Facilitation of Fusarium graminearum Infection by 9-Lipoxygenases in Arabidopsis and Wheat

Fusarium graminearum causes Fusarium head blight, an important disease of wheat. F. graminearum can also cause disease in Arabidopsis thaliana. Here, we show that the Arabidopsis LOX1 and LOX5 genes, which encode 9-lipoxygenases (9-LOXs), are targeted during this interaction to facilitate infection. LOX1 and LOX5 expression were upregulated in F. graminearum–inoculated plants and loss of LOX1 or LOX5 function resulted in enhanced disease resistance in the corresponding mutant plants. The enhanced resistance to F. graminearum infection in the lox1 and lox5 mutants was accompanied by more robust induction of salicylic acid (SA) accumulation and signaling and attenuation of jasmonic acid (JA) signaling in response to infection. The lox1- and lox5-conferred resistance was diminished in plants expressing the SA-degrading salicylate hydroxylase or by the application of methyl-JA. Results presented here suggest that plant 9-LOXs are engaged during infection to control the balance between SA and JA signaling to facilitate infection. Furthermore, since silencing of TaLpx-1 encoding a 9-LOX with homology to LOX1 and LOX5, resulted in enhanced resistance against F. graminearum in wheat, we suggest that 9-LOXs have a conserved role as susceptibility factors in disease caused by this important fungus in Arabidopsis and wheat.

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Genome-Wide Characterization of Jasmonates Signaling Components Reveals the Essential Role of ZmCOI1a-ZmJAZ15 Action Module in Regulating Maize Immunity to Gibberella Stalk Rot

International Journal of Molecular Sciences ◽

10.3390/ijms22020870 ◽

2021 ◽

Vol 22 (2) ◽

pp. 870

Author(s):

Liang Ma ◽

Yali Sun ◽

Xinsen Ruan ◽

Pei-Cheng Huang ◽

Shi Wang ◽

...

Keyword(s):

Fusarium Graminearum ◽

Maize Production ◽

Stalk Rot ◽

Enhanced Resistance ◽

Genome Wide ◽

Susceptibility Factors ◽

A Genome ◽

Function Module ◽

Ja Signaling ◽

Signaling Components

Gibberella stalk rot (GSR) by Fusarium graminearum causes significant losses of maize production worldwide. Jasmonates (JAs) have been broadly known in regulating defense against pathogens through the homeostasis of active JAs and COI-JAZ-MYC function module. However, the functions of different molecular species of JAs and COI-JAZ-MYC module in maize interactions with Fusarium graminearum and regulation of diverse metabolites remain unknown. In this study, we found that exogenous application of MeJA strongly enhanced resistance to GSR. RNA-seq analysis showed that MeJA activated multiple genes in JA pathways, which prompted us to perform a genome-wide screening of key JA signaling components in maize. Yeast Two-Hybrid, Split-Luciferase, and Pull-down assays revealed that the JA functional and structural mimic coronatine (COR) functions as an essential ligand to trigger the interaction between ZmCOIa and ZmJAZ15. By deploying CRISPR-cas9 knockout and Mutator insertional mutants, we demonstrated that coi1a mutant is more resistant, whereas jaz15 mutant is more susceptible to GSR. Moreover, JA-deficient opr7-5opr8-2 mutant displayed enhanced resistance to GSR compared to wild type. Together, these results provide strong evidence that ZmJAZ15 plays a pivotal role, whereas ZmCOIa and endogenous JA itself might function as susceptibility factors, in maize immunity to GSR.

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The Combined Action of ENHANCED DISEASE SUSCEPTIBILITY1, PHYTOALEXIN DEFICIENT4, and SENESCENCE-ASSOCIATED101 Promotes Salicylic Acid-Mediated Defenses to Limit Fusarium graminearum Infection in Arabidopsis thaliana

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-04-15-0079-r ◽

2015 ◽

Vol 28 (8) ◽

pp. 943-953 ◽

Cited By ~ 17

Author(s):

Ragiba Makandar ◽

Vamsi J. Nalam ◽

Zulkarnain Chowdhury ◽

Sujon Sarowar ◽

Guy Klossner ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Salicylic Acid ◽

