The Tomato Brown Rugose Fruit Virus Movement Protein Overcomes Tm-2 Resistance in Tomato While Attenuating Viral...

Tomato brown rugose fruit virus is a new virus species in the Tobamovirus genus, causing substantial damage to tomato crops. Reports of recent tomato brown rugose fruit virus (ToBRFV) outbreaks from around the world indicate an emerging global epidemic. ToBRFV overcomes all tobamovirus resistances in tomato, including the durable Tm-2 resistance gene, which had been effective against multiple tobamoviruses. Here, we show that the ToBRFV movement protein (MP^ToBRFV) enables the virus to evade Tm-2 resistance. Transient expression of MP^ToBRFV failed to activate the Tm-2 resistance response. Replacement of the original MP sequence of tomato mosaic virus (ToMV) with MP^ToBRFV enabled this recombinant virus to infect Tm-2-resistant plants. Using hybrid protein analysis, we show that the elements required to evade Tm-2 are located between MP^ToBRFV amino acids 1 and 216 and not the C terminus, as previously assumed. Analysis of ToBRFV systemic infection in tomato revealed that ToBRFV spreads more slowly compared with ToMV. Interestingly, replacement of tobacco mosaic virus (TMV) and ToMV MPs with MP^ToBRFV caused an attenuation of systemic infection of both viruses. Cell-to-cell movement analysis showed that MP^ToBRFV moves less effectively compared with the TMV MP (MP^TMV). These findings suggest that overcoming Tm-2 is associated with attenuated MP function. This may explain the high durability of Tm-2 resistance, which had remained unbroken for over 60 years.[Formula: see text] Copyright © 2021 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.