Department of Plant Pathology and Weed Research, Agricultural Research Organization, The Volcani Institute, Rishon LeZion, Israel.
Gilat Research Center, Agricultural Research Organization, Negev, Israel.
Mol Plant Pathol. 2023 Aug;24(8):838-848. doi: 10.1111/mpp.13318. Epub 2023 Apr 21.
The tomato Tm-2 gene was considered to be one of the most durable resistance genes in agriculture, protecting against viruses of the Tobamovirus genus, such as tomato mosaic virus (ToMV) and tobacco mosaic virus (TMV). However, an emerging tobamovirus, tomato brown rugose fruit virus (ToBRFV), has overcome Tm-2 , damaging tomato production worldwide. Tm-2 encodes a nucleotide-binding leucine-rich repeat (NLR) class immune receptor that recognizes its effector, the tobamovirus movement protein (MP). Previously, we found that ToBRFV MP (MP ) enabled the virus to overcome Tm-2 -mediated resistance. Yet, it was unknown how Tm-2 remained durable against other tobamoviruses, such as TMV and ToMV, for over 60 years. Here, we show that a conserved cysteine (C68) in the MP of TMV (MP ) plays a dual role in Tm-2 activation and viral movement. Substitution of MP amino acid H67 with the corresponding amino acid in MP (C68) activated Tm-2 -mediated resistance. However, replacement of C68 in TMV and ToMV disabled the infectivity of both viruses. Phylogenetic and structural prediction analysis revealed that C68 is conserved among all Solanaceae-infecting tobamoviruses except ToBRFV and localizes to a predicted jelly-roll fold common to various MPs. Cell-to-cell and subcellular movement analysis showed that C68 is required for the movement of TMV by regulating the MP interaction with the endoplasmic reticulum and targeting it to plasmodesmata. The dual role of C68 in viral movement and Tm-2 immune activation could explain how TMV was unable to overcome this resistance for such a long period.
番茄 Tm-2 基因被认为是农业中最持久的抗性基因之一，可抵抗 Tobamovirus 属的病毒，如番茄花叶病毒（ToMV）和烟草花叶病毒（TMV）。然而，一种新兴的 Tobamovirus，即番茄褐色皱果病毒（ToBRFV），已经克服了 Tm-2，对全球的番茄生产造成了损害。Tm-2 编码一种核苷酸结合富含亮氨酸重复（NLR）类免疫受体，可识别其效应物，即 Tobamovirus 运动蛋白（MP）。此前，我们发现 ToBRFV MP（MP）使该病毒能够克服 Tm-2 介导的抗性。然而，尚不清楚 Tm-2 如何在 60 多年的时间里仍然对其他 Tobamovirus （如 TMV 和 ToMV）保持持久抗性。在这里，我们表明 TMV MP（MP）中的保守半胱氨酸（C68）在 Tm-2 激活和病毒运动中发挥双重作用。用 MP（C68）中相应的氨基酸取代 TMV MP 的氨基酸 H67 可激活 Tm-2 介导的抗性。然而，C68 的替换会使 TMV 和 ToMV 的感染性均丧失。系统发育和结构预测分析表明，除了 ToBRFV 之外，C68 在所有侵染茄科植物的 Tobamovirus 中均保守，位于各种 MPs 中预测的凝胶卷折叠结构域。细胞间和亚细胞运动分析表明，C68 通过调节 MP 与内质网的相互作用并将其靶向胞间连丝，从而对 TMV 的运动是必需的。C68 在病毒运动和 Tm-2 免疫激活中的双重作用可以解释为什么 TMV 在如此长的时间内无法克服这种抗性。