Fusarium Graminearum ◽

Response Regulator ◽

Constitutive Expression ◽

Catalytic Triad ◽

Head Blight ◽

Molecular Configuration ◽

Combined Action ◽

Arabidopsis Defense

Fusarium graminearum causes Fusarium head blight (FHB) disease in wheat and other cereals. F. graminearum also causes disease in Arabidopsis thaliana. In both Arabidopsis and wheat, F. graminearum infection is limited by salicylic acid (SA) signaling. Here, we show that, in Arabidopsis, the defense regulator EDS1 (ENHANCED DISEASE SUSCEPTIBILITY1) and its interacting partners, PAD4 (PHYTOALEXIN-DEFICIENT4) and SAG101 (SENESCENCE-ASSOCIATED GENE101), promote SA accumulation to curtail F. graminearum infection. Characterization of plants expressing the PAD4 noninteracting eds1L262P indicated that interaction between EDS1 and PAD4 is critical for limiting F. graminearum infection. A conserved serine in the predicted acyl hydrolase catalytic triad of PAD4, which is not required for defense against bacterial and oomycete pathogens, is necessary for limiting F. graminearum infection. These results suggest a molecular configuration of PAD4 in Arabidopsis defense against F. graminearum that is different from its defense contribution against other pathogens. We further show that constitutive expression of Arabidopsis PAD4 can enhance FHB resistance in Arabidopsis and wheat. Taken together with previous studies of wheat and Arabidopsis expressing salicylate hydroxylase or the SA-response regulator NPR1 (NON-EXPRESSER OF PR GENES1), our results show that exploring fundamental processes in a model plant provides important leads to manipulating crops for improved disease resistance.

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Limitation of Nocturnal ATP Import into Chloroplasts Seems to Affect Hormonal Crosstalk, Prime Defense, and Enhance Disease Resistance in Arabidopsis thaliana

Molecular Plant-Microbe Interactions ◽

10.1094/mpmi-02-10-0045 ◽

2010 ◽

Vol 23 (12) ◽

pp. 1584-1591 ◽

Cited By ~ 9

Author(s):

Gudrun Schmitz ◽

Thomas Reinhold ◽

Cornelia Göbel ◽

Ivo Feussner ◽

H. Ekkehard Neuhaus ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Salicylic Acid ◽

Jasmonic Acid ◽

Pseudomonas Syringae ◽

Pathogen Resistance ◽

Short Day ◽

Enhanced Resistance ◽

Genes Encoding ◽

Hormonal Crosstalk ◽

Hyaloperonospora Arabidopsidis

When grown under short-day conditions at low light, leaves of an Arabidopsis thaliana (accession Col-0) mutant with defects in the two genes encoding plastid ATP/ADP antiporters (so-called ntt1-2 null mutants) display a variety of physiological changes. These include the formation of necrotic lesions and the accumulation of hydrogen peroxide in the leaves. Here, we show that, under short-day conditions, leaves of the ntt1-2 mutant display enhanced resistance to Hyaloperonospora arabidopsidis, Botrytis cinerea, and Pseudomonas syringae pv. tomato DC3000. Resistance to these pathogens was associated with constitutively elevated levels of the plant hormone salicylic acid and, eventually, jasmonic acid, and constitutive or primed activation after pathogen attack of various defense genes that are dependent on these hormones. In addition, the antagonistic crosstalk between the salicylic acid and jasmonic acid signaling pathways seems to be affected in ntt1-2. Because the enhanced resistance of ntt1-2 to H. arabidopsidis was not seen when the mutant was grown under long-day conditions, our findings argue that nocturnal ATP import into chloroplasts is crucial to keep A. thaliana from runaway activation of pathogen resistance.

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ERECTA, salicylic acid, abscisic acid, and jasmonic acid modulate quantitative disease resistance of Arabidopsis thaliana to Verticillium longisporum

BMC Plant Biology ◽

10.1186/1471-2229-14-85 ◽

2014 ◽

Vol 14 (1) ◽

pp. 85 ◽

Cited By ~ 35

Author(s):

Eva Häffner ◽

Petr Karlovsky ◽

Richard Splivallo ◽

Anna Traczewska ◽

Elke Diederichsen

Keyword(s):

Arabidopsis Thaliana ◽

Salicylic Acid ◽

Abscisic Acid ◽

Disease Resistance ◽

Jasmonic Acid ◽

Quantitative Disease Resistance ◽

Verticillium Longisporum

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A family of pathogen-induced cysteine-rich transmembrane proteins is involved in plant disease resistance

