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

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ORIGINAL ARTICLE

Tomato auxin biosynthesis/signaling is reprogrammed by the geminivirus to enhance its pathogenicity T. Vinutha1 · S. Vanchinathan1 · Navita Bansal1 · Gaurav Kumar2 · Vipin Permar3 · Archana Watts4 · S. V. Ramesh5   · Shelly Praveen1 Received: 18 May 2020 / Accepted: 27 August 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020

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. Keywords  ToLCNDV · Pathogenicity factor · Phytohormones · AC4 · miRNAs · Host–virus interactions

Communicated by Anastasios Melis. * S. V. Ramesh [email protected]; [email protected]

Archana Watts [email protected]

* Shelly Praveen [email protected]; [email protected]

1



T. Vinutha [email protected]

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

2



S. Vanchinathan [email protected]

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

3



Navita Bansal [email protected]

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

4

Gaurav Kumar [email protected]



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

5



ICAR‑Division