein response (UPR) independently of ER stress. Growth inhibition from induced immunity in wild-type plants is likely caused by AGB1-AGG1/2 dimers interacting with nascent BRI1 and FLS2 proteins on the endoplasmic reticulum (ER) membrane and repressing an UPR response that is hardwired to promote BRI1 protein biogenesis and FLS2 protein degradation via autophagy. The ability to unlock and fine-tune growth-defense tradeoffs through UPR signaling provides a novel strategy to increase the natural defenses of crops while maintaining optimal plant productivity.
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NIN interacts with NLPs to mediate nitrate inhibition of nodulation in Medicago truncatula

NIN interacts with NLPs to mediate nitrate inhibition of nodulation in Medicago truncatula | Plant-Microbe Interactions: Pathogenesis & Symbiosis | Scoop.it
Legume plants can assimilate inorganic nitrogen and have access to fixed nitrogen through symbiotic interaction with diazotrophic bacteria called rhizobia. Symbiotic nitrogen fixation is an energy-consuming process and is strongly inhibited when sufficient levels of fixed nitrogen are available, but the molecular mechanisms governing this regulation are largely unknown. The transcription factor nodule inception (NIN) is strictly required for nodulation and belongs to a family of NIN-like proteins (NLPs), which have been implicated in the regulation of nitrogen homeostasis in Arabidopsis. Here, we show that mutation or downregulation of NLP genes prevents nitrate inhibition of infection, nodule formation and nitrogen fixation. We find that NIN and NLPs physically interact through their carboxy-terminal PB1 domains. Furthermore, we find that NLP1 is required for the expression of nitrate-responsive genes and that nitrate triggers NLP1 re-localization from the cytosol to the nucleus. Finally, we show that NLP1 can suppress NIN activation of CRE1 expression in Nicotiana benthamiana and Medicago truncatula. Our findings highlight a central role for NLPs in the suppression of nodulation by nitrate.
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A WW domain-containing protein forms immune nuclear bodies against begomoviruses

As DNA viruses, which replicate in the nucleus of infected cells, the bipartite begomoviruses (Geminiviridae family) encode the nuclear shuttle protein (NSP) to facilitate the translocation of viral DNA from the nucleus to the cytoplasm via nuclear pores. This intracellular trafficking of NSP-DNA complexes is accessorized by the NSP-interacting GTPase (NIG) at the cytosolic side. Here, we report the nuclear redistribution of NIG by AtWWP1, a WW domain-containing protein, which forms immune nuclear bodies (NBs) against begomoviruses. We demonstrated that AtWWP1 relocates NIG from the cytoplasm to the nucleus where it is confined to AtWWP1-NBs. Therefore, the NIG-AtWWP1 interaction may interfere with the NIG pro-viral function that is associated with its cytosolic localization. Consistent with this hypothesis, loss of AtWWP1 function further debilitated the plant upon begomovirus infection and overexpression of AtWWP1 enhanced resistance to begomovirus. Furthermore, a defective AtWWP1 mutant for nuclear body formation was no longer capable of interacting and relocating NIG to the nucleus and lost its immune function against begomovirus. The antiviral function of AtWWP1-NBs, however, may be antagonized by the viral infection, which was demonstrated to induce either a decrease in the number or disruption of AtWWP1-NBs. Collectively, our data establish that AtWWP1 organizes nuclear structures as nuclear foci, which provide intrinsic immunity against begomovirus infection.
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Identification and characterization of a new class of temperature‐dependent Tsw‐based Tomato spotted wilt virus resistance breaking isolates - de Ronde - - Plant Pathology - Wiley Online Library

