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

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. 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.