Ray Swayamjit, Murad Tyseen, Arena Gabriella D, Arshad Kanza, Arendsee Zebulun, Herath Venura, Whitham Steven A, Casteel Clare L
Department of Plant Pathology and Plant-Microbe Biology, Cornell University, 309 Plant Science Building, Ithaca, NY, 14853, USA.
Laboratório de Biologia Molecular Aplicada, Instituto Biológico de São Paulo, São Paulo, 04014-002, Brazil.
BMC Plant Biol. 2025 Apr 2;25(1):411. doi: 10.1186/s12870-025-06411-2.
Plant viruses both trigger and inhibit host plant defense responses, including defenses that target their insect vectors, such as aphids. Turnip mosaic viru (TuMV) infection and its protein, NIa-Pro (nuclear inclusion protease a), suppress aphid-induced plant defenses, however the mechanisms of this suppression are still largely unknown. In this study, we determined that NIa-Pro's protease activity is required to increase aphid performance on host plants and that 40 transcripts with predicted NIa-Pro cleavage sequences are regulated in Arabidopsis plants challenged with aphids and/or virus compared to healthy controls. One of the candidates, MEDIATOR 16 (MED16), regulates the transcription of ethylene (ET)/jasmonic acid (JA)-dependent defense responses against necrotrophic pathogens. We show that a nuclear localization signal is removed from MED16 by specific proteolytic cleavage in virus-infected plants and in plants overexpressing NIa-Pro in the presence of aphids. Although some cleavage was occasionally detected in the absence of virus infection, it occurred at a much higher rate in plants that were virus-infected or overexpressing NIa-Pro, especially when aphids were also present. This suggests MED16 functions in the nucleus may be impacted in virus infected plants. Consistent with this, induction of the MED16-dependent transcript of PLANT DEFENSIN 1.2 (PDF1.2), was reduced in virus-infected plants and in plants expressing NIa-Pro compared to controls, but not in plants expressing NIa-Pro C151A that lacks its protease activity. Finally, we show the performance of both the virus and the aphid vector was enhanced on med16 mutant Arabidopsis compared to controls. Overall, this study demonstrates MED16 regulates defense responses against both the virus and the aphid and provides insights into the mechanism by which TuMV suppresses anti-virus and anti-herbivore defenses.
植物病毒既能触发也能抑制宿主植物的防御反应，包括针对其昆虫传播介体（如蚜虫）的防御反应。芜菁花叶病毒（TuMV）感染及其蛋白NIa-Pro（核内含物蛋白酶a）会抑制蚜虫诱导的植物防御反应，然而这种抑制机制在很大程度上仍不清楚。在本研究中，我们确定NIa-Pro的蛋白酶活性是提高蚜虫在宿主植物上生存能力所必需的，并且与健康对照相比，在受到蚜虫和/或病毒攻击的拟南芥植物中，40个具有预测NIa-Pro切割序列的转录本受到调控。其中一个候选基因MEDIATOR 16（MED16），调节针对坏死营养型病原体的乙烯（ET）/茉莉酸（JA）依赖性防御反应的转录。我们发现，在病毒感染的植物和在有蚜虫存在的情况下过表达NIa-Pro的植物中，MED16通过特异性蛋白水解切割去除了核定位信号。虽然在没有病毒感染的情况下偶尔也能检测到一些切割，但在病毒感染或过表达NIa-Pro的植物中，尤其是在也有蚜虫存在的情况下，切割发生率要高得多。这表明MED16在细胞核中的功能可能在病毒感染的植物中受到影响。与此一致的是，与对照相比，病毒感染的植物和表达NIa-Pro的植物中，由MED16依赖性转录的植物防御素1.2（PDF1.2）的诱导水平降低，但在表达缺乏蛋白酶活性的NIa-Pro C151A的植物中没有降低。最后，我们发现与对照相比，在med16突变体拟南芥上，病毒和蚜虫介体二者的生存能力均增强。总体而言，本研究表明MED16调节针对病毒和蚜虫的防御反应，并为TuMV抑制抗病毒和抗食草动物防御的机制提供了见解。
