Prigigallo Maria Isabella, Picciotti Ugo, Bubici Giovanni
Istituto per la Protezione Sostenibile delle Piante, Consiglio Nazionale delle Ricerche, via Amendola 165/A, 70126, Bari, Italy.
Sci Rep. 2025 Jan 29;15(1):3630. doi: 10.1038/s41598-025-88028-x.
Tomato spotted wilt virus (TSWV; Orthotospovirus tomatomaculae) is one of the major horticultural threats due to its worldwide distribution and broad host range. In Italy, TSWV is widely spread in tomato (Solanum lycopersicum) crops and causes severe yield losses. In the last decades, several tomato varieties carrying the Sw-5b gene for resistance to TSWV have been released. We investigated the interaction between Sw-5b-carrying tomatoes and Sw5-Resistance-Breaking (SRB) TSWV to elucidate the molecular mechanisms underlying resistance breakage. Transcriptome sequencing (RNA-Seq) was used to analyze 18 tomato leaf samples collected from a field crop naturally infected by SRB TSWV in Italy. An increase in virus accumulation level in leaf tissues (titer) resulted in a higher number of differentially expressed genes (DEGs), ranging from 33 to 44% of the whole transcriptome, when the samples with the lowest and the highest virus titer were compared to the asymptomatic sample, respectively. Photosynthesis and protein biosynthesis were the main down-regulated biological processes, while enzyme families such as oxidoreductases and transferases, genes related to the response to biotic stimuli, solute transport, and vesicle trafficking were overall up-regulated. Remarkably, the expression of around 45% of genes (ca. 14000) of the whole transcriptome was significantly (P < 0.05) correlated (positively or negatively) to the virus titer, and in 6% of cases (about 2000 genes) the correlation was high (i.e., absolute value of R > 0.85). This phenomenon was also verified on 15 genes by a quantitative reverse transcription PCR assay on a greenhouse experiment with a different Sw-5b-tomato variety artificially inoculated with another SRB TSWV strain. In conclusion, the tomato transcriptome was considerably rearranged upon TSWV infection, with deregulation of photosynthesis, protein biosynthesis, and induction of defense pathways. Finally, this research demonstrated that the magnitude of transcriptional changes was proportional to the virus accumulation level in the leaves.
番茄斑萎病毒（TSWV；番茄斑萎正番茄病毒）是主要的园艺威胁之一，因其在全球范围内分布且寄主范围广泛。在意大利，TSWV在番茄（Solanum lycopersicum）作物中广泛传播，导致严重的产量损失。在过去几十年里，已推出了几个携带Sw-5b基因以抵抗TSWV的番茄品种。我们研究了携带Sw-5b的番茄与Sw5抗性破除（SRB）TSWV之间的相互作用，以阐明抗性破除背后的分子机制。转录组测序（RNA-Seq）用于分析从意大利一块自然感染SRB TSWV的田间作物中采集的18个番茄叶片样本。当将病毒滴度最低和最高的样本分别与无症状样本进行比较时，叶片组织中病毒积累水平（滴度）的增加导致差异表达基因（DEG）数量增加，范围为整个转录组的33%至44%。光合作用和蛋白质生物合成是主要下调的生物学过程，而氧化还原酶和转移酶等酶家族、与生物刺激反应相关的基因、溶质转运和囊泡运输总体上调。值得注意的是，整个转录组中约45%的基因（约14000个）的表达与病毒滴度显著（P < 0.05）相关（正相关或负相关），在6%的情况下（约2000个基因）相关性很高（即R的绝对值> 0.85）。在温室实验中，用另一种SRB TSWV菌株人工接种不同的携带Sw-5b的番茄品种，通过定量逆转录PCR分析对15个基因也验证了这一现象。总之，TSWV感染后番茄转录组发生了相当大的重排，光合作用失调、蛋白质生物合成受影响，并诱导了防御途径。最后，这项研究表明转录变化的程度与叶片中的病毒积累水平成正比。
