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Tomato auxin biosynthesis/signaling is reprogrammed by the geminivirus to enhance its pathogenicity

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Abstract

Main conclusion

Tomato leaf curl New Delhi virus-derived AC4 protein interacts with host proteins involved in auxin biosynthesis and reprograms auxin biosynthesis/signaling to help in viral replication and manifestation of the disease-associated symptoms.

Abstract

Perturbations of phytohormone-mediated gene regulatory network cause growth and developmental defects. Furthermore, plant viral infections cause characteristic disease symptoms similar to hormone-deficient mutants. Tomato leaf curl New Delhi Virus (ToLCNDV)-encoded AC4 is a small protein that attenuates the host transcriptional gene silencing, and aggravated disease severity in tomato is correlated with transcript abundance of AC4. Hence, investigating the role of AC4 in pathogenesis divulged that ToLCNDV-AC4 interacted with host TAR1 (tryptophan amino transferase 1)-like protein, CYP450 monooxygenase—the key enzyme of indole acetic acid (IAA) biosynthesis pathway—and with a protein encoded by senescence-associated gene involved in jasmonic acid pathway. Also, ToLCNDV infection resulted in the upregulation of host miRNAs, viz., miR164, miR167, miR393 and miR319 involved in auxin signaling and leaf morphogenesis concomitant with the decline in endogenous IAA levels. Ectopic overexpression of ToLCNDV-derived AC4 in tomato recapitulated the transcriptomic and disruption of auxin biosynthesis/signaling features of the infected leaves. Furthermore, exogenous foliar application of IAA caused remission of the characteristic disease-related symptoms in tomato. The roles of ToLCNDV-AC4 in reprogramming auxin biosynthesis, signaling and cross-talk with JA pathway to help viral replication and manifest the disease-associated symptoms during ToLCNDV infection are discussed.

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Acknowledgements

The authors gratefully acknowledge the financial support from ICAR-IARI for this work.

Funding

This work was supported by the Indian Council of Agricultural Research-Indian Agricultural Research Institute, New Delhi, India.

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Authors and Affiliations

  1. Division of Biochemistry, ICAR-Indian Agricultural Research Institute, New Delhi, 110012, India

    T. Vinutha, S. Vanchinathan, Navita Bansal & Shelly Praveen

  2. Division of Biochemistry, ICAR-National Rice Research Institute, Cuttack, Orissa, 753006, India

    Gaurav Kumar

  3. Division of Plant Pathology-Advanced Centre for Plant Virology, ICAR-Indian Agricultural Research Institute, New Delhi, 110012, India

    Vipin Permar

  4. Division of Plant Physiology, ICAR-Indian Agricultural Research Institute, New Delhi, 110012, India

    Archana Watts

  5. ICAR-Division of Physiology, Biochemistry and PHT, ICAR-Central Plantation Crops Research Institute, Kasaragod, Kerala, 671124, India

    S. V. Ramesh

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Correspondence to S. V. Ramesh or Shelly Praveen.

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Vinutha, T., Vanchinathan, S., Bansal, N. et al. Tomato auxin biosynthesis/signaling is reprogrammed by the geminivirus to enhance its pathogenicity. Planta 252, 51 (2020). https://doi.org/10.1007/s00425-020-03452-9

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