School of Biosciences, University of Sheffield, Western Bank, Sheffield, S10 2TN, UK.
Present address: Department of Cell and Systems Biology, University of Toronto, Toronto, ON, M5S 3B2, Canada.
BMC Plant Biol. 2024 Apr 6;24(1):251. doi: 10.1186/s12870-024-04935-7.
Many parasitic plants of the genera Striga and Cuscuta inflict huge agricultural damage worldwide. To form and maintain a connection with a host plant, parasitic plants deploy virulence factors (VFs) that interact with host biology. They possess a secretome that represents the complement of proteins secreted from cells and like other plant parasites such as fungi, bacteria or nematodes, some secreted proteins represent VFs crucial to successful host colonisation. Understanding the genome-wide complement of putative secreted proteins from parasitic plants, and their expression during host invasion, will advance understanding of virulence mechanisms used by parasitic plants to suppress/evade host immune responses and to establish and maintain a parasite-host interaction.
We conducted a comparative analysis of the secretomes of root (Striga spp.) and shoot (Cuscuta spp.) parasitic plants, to enable prediction of candidate VFs. Using orthogroup clustering and protein domain analyses we identified gene families/functional annotations common to both Striga and Cuscuta species that were not present in their closest non-parasitic relatives (e.g. strictosidine synthase like enzymes), or specific to either the Striga or Cuscuta secretomes. For example, Striga secretomes were strongly associated with 'PAR1' protein domains. These were rare in the Cuscuta secretomes but an abundance of 'GMC oxidoreductase' domains were found, that were not present in the Striga secretomes. We then conducted transcriptional profiling of genes encoding putatively secreted proteins for the most agriculturally damaging root parasitic weed of cereals, S. hermonthica. A significant portion of the Striga-specific secretome set was differentially expressed during parasitism, which we probed further to identify genes following a 'wave-like' expression pattern peaking in the early penetration stage of infection. We identified 39 genes encoding putative VFs with functions such as cell wall modification, immune suppression, protease, kinase, or peroxidase activities, that are excellent candidates for future functional studies.
Our study represents a comprehensive secretome analysis among parasitic plants and revealed both similarities and differences in candidate VFs between Striga and Cuscuta species. This knowledge is crucial for the development of new management strategies and delaying the evolution of virulence in parasitic weeds.
许多列当属和菟丝子属的寄生植物在全球范围内造成了巨大的农业损失。为了与宿主植物形成和维持连接，寄生植物会部署毒力因子（Virulence Factors，VFs），这些因子与宿主生物学相互作用。它们拥有一个分泌组，代表了从细胞中分泌的蛋白质的总和，与其他植物寄生虫（如真菌、细菌或线虫）一样，一些分泌蛋白代表了对成功定殖宿主至关重要的 VFs。了解寄生植物的全基因组分泌蛋白组成及其在入侵宿主时的表达情况，将有助于我们理解寄生植物用于抑制/逃避宿主免疫反应、建立和维持寄生-宿主相互作用的毒力机制。
我们对根寄生植物（列当属）和茎寄生植物（菟丝子属）的分泌组进行了比较分析，以预测候选 VFs。通过同源簇聚类和蛋白质结构域分析，我们鉴定了列属和菟丝子属物种共有的基因家族/功能注释，这些基因家族/功能注释在它们最接近的非寄生亲属中不存在（例如，strictosidine synthase 样酶），或者是列属或菟丝子属分泌组特有的。例如，列当属的分泌组与“PAR1”蛋白结构域强烈相关。这些结构域在菟丝子属的分泌组中很少见，但存在大量的“GMC 氧化还原酶”结构域，而这些结构域在列当属的分泌组中不存在。然后，我们对最具农业破坏性的谷类根寄生杂草列当的编码推定分泌蛋白的基因进行了转录谱分析。在寄生过程中，列当属特有的分泌组中有很大一部分基因表达差异显著，我们进一步探测了这些基因，以鉴定在感染早期穿透阶段表达峰值呈“波浪状”的基因。我们鉴定了 39 个编码推定 VFs 的基因，这些基因具有细胞壁修饰、免疫抑制、蛋白酶、激酶或过氧化物酶等功能，是未来功能研究的优秀候选基因。
我们的研究代表了寄生植物之间的全面分泌组分析，揭示了列当属和菟丝子属物种之间候选 VFs 的相似性和差异。这一知识对于制定新的管理策略和延缓寄生杂草毒力的进化至关重要。
