Synergistic interaction among begomoviruses leads to the suppression of host defense-related gene expression and breakdown of resistance in chilli

Abstract

Chilli (Capsicum sp.) is one of the economically important spice and vegetable crops grown in India and suffers great losses due to the infection of begomoviruses. Conventional breeding approaches have resulted in development of a few cultivars of chilli resistant to begomoviruses. A severe leaf curl disease was observed on one such resistant chilli cultivar (Capsicum annuum cv. Kalyanpur Chanchal) grown in the experimental field of the Jawaharlal Nehru University, New Delhi. Four different viral genomic components namely, Chilli leaf curl virus (DNA A), Tomato leaf curl Bangladesh betasatellite (DNA β), Tomato leaf curl New Delhi virus (DNA A), and Tomato leaf curl Gujarat virus (DNA B) were associated with the severe leaf curl disease. Further, frequent association of these four genomic components was also observed in symptomatic plants of other chilli cultivars (Capsicum annuum cv. Kashi Anmol and Capsicum chinense cv. Bhut Jolokia) grown in the experimental field. Interaction studies among the isolated viral components revealed that Nicotiana benthamiana and chilli plants inoculated with four genomic components of begomoviruses exhibited severe leaf curl disease symptoms. In addition, this synergistic interaction resulted in increased viral DNA accumulation in infected plants. Resistant chilli plants co-inoculated with four genomic components of begomoviruses showed drastic reduction of host basal (ascorbate peroxidase, thionin, polyphenol oxidase) and specific defense-related gene (NBS-LRR) expression. Our results suggested that synergistic interaction among begomoviruses created permissive cellular environment in the resistant chilli plants which leads to breakdown of natural resistance, a phenomenon observed for the first time in chilli.

A Novel Strain of Tomato Leaf Curl New Delhi Virus Has Spread to the Mediterranean Basin

“…Moreover, the exchange of DNA components (pseudo-recombination) might occur between begomoviruses, which can determine changes in the aggressiveness and host range. The latter was shown for example for pseudo-recombination between isolates of the bipartite begomoviruses ToLCNDV and tomato leaf curl Gujarat virus that can result in extremely severe infections in tomato [15] or determine a resistance break in chili pepper plants [57]. Viable pseudo-recombination between monopartite and bipartite begomoviruses has been reported, with evidence for acquisition of a DNA-B component by a monopartite begomovirus (e.g., [58]).…”

“…As DNA-B contains genes encoding the movement functions [59], its acquisition can determine novel host range abilities. Furthermore, synergistic interactions might occur in mixed infections [57], which eventually can lead to increased damage or even overcoming of resistance [57,60,61]. …”

Tomato leaf curl New Delhi virus: a widespread bipartite begomovirus in the territory of monopartite begomoviruses

“…The DNA‐A of Tomato leaf curl Gujarat virus (ToLCGuV) can trans‐replicate the DNA‐B of ToLCNDV and vice versa (Chakraborty et al ., ; Jyothsna et al ., ). Mixed infections of ToLCNDV with ToLCGuV have also been observed in the field (Singh et al ., ; Zaidi et al ., ) and demonstrated experimentally (Chakraborty et al ., ; Jyothsna et al ., ; Singh et al ., ).…”

“…The first association of a bipartite begomovirus with a betasatellite was observed in tomato in 2004 (W. S. Tsai and S. K. Green, unpublished results; as cited by Bull et al ., ). Further emphasizing the unusual promiscuity of ToLCNDV is the fact that it has also been found to be associated with several betasatellites, such as chilli leaf curl betasatellite (ChLCB) (Akhter et al ., ), radish leaf curl betasatellite (RaLCB) (Singh et al ., ), tobacco leaf curl betasatellite (TbLCB) (Singh et al ., ), tomato leaf curl Ranchi betasatellite (ToLCRnB) (Kumari et al ., ), cotton leaf curl Multan betasatellite (CLCuMuB) (Sivalingam et al ., ) and CLCuMuB in combination with luffa leaf distortion betasatellite (LuLDB) (Jyothsna et al ., ).…”

The Prediction of a New CLCuD Epidemic in the Old World

“…Rather, it may be an alarm bell for the third epidemic of CLCuD in this area ( Figure 1C ). The ability of ToLCNDV to develop synergistic interactions with other begomoviruses has recently been shown to cause resistance breakdown in chilies (Singh et al, 2016). CLCuAlV has been found associated with and trans-replicating a recombinant DNA-B of a bipartite begomovirus in wild cotton germplasm, proving the ability of CABs to acquire components from bipartite begomoviruses (Nawaz-ul-Rehman et al, 2012).…”