Planta ◽

10.1007/s00425-021-03606-3 ◽

2021 ◽

Vol 253 (5) ◽

Author(s):

Marciel Pereira Mendes ◽

Richard Hickman ◽

Marcel C. Van Verk ◽

Nicole M. Nieuwendijk ◽

Anja Reinstädler ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Plasma Membrane ◽

Disease Resistance ◽

Plant Disease Resistance ◽

Transmembrane Proteins ◽

Series Data ◽

Immune Gene ◽

Biological Processes ◽

Hypocotyl Growth ◽

Enhanced Resistance

Abstract Main conclusion Overexpression of pathogen-induced cysteine-rich transmembrane proteins (PCMs) in Arabidopsis thaliana enhances resistance against biotrophic pathogens and stimulates hypocotyl growth, suggesting a potential role for PCMs in connecting both biological processes. Abstract Plants possess a sophisticated immune system to protect themselves against pathogen attack. The defense hormone salicylic acid (SA) is an important player in the plant immune gene regulatory network. Using RNA-seq time series data of Arabidopsis thaliana leaves treated with SA, we identified a largely uncharacterized SA-responsive gene family of eight members that are all activated in response to various pathogens or their immune elicitors and encode small proteins with cysteine-rich transmembrane domains. Based on their nucleotide similarity and chromosomal position, the designated Pathogen-induced Cysteine-rich transMembrane protein (PCM) genes were subdivided into three subgroups consisting of PCM1-3 (subgroup I), PCM4-6 (subgroup II), and PCM7-8 (subgroup III). Of the PCM genes, only PCM4 (also known as PCC1) has previously been implicated in plant immunity. Transient expression assays in Nicotiana benthamiana indicated that most PCM proteins localize to the plasma membrane. Ectopic overexpression of the PCMs in Arabidopsis thaliana resulted in all eight cases in enhanced resistance against the biotrophic oomycete pathogen Hyaloperonospora arabidopsidis Noco2. Additionally, overexpression of PCM subgroup I genes conferred enhanced resistance to the hemi-biotrophic bacterial pathogen Pseudomonas syringae pv. tomato DC3000. The PCM-overexpression lines were found to be also affected in the expression of genes related to light signaling and development, and accordingly, PCM-overexpressing seedlings displayed elongated hypocotyl growth. These results point to a function of PCMs in both disease resistance and photomorphogenesis, connecting both biological processes, possibly via effects on membrane structure or activity of interacting proteins at the plasma membrane.

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Resistance of Arabidopsis thaliana to the obligate biotrophic parasite Plasmodiophora brassicae

Plant Protection Science ◽

10.17221/10543-pps ◽

2017 ◽

Vol 38 (SI 2 - 6th Conf EFPP 2002) ◽

pp. 519-522 ◽

Cited By ~ 3

Author(s):

A. Arbeiter ◽

M. Fähling ◽

H. Graf ◽

M.D. Sacristán ◽

J. Siemens

Keyword(s):

Arabidopsis Thaliana ◽

Salicylic Acid ◽

Jasmonic Acid ◽

Resistance Gene ◽

Resistance Genes ◽

Plasmodiophora Brassicae ◽

Chromosome 1 ◽

Coding Sequences ◽

Resistance Phenotype ◽

Resistance Reaction

Two resistance phenotypes to P. brassicae have been found in A. thaliana. A first resistance phenotype has been detected to the isolate 'e<sub>2</sub>' and is polygenically inherited. The second resistance to isolate 'e<sub>3</sub>' is caused by the dominant resistance gene RPB1. By crossing no influence could be shown for salicylic acid, jasmonic acid and ethylene in the latter resistance reaction. The RPB1 locus was narrowed down to 71 kb on chromosome 1, where three pseudogenes and 13 coding sequences are located. Six of them showed cosegregation with RPB1. None of these sequences have similarities to identified resistance genes or other known genes. Ten coding sequences were expressed, but CDS9 was exclusively expressed in the resistant ecotype Tsu-0.

