Reactive Oxygen Species Play a Role in the Infection of the Necrotrophic Fungi, Rhizoctonia solani in Wheat

Foley, Rhonda C.; Kidd, Brendan N.; Hane, James K.; Anderson, Jonathan P.; Singh, Karam B.

doi:10.1371/journal.pone.0152548

Cited by 68 publications

(46 citation statements)

References 80 publications

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“…Here we report that the barley Sbs1 and Sbs2 genes were upregulated at 36 and 12 hpi, respectively, by a virulent isolate of B. sorokiniana , which facilitates further disease development in the pathogen’s necrotrophic phase. ROS production is considered as a signal cue for activating cell death responses providing resistance against biotrophic pathogens but increasing the virulence of a necrotroph (60). DAB staining of the susceptible barley cv Steptoe that contains functional Sbs1 and Sbs2 alleles and the resistant cv Morex showed a different timeline of H 2 O 2 production.…”

Section: Discussionmentioning

confidence: 99%

rcs5-mediated spot blotch resistance in barley is conferred by wall-associated kinases that resist pathogen manipulation

Ameen

Solanki

Drader

et al. 2020

Preprint

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27Plant biotrophic pathogen disease resistances rely on immunity receptor-mediated programmed 28 cell death (PCD) responses, but specialized necrotrophic/hemi-biotrophic pathogens hijack these 29 mechanisms to colonize the resulting dead tissue in their necrotrophic phase. Thus, immunity receptors 30 can become necrotrophic pathogen dominant susceptibility targets but resistance mechanisms that resist 31 necrotroph manipulation are recessive resistance genes. The barley rcs5 QTL imparts recessive resistance 32 against the disease spot blotch caused by the hemi-biotrophic fungal pathogen Bipolaris sorokiniana. The 33 rcs5 genetic interval was delimited to ~0.23 cM, representing an ~234 kb genomic region containing four 34 wall-associated kinase (WAK) genes, designated HvWak2, Sbs1, Sbs2 (susceptibility to Bipolaris 35 sorokiniana 1&2), and HvWak5. Post-transcriptional gene silencing of Sbs1&2 in susceptible barley 36 cultivars resulted in resistance showing dominant susceptibility function. Allele analysis of Sbs1&2 from 37 resistant and susceptible barley cultivars identified sequence polymorphisms associated with phenotypes 38in their primary coding sequence and promoter regions, suggesting differential transcriptional regulation 39 may contribute to susceptibility. Transcript analysis of Sbs1&2 showed nearly undetectable expression in 40 resistant and susceptible cultivars prior to pathogen challenge; however, upregulation of both genes 41 occurred specifically in susceptible cultivars post-inoculation with a virulent isolate. Apoplastic wash 42 fluids collected from barley infected with a virulent isolate induced Sbs1, suggesting regulation by an 43 apoplastic-secreted effector. Thus, Sbs1&2 function as B. sorokiniana susceptibility targets and non-44 functional alleles or alleles that resist induction by the pathogen mediate rcs5-recessive resistance. The 45 sbs1&2 alleles underlying the rcs5 QTL that the pathogen is unable to manipulate are the first resistance 46 genes identified against spot blotch. 47Bipolaris sorokiniana 1 and 2) as wall-associated kinases. These genes are hijacked by the 53 hemibiotrophic pathogen in its necrotrophic phase to induce programmed cell death, facilitating disease 54 development. We report the first spot blotch resistance/susceptibility genes cloned that function via alleles 55 that cannot be specifically induced and hijacked by virulent isolates of the pathogen. 56 study on a large breeding panel provided a comprehensive assessment of the genetic architecture of this 79 durable spot blotch resistance, identifying three quantitative trait loci (QTL): Rcs-qtl-1H-11_10764, Rcs-80 qtl-3H-11_10565 and Rcs-qtl-7H-11_20162. Of these QTL, Rcs-qtl-7H-11_20162 conferred the largest 81 allelic effect across different populations (10) with several genetic studies positioning rcs5 within the 82 interval of this chromosome 7H QTL (9-11). Thus, the gene/s underlying the rcs5 QTL is an important 83 target for cloning and functional characterization, which was the objective of this study. 8...