The single dominant Tsw resistance gene from Capsicum chinense against the Tomato spotted wilt orthotospovirus (TSWV) is temperature sensitive, i.e. the resistance fails to function at or above 32 °C. Here, we describe a new class of temperature‐sensitive resistance breaking TSWV isolates that induce Tsw‐mediated resistance at T <28 °C but at T ≥ 28 °C break this resistance. The NSs genes from these isolates were cloned and expressed to be analyzed for RNA silencing suppressor (RSS) activity and the ability to induce a Tsw‐mediated hypersensitive response (HR) in Capsicum chinense and Capsicum annuum (Tsw+). Unlike in viral infection, transient expression of some of the NSs proteins at standard temperatures (22°C) did not induce Tsw‐mediated HR, although varying degrees of RSS activity were observed. Attempts to express and test the NSs proteins for functionality at an elevated temperature through agroinfiltration remained unsuccessful. The NSs proteins of some TSWV resistance breaking (RB) isolates analyzed lacked amino acid residues that were previously shown to be important for RNA silencing suppression and avirulence. This study describes a new class of resistance breaking TSWV isolates that may be of importance for breeders and growers, and for which the underlying mechanism still remains unknown.
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A plant chitinase controls cortical infection thread progression and nitrogen-fixing symbiosis

Morphogens provide positional information and their concentration is key to the organized development of multicellular organisms. Nitrogen-fixing root nodules are unique organs induced by Nod factor-producing bacteria. Localized production of Nod factors establishes a developmental field within the root where plant cells are reprogrammed to form infection threads and primordia. We found that regulation of Nod factor levels by Lotus japonicus is required for the formation of nitrogen-fixing organs, determining the fate of this induced developmental program. Our analysis of plant and bacterial mutants shows that a host chitinase modulates Nod factor levels possibly in a structure-dependent manner. In Lotus, this is required for maintaining Nod factor signalling in parallel with the elongation of infection threads within the nodule cortex, while root hair infection and primordia formation are not influenced. Our study shows that infected nodules require balanced levels of Nod factors for completing their transition to functional, nitrogen-fixing organs.
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Frontiers | Metabolomics analysis of soybean hypocotyls in response to Phytophthora sojae infection | Plant Science

Soybean is one of the most important economic and oil crops across the world. Phytophthora root rot (PRR), caused by Phytophthora sojae (P. sojae), is a major disease in most soybean-growing regions worldwide. Here, we investigated metabolic changes in hypocotyls of two soybean lines, Nannong 10-1 (resistant line, R) and 06-070583 (susceptible line, S), at two time points (12 hpi and 36 hpi) after P. sojae infection and metabolic differences between the R line and the S line. In total, 90 differentially accumulated metabolites (DAMs) were identified after P. sojae infection; the levels of 50 metabolites differed between the R line and the S line. There are 28 DAMs that not only differentially accumulated between the R line and the S line but also differentially accumulated after P. sojae infection. Based on the changes of these DAMs in response to P. sojae infection in different lines and at different timepoints, and the differences in the contents of these DAMs between the R line and the S line, we speculated that DAMs, including sugars (monosaccharides and oligosaccharides), organic acids (oxalic acid, cumic acid), amino acid derivatives, and other secondary metabolites (mannitol, octanal, hypoxanthine and daidzein etc.) may participate in the metabolic-level defense response of soybean to P. sojae. In this study, an integrated pathway-level analysis of transcriptomics (obtained by RNA-Seq) and metabolomics data illustrated the poor connections and interdependencies between the metabolic and transcriptional responses of soybean to P. sojae infection. This work emphasizes the value of metabolomic studies of plant-pathogen interactions and paves the way for future research of critical metabolic determinants of the soybean-P. sojae interaction.
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Bias in resistance gene prediction due to repeat masking

Several recently published Brassicaceae genome annotations show strong differences in resistance (R)-gene content. We believe that this is caused by different approaches to repeat masking. Here we show that some of the repeats stored in public databases used for repeat masking carry pieces of predicted R-gene-related domains, and demonstrate that at least some of the variance in R-gene content in recent genome annotations is caused by using these repeats for repeat masking. We also show that other classes of genes are less affected by this phenomenon, and estimate a false positive rate of R genes (0 to 4.6%) that are in reality transposons carrying the R-gene domains. These results may partially explain why there has been a decrease in published novel R genes in recent years, which has implications for plant breeding, especially in the face of pathogens changing as a response to climate change.
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