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

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Abstract

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Successful orange rust development on sugarcane can potentially be explained as suppression of the plant immune system by the pathogen or delayed plant signaling to trigger defense responses.

Abstract

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. One of the knowledge gaps of that pathosystem is to understand the molecular mechanisms altered in susceptible plants by this biotic stress. Here, we investigated the 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 five time points after inoculation. Differential expression analyses of adjacent time points revealed substantial changes at 12, 48 h after inoculation and 12 days after inoculation, coinciding with the events of spore germination, haustoria post-penetration and post-sporulation, respectively. During the first 24 h, a lack of transcripts involved with resistance mechanisms was revealed by underrepresentation of hypersensitive and defense response related genes. 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 responses were predominantly downregulated in the initial time points, but expression was later restored to basal levels. Genes involved in carbohydrate metabolism showed evidence of repression followed by upregulation, possibly to ensure the 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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Acknowledgements

FHC received a fellowship grant #2015/17935-8, São Paulo Research Foundation (FAPESP). GRAM received a research grant #2015/22993-7, São Paulo Research Foundation (FAPESP). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001. This research was supported by the Brazilian Innovation Agency (FINEP), Grant number 01.09.0335.00 to MSC.

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Authors

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SGPG, NSM and MSC designed the study. SGPG performed the phytopathology experiment. NSM, MSC, LEAC and GRAM planned the RNA sequencing and qPCR experiments. FHC and GKH performed the RNA extraction, and MCC performed the qPCR experiments. FHC, GKH and GRAM analyzed the RNA-Seq data. FHC, GKH, MCC, CBMV, LEAC and GRAM wrote the manuscript. All authors reviewed the manuscript.

Corresponding author

Correspondence to Gabriel Rodrigues Alves Margarido.

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The authors declare that they have no conflict of interest.

Additional information

Communicated by Prakash Lakshmanan.

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Correr, F.H., Hosaka, G.K., Gómez, S.G.P. et al. Time-series expression profiling of sugarcane leaves infected with Puccinia kuehnii reveals an ineffective defense system leading to susceptibility. Plant Cell Rep 39, 873–889 (2020). https://doi.org/10.1007/s00299-020-02536-w

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  • DOI: https://doi.org/10.1007/s00299-020-02536-w

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