Synergism Among the Four Tobacco Bushy Top Disease Casual Agents in Symptom Induction and Aphid Transmission

Abstract

Tobacco bushy top disease (TBTD), caused by multiple pathogens including tobacco bushy top virus (TBTV), tobacco vein distorting virus (TVDV), TBTV satellite RNA (TBTVsatRNA), and TVDV-associated RNA (TVDVaRNA), is a destructive disease in tobacco fields. To date, how these causal agents are co-transmitted by aphid vectors in field and their roles in disease symptom induction remain largely unknown, due mainly to the lack of purified causal agents. In this study, we have constructed four full-length infectious clones, representing the Yunnan Kunming isolates of TVDV, TBTV, TBTVsatRNA, and TVDVaRNA (TVDV-YK, TBTV-YK, TBTVsatRNA-YK, and TVDVaRNA-YK), respectively. Co-inoculation of these four causal agents to tobacco K326 plants caused typical TBTD symptoms, including smaller leaves, necrosis, and plant stunting. In addition, inoculation of tobacco K326 plants with TBTV alone caused necrosis in systemic leaves by 7 dpi. Tobacco K326 and Nicotiana benthamiana plants infected by single virus or multiple viruses showed very different disease symptoms at various dpi. RT-PCR results indicated that co-infection of TVDVaRNA-YK could increase TVDV-YK or TBTV-YK accumulation in N. benthamiana plants, suggesting that TVDVaRNA-YK can facilitate TVDV-YK and TBTV-YK replication and/or movement in the infected plants. Aphid transmission assays showed that the successful transmission of TBTV-YK, TBTVsatRNA-YK, and TVDVaRNA-YK by Myzus persicae depended on the presence of TVDV-YK, while the presence of TBTVsatRNA-YK increased the aphid transmission efficiency of TBTV and TVDV. We consider that these four new infectious clones will allow us to further dissect the roles of these four causal agents in TBTD induction as well as aphid transmission.

Dissecting dynamic plant virus synergism in mixed infections of poleroviruses, umbraviruses, and tombusvirus-like associated RNAs

“…Our results show that CMoV appears to be a driver of symptom development when co-infected with TuYV and/or Sigma or ST9. CMoV also facilitated the systemic movement of all three tlaRNAsalbeit with differing efficiencies-in the absence of TuYV, corroborating the results of a recent study that demonstrated umbravirus-facilitated tlaRNA systemic movement in the tobacco bushy top disease (TBTD) complex (Chen et al, 2022).…”

“…Japonica), only CMoV and the CRLVaRNA could be detected in the recipient plant, making this the first reported evidence that an umbravirus may support tlaRNA systemic movement in the absence of a co-infecting polerovirus, although these results could also have other potential explanations. In another recent study by Chen et al (2022), after co-agroinoculation of infectious clones of the umbravirus tobacco bushy top virus (TBTV) with the tobacco vein distorting virus associated RNA (TVDVaRNA) the authors could detect the TVDVaRNA along with TBTV in the distal non-inoculated leaves, thereby confirming an umbravirus could independently support tlaRNA systemic movement. Here, we present data demonstrating that CMoV was able to support systemic movement of all three tlaRNAs (Gamma, Sigma, ST9), however this interaction appeared to be less efficient in co-infections with Gamma, suggesting some degree of specificity in these umbravirus-tlaRNA interactions.…”

“…While there are many studies on polerovirus-tlaRNA and polerovirus-umbravirus interactions in disease complexes harboring various combinations of these viruses, there exist only two recent studies that have begun to touch upon umbravirus-tlaRNA interactions (Yoshida, 2020;Chen et al, 2022). While we investigated the effects of co-infection in all possible co-infection combinations of the polerovirus TuYV, the umbravirus CMoV, and the tlaRNAs Gamma, Sigma, and ST9-with respect to single infections of each of these viruses-perhaps the most intriguing findings we uncovered were those concerning interactions involving CMoV and tlaRNAs.…”

Virome Analysis of Aconitum carmichaelii Reveals Infection by Eleven Viruses, including Two Potentially New Species

“…Vectors play vital roles in viral long-distance transmission and prevalence [30]. This study identified aphid-borne viruses CMV [31], ChiVMV [32], TVDV [33], and PLRV [34], as well as thrips-borne TSWV [35], infecting A. carmichaelii plants. Potyviruses [36], certain cheraviruses [19], and the majority of carlaviruses [37] are transmitted by aphids.…”

“…Regarding the viruses detected in A. carmichaeli, it is well-documented that CMV [38], ASGV [39,40], ChiVMV [41], PLRV [34], TVDV [33,42], and TSWV [38] have the ability to infect other economically important crops. The findings reported in this study suggest that the host range of these viruses is expanding.…”