Virus-virus interactions alter the mechanical transmissibility and host range of begomoviruses

Ho-Hsiung Chang; Deri Gustian; Chung-Jan Chang; Fuh-Jyh Jan

doi:10.3389/fpls.2023.1092998

Virus-virus interactions alter the mechanical transmissibility and host range of begomoviruses

Front Plant Sci. 2023 Jun 2:14:1092998. doi: 10.3389/fpls.2023.1092998. eCollection 2023.

Authors

Ho-Hsiung Chang¹, Deri Gustian¹, Chung-Jan Chang², Fuh-Jyh Jan^{1

3}

Affiliations

¹ Department of Plant Pathology, National Chung Hsing University, Taichung, Taiwan.
² Department of Plant Pathology, University of Georgia, Griffin, GA, United States.
³ Advanced Plant and Food Crop Biotechnology Center, National Chung Hsing University, Taichung, Taiwan.

Abstract

Introduction: Begomoviruses are mainly transmitted by whiteflies. However, a few begomoviruses can be transmitted mechanically. Mechanical transmissibility affects begomoviral distribution in the field.

Materials and methods: In this study, two mechanically transmissible begomoviruses, tomato leaf curl New Delhi virus-oriental melon isolate (ToLCNDV-OM) and tomato yellow leaf curl Thailand virus (TYLCTHV), and two nonmechanically transmissible begomoviruses, ToLCNDV-cucumber isolate (ToLCNDV-CB) and tomato leaf curl Taiwan virus (ToLCTV), were used to study the effects of virus-virus interactions on mechanical transmissibility.

Results: Nicotiana benthamiana and host plants were coinoculated through mechanical transmission with inoculants derived from plants that were mix-infected or inoculants derived from individually infected plants, and the inoculants were mixed immediately before inoculation. Our results showed that ToLCNDV-CB was mechanically transmitted with ToLCNDV-OM to N. benthamiana, cucumber, and oriental melon, whereas ToLCTV was mechanically transmitted with TYLCTHV to N. benthamiana and tomato. For crossing host range inoculation, ToLCNDV-CB was mechanically transmitted with TYLCTHV to N. benthamiana and its nonhost tomato, while ToLCTV with ToLCNDV-OM was transmitted to N. benthamiana and its nonhost oriental melon. For sequential inoculation, ToLCNDV-CB and ToLCTV were mechanically transmitted to N. benthamiana plants that were either preinfected with ToLCNDV-OM or TYLCTHV. The results of fluorescence resonance energy transfer analyses showed that the nuclear shuttle protein of ToLCNDV-CB (CBNSP) and the coat protein of ToLCTV (TWCP) localized alone to the nucleus. When coexpressed with movement proteins of ToLCNDV-OM or TYLCTHV, CBNSP and TWCP relocalized to both the nucleus and the cellular periphery and interacted with movement proteins.

Discussion: Our findings indicated that virus-virus interactions in mixed infection circumstances could complement the mechanical transmissibility of nonmechanically transmissible begomoviruses and alter their host range. These findings provide new insight into complex virus-virus interactions and will help us to understand the begomoviral distribution and to reevaluate disease management strategies in the field.

Keywords: begomovirus; host range; mechanical transmissibility; movement protein; virus-virus interaction.

Grants and funding

This work was supported by grants from the Ministry of Science and Technology (MOST 108-2313-B-005-034-MY3 and 110-2313-B-005-012-MY3), Executive Yuan, Taiwan.