Functional analysis of oxidative burst in sugarcane smut-resistant and -susceptible genotypes

Peters, Leila Priscila; Carvalho, Gabriela Ferreira; Vilhena, Milca Bartz; Creste, Silvana; Azevedo, Ricardo Antunes; Monteiro-Vitorello, Cláudia Barros

doi:10.1007/s00425-016-2642-z

Cited by 46 publications

(59 citation statements)

References 64 publications

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“…Following sexual mating, dikaryotic hyphae with two compatible nuclei are formed and these hyphae are infectious (Sundar et al, 2012). The dikaryotic hypha grows along with sugarcane bud meristem and eventually forms the appressorium on the inner scales of the young buds (Peters et al, 2016). The two compatible nuclei then fuse and give rise to a diploid teliospore.…”

Section: Introductionmentioning

confidence: 99%

“…The two compatible nuclei then fuse and give rise to a diploid teliospore. A round of meiosis occurs during teliospore germination and generates four haploid sporidia (Sundar et al, 2012;Yan et al, 2015;Peters et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

“…In the long-term interaction between plant hosts and fungal pathogens, plants have evolved two layers of defence, namely PTI (pathogen-associated molecular pattern-triggered immunity) and ETI (effector-triggered immunity), both of which involve ROS (reactive oxygen species) burst to restrict pathogen infection (Apostol et al, 1989;Scheel, 1998). On the other hand, plant pathogens have evolved ability to neutralize host-derived ROS to ensure successful infection (Apel & Hirt, 2004;Deng et al, 2012;Peters et al, 2016). Besides as a host defence mechanism, ROS also carries out physiological functions in the pathogenic fungi, to ensure proper pathogenic development.…”

Section: Introductionmentioning

confidence: 99%

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cAMP/PKA signalling pathway regulates redox homeostasis essential for Sporisorium scitamineum mating/filamentation and virulence

Chang

Cai

Deng

et al. 2019

Environmental Microbiology

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Summary The fungal pathogen Sporisorium scitamineum causes sugarcane smut disease. The formation and growth of dikaryotic hypha after sexual mating is critical for S. scitamineum pathogenicity, however regulation of S. scitimineum mating has not been studied in detail. We identified and characterized the core components of the conserved cAMP/PKA pathway in S. scitamineum by reverse genetics. Our results showed that cAMP/PKA signalling pathway is essential for proper mating and filamentation, and thus critical for S. scitamineum virulence. We further demonstrated that an elevated intracellular ROS (reactive oxygen species) level promotes S. scitamineum mating‐filamentation, via transcriptional regulation of ROS catabolic enzymes, and is under regulation of the cAMP/PKA signalling pathway. Furthermore, we found that fungal cAMP/PKA signalling pathway is also involved in regulation of host ROS response. Overall, our work displayed a positive role of elevated intracellular ROS in fungal differentiation and virulence.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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cAMP/PKA signalling pathway regulates redox homeostasis essential for Sporisorium scitamineum mating/filamentation and virulence

Chang

Cai

Deng

et al. 2019

Environmental Microbiology

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“…Raffinose accumulation is an attractive candidate strategy together with the antioxidant system to restrain plant cell damage. Peters et al (2017) did not detect membrane damage in their experiments in any of the genotypes analyzed (susceptible and resistant).…”

Section: Discussionmentioning

confidence: 87%

“…Sugarcane is known to promote oxidative burst in response to smut infection (Lao et al, 2008; Su et al, 2014; Peters et al, 2017). Recently, detailed analysis of ROS metabolism revealed that a sugarcane resistant genotype maintained high levels of oxygen peroxide by a SOD independent pathway potentially to activate defense responses (Peters et al, 2017). Raffinose accumulation is an attractive candidate strategy together with the antioxidant system to restrain plant cell damage.…”