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Enhanced Resistance to Fusarium graminearum in Transgenic Arabidopsis Plants Expressing a Modified Plant Thionin

Phytopathology ◽

10.1094/phyto-12-19-0447-r ◽

2020 ◽

Vol 110 (5) ◽

pp. 1056-1066 ◽

Cited By ~ 2

Author(s):

Guixia Hao ◽

Matthew G. Bakker ◽

Hye-Seon Kim

Keyword(s):

Transgenic Plants ◽

Fusarium Graminearum ◽

Transgenic Arabidopsis ◽

Hyphal Growth ◽

Marker Genes ◽

Head Blight ◽

Transgenic Expression ◽

Transgenic Arabidopsis Plants ◽

Enhanced Resistance ◽

And Control

The fungal pathogen Fusarium graminearum causes Fusarium head blight (FHB) on wheat, barley, and other grains. FHB results in yield reductions and contaminates grain with trichothecene mycotoxins, which threaten food safety and food security. Innovative mechanisms for controlling FHB are urgently needed. We have previously shown that transgenic tobacco and citrus plants expressing a modified thionin (Mthionin) exhibited enhanced resistance toward several bacterial pathogens. The aim of this study was to investigate whether overexpression of Mthionin could be similarly efficacious against F. graminearum, and whether transgenic expression of Mthionin impacts the plant microbiome. Transgenic Arabidopsis plants expressing Mthionin were generated and confirmed. When challenged with F. graminearum, Mthionin-expressing plants showed less disease and fungal biomass in both leaves and inflorescences compared with control plants. When infiltrated into leaves, macroconidia of F. graminearum germinated at lower rates and produced less hyphal growth in Arabidopsis leaves expressing Mthionin. Moreover, marker genes related to defense signaling pathways were expressed at significantly higher levels after F. graminearum infection in Mthionin transgenic Arabidopsis plants. However, Mthionin expression did not appreciably alter the overall microbiome associated with transgenic plants grown under controlled conditions; across leaves and roots of Mthionin-expressing and control transgenic plants, only a few bacterial and fungal taxa differed, and differences between Mthionin transformants were of similar magnitude compared with control plants. In sum, our data indicate that Mthionin is a promising candidate to produce transgenic crops for reducing FHB severity and ultimately mycotoxin contamination.

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Fusarium graminearum ATP-Binding Cassette Transporter Gene FgABCC9 Is Required for Its Transportation of Salicylic Acid, Fungicide Resistance, Mycelial Growth and Pathogenicity towards Wheat

International Journal of Molecular Sciences ◽

10.3390/ijms19082351 ◽

2018 ◽

Vol 19 (8) ◽

pp. 2351 ◽

Cited By ~ 5

Author(s):

Peng-Fei Qi ◽

Ya-Zhou Zhang ◽

Cai-Hong Liu ◽

Jing Zhu ◽

Qing Chen ◽

...

Keyword(s):

Salicylic Acid ◽

Fusarium Graminearum ◽

Mycelial Growth ◽

Tertiary Structure ◽

Severe Disease ◽

Atp Binding ◽

Head Blight ◽

Transporter Family ◽

Wide Range ◽

Atp Binding Cassette

ATP-binding cassette (ABC) transporters hydrolyze ATP to transport a wide range of substrates. Fusarium graminearum is a major causal agent of Fusarium head blight, which is a severe disease in wheat worldwide. FgABCC9 (FG05_07325) encodes an ABC-C (ABC transporter family C) transporter in F. graminearum, which was highly expressed during the infection in wheat and was up-regulated by the plant defense hormone salicylic acid (SA) and the fungicide tebuconazole. The predicted tertiary structure of the FgABCC9 protein was consistent with the schematic of the ABC exporter. Deletion of FgABCC9 resulted in decreased mycelial growth, increased sensitivity to SA and tebuconazole, reduced accumulation of deoxynivalenol (DON), and less pathogenicity towards wheat. Re-introduction of a functional FgABCC9 gene into ΔFgABCC9 recovered the phenotypes of the wild type strain. Transgenic expression of FgABCC9 in Arabidopsis thaliana increased the accumulation of SA in its leaves without activating SA signaling, which suggests that FgABCC9 functions as an SA exporter. Taken together, FgABCC9 encodes an ABC exporter, which is critical for fungal exportation of SA, response to tebuconazole, mycelial growth, and pathogenicity towards wheat.

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