Cai Yanling, Wang Zhiqing, Wan Wei, Qi Jinfeng, Liu Xiao-Feng, Wang Yantao, Lyu Yaqing, Li Tao, Dong Suomeng, Huang Sanwen, Zhou Shaoqun
Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, Guangdong 518120, China.
State Key Laboratory of Resource Insects, Institute of Sericulture and Systems Biology, Southwest University, Chongqing 400715, China.
Plant Physiol. 2025 Mar 28;197(4). doi: 10.1093/plphys/kiaf112.
Late blight caused by Phytophthora infestans is a major threat to global potato and tomato production. Sustainable management of late blight requires the development of resistant crop cultivars. This process can be facilitated by high-throughput identification of functional genes involved in late blight pathogenesis. In this study, we generated a high-quality transcriptomic time-course dataset focusing on the initial 24 h of contact between P. infestans and 3 solanaceous plant species, tobacco (Nicotiana benthamiana), tomato (Solanum lycopersicum), and potato (Solanum tuberosum). Our results demonstrate species-specific transcriptional regulation in early stages of the infection. Transient silencing of putative RIBOSE-5-PHOSPHATE ISOMERASE and HMG-CoA REDUCTASE genes in N. benthamiana lowered plant resistance against P. infestans. Furthermore, heterologous expression of a putative tomato Golgi-localized nucleosugar transporter-encoding gene exacerbated P. infestans infection of N. benthamiana. In comparison, bioassays using transgenic tomato lines showed that the quantitative disease resistance genes were required but insufficient for late blight resistance; genetic knock-out of the susceptibility gene enhanced resistance. The same RNA-seq dataset was exploited to examine the transcriptional landscape of P. infestans and revealed host-specific gene expression patterns in the pathogen. This temporal transcriptomic diversity, in combination with genomic distribution features, identified the P. infestans IPI-B family GLYCINE-RICH PROTEINs as putative virulence factors that promoted disease severity or induced plant tissue necrosis when transiently expressed in N. benthamiana. These functional genes underline the effectiveness of functional gene-mining through a time-course dual RNA-seq approach and provide insight into the molecular interactions between solanaceous plants and P. infestans.
由致病疫霉引起的晚疫病是全球马铃薯和番茄生产的主要威胁。晚疫病的可持续管理需要培育抗病作物品种。高通量鉴定参与晚疫病发病机制的功能基因有助于这一过程。在本研究中，我们生成了一个高质量的转录组时间进程数据集，重点关注致病疫霉与3种茄科植物烟草（本氏烟草）、番茄（番茄）和马铃薯（马铃薯）接触的最初24小时。我们的结果表明，在感染早期存在物种特异性转录调控。本氏烟草中假定的5-磷酸核糖异构酶和HMG-CoA还原酶基因的瞬时沉默降低了植物对致病疫霉的抗性。此外，一个假定的番茄高尔基体定位的核苷糖转运蛋白编码基因的异源表达加剧了致病疫霉对本氏烟草的感染。相比之下，使用转基因番茄品系的生物测定表明，数量抗病基因是晚疫病抗性所必需的，但并不充分；感病基因的基因敲除增强了抗性。利用相同的RNA测序数据集来研究致病疫霉的转录图谱，并揭示了病原体中宿主特异性的基因表达模式。这种时间转录组多样性与基因组分布特征相结合，确定致病疫霉IPI-B家族富含甘氨酸的蛋白是假定的毒力因子，当在本氏烟草中瞬时表达时，可促进病害严重程度或诱导植物组织坏死。这些功能基因强调了通过时间进程双RNA测序方法进行功能基因挖掘的有效性，并为茄科植物与致病疫霉之间的分子相互作用提供了见解。