Section: Discussionmentioning

confidence: 99%

Metabolome Dynamics of Smutted Sugarcane Reveals Mechanisms Involved in Disease Progression and Whip Emission

et al. 2017

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Sugarcane smut disease, caused by the biotrophic fungus Sporisorium scitamineum, is characterized by the development of a whip-like structure from the plant meristem. The disease causes negative effects on sucrose accumulation, fiber content and juice quality. The aim of this study was to exam whether the transcriptomic changes already described during the infection of sugarcane by S. scitamineum result in changes at the metabolomic level. To address this question, an analysis was conducted during the initial stage of the interaction and through disease progression in a susceptible sugarcane genotype. GC-TOF-MS allowed the identification of 73 primary metabolites. A set of these compounds was quantitatively altered at each analyzed point as compared with healthy plants. The results revealed that energetic pathways and amino acid pools were affected throughout the interaction. Raffinose levels increased shortly after infection but decreased remarkably after whip emission. Changes related to cell wall biosynthesis were characteristic of disease progression and suggested a loosening of its structure to allow whip growth. Lignin biosynthesis related to whip formation may rely on Tyr metabolism through the overexpression of a bifunctional PTAL. The altered levels of Met residues along with overexpression of SAM synthetase and ACC synthase genes suggested a role for ethylene in whip emission. Moreover, unique secondary metabolites antifungal-related were identified using LC-ESI-MS approach, which may have potential biomarker applications. Lastly, a putative toxin was the most important fungal metabolite identified whose role during infection remains to be established.

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Time-series expression profiling of sugarcane leaves infected with Puccinia kuehnii reveals an ineffective defense system leading to susceptibility

et al. 2020

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Puccinia kuehnii is an obligate biotrophic fungus that infects sugarcane leaves causing a disease called orange rust. It spread out to other countries resulting in reduction of crop yield since its first outbreak in Australia. One of the knowledge gaps of that pathosystem is to understand the molecular mechanisms altered in susceptible plants by the stress induced by P. kuehnii. Here we investigated changes in temporal expression of transcripts in pathways associated with the immune system. To achieve this purpose, we used RNA-Seq to analyze infected leaf samples collected at 0, 12, 24, 48 hours after inoculation (hai), 5 and 12 days after inoculation (dai). A de novo transcriptome was assembled with preprocessed reads, filtering out potential fungal sequences to focus on plant transcripts. Differential expression analyses of adjacent time points revealed substantial changes at 12, 48 hai and 12 dai, coinciding with the events of spore germination, haustoria post-penetration and post-sporulation. During the first 24 hours, a lack of transcripts involved with resistance mechanisms was revealed by underrepresentation of hypersensitive and defense responses. However, two days after inoculation, upregulation of genes involved with immune response regulation provided evidence of some potential defense response. Events related to biotic stress and phenylpropanoid biosynthesis pathways were predominantly downregulated in the initial time points, but expression was later restored to basal levels. Similar waves of expression were apparent for sets of genes in photosynthesis and oxidative processes, whose initial repression could avoid production of signaling molecules. Their subsequent upregulation possibly restored carbohydrate metabolism, ensuring pathogen nutritional requirements were met. Our results support the hypothesis that P. kuehnii initially suppressed sugarcane genes involved in plant defense systems. Late overexpression of specific regulatory pathways also suggests the possibility of an inefficient recognition system by a susceptible sugarcane genotype.

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Functional analysis of oxidative burst in sugarcane smut-resistant and -susceptible genotypes

Cited by 46 publications

References 64 publications

cAMP/PKA signalling pathway regulates redox homeostasis essential for Sporisorium scitamineum mating/filamentation and virulence

cAMP/PKA signalling pathway regulates redox homeostasis essential for Sporisorium scitamineum mating/filamentation and virulence

Metabolome Dynamics of Smutted Sugarcane Reveals Mechanisms Involved in Disease Progression and Whip Emission

Time-series expression profiling of sugarcane leaves infected with Puccinia kuehnii reveals an ineffective defense system leading to susceptibility

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