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Heightened miR6024-NLR interactions facilitate necrotrophic pathogenesis in tomato

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Abstract

Key message

miR6024 acts as a negative regulator of R genes, hence of Tomato plant immunity, and facilitates disease by the necrotrophic pathogen A. solani.

Abstract

Plant resistance genes or Nucleotide-binding leucine-rich repeat (NLR) genes, integral components of plant disease stress-signaling are targeted by variable groups of miRNAs. However, the significance of miRNA-mediated regulation of NLRs during a pathogen stress response, specifically for necrotrophic fungus, is poorly understood. A thorough examination of Tomato NLRs and miRNAs could map substantial interactions of which half the annotated NLRs were targets of Solanaceae-specific and conserved miRNAs, at the NB subdomain. The Solanaceae-specific miR6024 and its NLR targets analysed in different phytopathogenic stresses revealed differential and mutually antagonistic regulation. Interestingly, miR6024-targeted cleavage of a target NLR also triggered the generation of secondary phased siRNAs which could potentially amplify the defense signal. RNA-seq analysis of leaf tissues from miR6024 overexpressing Tomato plants evidenced a perturbation in the defense transcriptome with the transgenics showing unwarranted immune response-related genes’ expression with or without infection with necrotrophic Alternaria solani, though no adverse effect could be observed in the growth and development of the transgenic plants. Transgenic plants exhibited constitutive downregulation of the target NLRs, aggravated disease phenotype with an enhanced lesion, greater ROS generation and hypersusceptibility to A. solani infection, thus establishing that miR6024 negatively impacts plant immune response during necrotrophic pathogenesis. Limited knowledge about the outcome of NLR-miRNA interaction during necrotrophic pathogenesis is a hindrance to the deployment of miRNAs in crop improvement programs. With the elucidation of the necrotrophic disease-synergistic role played by miR6024, it becomes a potent candidate for biotechnological manipulation for the rapid development of pathogen-tolerant solanaceous plants.

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Data availability

All data supporting the findings of this study are available within the paper and within its supplementary data published online. RNA-seq data is available at GEO under the accession GSE166013.

Abbreviations

NLR:

Nucleotide-binding leucine-rich repeat

ToLCNDV:

Tomato Leaf Curl New Delhi Virus

RBOH:

Respiratory Burst Oxidase Homologs

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Acknowledgements

SD and AS received fellowships from CSIR, GoI and SC received DST-INSPIRE fellowship. This work is supported by grants from DBT and SERB, GoI to PK. The authors acknowledge Bose Institute CIF for technical help.

Funding

This work was supported by the Department of Biotechnology, Ministry of Science and Technology (BT/PR12942/AGR/36/652/2009) and the Science and Engineering Research Board (CRG/2018/003362). DBT GoI to P.k.

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Authors and Affiliations

  1. Division of Plant Biology, Unified Academic Campus, Bose Institute, EN 80, Bidhan Nagar, Kolkata, West Bengal, 700091, India

    Sayani Dey, Shreya Chowdhury, Raghuvir Singh, Ananya Mukherjee & Pallob Kundu

  2. Division of Bioinformatics, Unified Academic Campus, Bose Institute, EN 80, Bidhan Nagar, Kolkata, West Bengal, 700091, India

    Arijita Sarkar & Zhumur Ghosh

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  1. Sayani Dey
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  2. Arijita Sarkar
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  3. Shreya Chowdhury
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  4. Raghuvir Singh
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  5. Ananya Mukherjee
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  7. Pallob Kundu
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Contributions

SD and PK conceptualised and planned the research. SD performed most of the experiments and analysed the data. RS quantitated the phasiRNAs. AS contributed to several bioinformatic analyses. SC contributed to transgenic generation. RS and AM contributed to dCas9-KRAB based NLR repression. SD and PK wrote and revised the manuscript. ZG, AS and SC edited the manuscript.

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Correspondence to Pallob Kundu.

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Dey, S., Sarkar, A., Chowdhury, S. et al. Heightened miR6024-NLR interactions facilitate necrotrophic pathogenesis in tomato. Plant Mol Biol 109, 717–739 (2022). https://doi.org/10.1007/s11103-022-01270-z

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