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Section: Discussionmentioning

confidence: 99%

rcs5-mediated spot blotch resistance in barley is conferred by wall-associated kinases that resist pathogen manipulation

Ameen

Solanki

Drader

et al. 2020

Preprint

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“…The role of pathogenproduced ROS in the Arabidopsis-A. brassicae pathosystem needs to be addressed, given the various studies that show the importance of pathogen-produced ROS in development of infection structures and host penetration (Foley et al, 2016;Samalova et al, 2014;Segmuller et al, 2008;Shetty et al, 2007;Tiedemann 1997).…”

Section: Discussionmentioning

confidence: 99%

ROS accumulation and associated cell death mediates susceptibility to Alternaria brassicae in Arabidopsis accessions

Mandal

Rajarammohan

Kaur

2019

Preprint

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Alternaria brassicae is a necrotrophic fungal pathogen capable of infecting most of the agriculturally important Brassica species. The mechanisms underlying invasion of A. brassicae and host responses are unknown. In the present study, we exploited the natural variation in Arabidopsis to understand the molecular and cellular mechanisms underlying resistance to A. brassicae. Using a subset of resistant (Ei-2, Ull2-3, Lz-0, and Cvi-0) and susceptible (Gre-0, Est-1, and Zdr1) accessions, we show that the susceptibility to A. brassicae is associated with higher ROS accumulation and cell death. Susceptibility to A. brassicae was reduced in the rboh (D, E and F) mutants that are incapable of producing ROS, suggesting that RBOH D, E and F may act as negative regulators of defence against this pathogen. Additionally, our data also supports the hypothesis that the Jasmonic acid (JA), Ethylene (ET) and Abscisic acid (ABA) signalling pathways positively contribute to resistance against necrotrophic pathogens. In summary, these results reveal the central role of ROS and cell death in the pathogenesis of A. brassicae and expand our understanding of plant-necrotroph interactions.

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“…Apoplastic synthesis of superoxide (O 2 •− ) and its dismutation product hydrogen peroxide (H 2 O 2 ) has been reported in response to a variety of pathogens (Doke 1983; Auh and Murphy 1995; Grant et al 2000). Although ROS accumulation typically correlates with active disease resistance reactions against biotrophic or hemibiotrophic pathogens (Vanacker et al 2000; Allan and Fluhr 1997), certain necrotrophs induce ROS synthesis in the infected tissue to promote cell death that facilitates subsequent infection (Govrin and Levine 2000; Foley et al 2016). In fact, ROS-mediated defense responses, effective against biotrophic pathogens, increase the susceptibility to necrotrophic pathogens (Kliebenstein and Rowe 2008).…”

Section: Discussionmentioning

confidence: 99%

The necrotrophic fungusMacrophomina phaseolinainduces oxidative stress-associated genes and related biochemical responses in charcoal rot susceptible sorghum genotypes

Bandara

Weerasooriya

Liu

et al. 2019

Preprint

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Macrophomina phaseolina (MP) is a necrotrophic fungus that causes charcoal rot disease in sorghum [Sorghum bicolor (L.) Moench]. The host resistance and susceptibility mechanisms for this disease are poorly understood. Here, the transcriptional and biochemical aspects of the oxidative stress and antioxidant system of charcoal rot resistant and susceptible sorghum genotypes in response to MP inoculation were investigated. RNA sequencing revealed 96 differentially expressed genes between resistant (SC599) and susceptible (Tx7000) genotypes that are related to the host oxidative stress and antioxidant system. Follow-up functional experiments demonstrated MP’s ability to significantly increase reactive oxygen (ROS) and nitrogen species (RNS) content in the susceptible genotypes. This was confirmed by increased malondialdehyde content, an indicator of ROS/RNS-mediated lipid peroxidation. The presence of nitric oxide (NO) in stalk tissues of susceptible genotypes was confirmed using a NO-specific fluorescent probe (DAF-FM DA) and visualized by confocal microscopy. Inoculation significantly increased peroxidase activity in susceptible genotypes while catalase activity was significantly higher in MP-inoculated resistant genotypes. MP inoculation significantly reduced superoxide dismutase activity in all genotypes. These findings suggested MP’s ability to promote a host-derived oxidative stress response in susceptible sorghum genotypes, which contributes to induced cell death-associated disease susceptibility to this necrotrophic phytopathogen.

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Reactive Oxygen Species Play a Role in the Infection of the Necrotrophic Fungi, Rhizoctonia solani in Wheat

Cited by 68 publications

References 80 publications

rcs5-mediated spot blotch resistance in barley is conferred by wall-associated kinases that resist pathogen manipulation

rcs5-mediated spot blotch resistance in barley is conferred by wall-associated kinases that resist pathogen manipulation

ROS accumulation and associated cell death mediates susceptibility to Alternaria brassicae in Arabidopsis accessions

The necrotrophic fungusMacrophomina phaseolinainduces oxidative stress-associated genes and related biochemical responses in charcoal rot susceptible sorghum genotypes

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