Botanical Institute and Cluster of Excellence on Plant Sciences (CEPLAS), BioCenter, University of Cologne, Zuelpicher Str. 47a, Cologne, 50674, Germany.
Center for Familial Breast and Ovarian Cancer, Medical Faculty, University Hospital Cologne, University of Cologne, Cologne, NRW, 50931, Germany.
New Phytol. 2018 Mar;217(4):1681-1695. doi: 10.1111/nph.14960. Epub 2018 Jan 4.
The biotrophic fungus Ustilago maydis causes smut disease on maize (Zea mays), which is characterized by immense plant tumours. To establish disease and reprogram organ primordia to tumours, U. maydis deploys effector proteins in an organ-specific manner. However, the cellular contribution to leaf tumours remains unknown. We investigated leaf tumour formation at the tissue- and cell type-specific levels. Cytology and metabolite analysis were deployed to understand the cellular basis for tumourigenesis. Laser-capture microdissection was performed to gain a cell type-specific transcriptome of U. maydis during tumour formation. In vivo visualization of plant DNA synthesis identified bundle sheath cells as the origin of hyperplasic tumour cells, while mesophyll cells become hypertrophic tumour cells. Cell type-specific transcriptome profiling of U. maydis revealed tailored expression of fungal effector genes. Moreover, U. maydis See1 was identified as the first cell type-specific fungal effector, being required for induction of cell cycle reactivation in bundle sheath cells. Identification of distinct cellular mechanisms in two different leaf cell types and of See1 as an effector for induction of proliferation of bundle sheath cells are major steps in understanding U. maydis-induced tumour formation. Moreover, the cell type-specific U. maydis transcriptome data are a valuable resource to the scientific community.
玉米黑粉菌（Ustilago maydis）是一种生物寄生性真菌，可引起玉米（Zea mays）的黑粉病，其特征是形成巨大的植物肿瘤。为了在器官特异性方式下引发疾病并重新编程器官原基为肿瘤，玉米黑粉菌会部署效应蛋白。然而，对于叶片肿瘤的细胞贡献仍不清楚。我们在组织和细胞类型特异性水平上研究了叶片肿瘤的形成。通过细胞学和代谢物分析来了解肿瘤发生的细胞基础。通过激光捕获显微切割技术，我们在肿瘤形成过程中获得了玉米黑粉菌的细胞类型特异性转录组。植物 DNA 合成的体内可视化鉴定出维管束鞘细胞是增生性肿瘤细胞的起源，而叶肉细胞则成为肥大的肿瘤细胞。玉米黑粉菌的细胞类型特异性转录组分析揭示了真菌效应基因的定制表达。此外，还鉴定出 See1 是第一个细胞类型特异性真菌效应因子，它是诱导维管束鞘细胞细胞周期重新激活所必需的。在两种不同的叶片细胞类型中发现不同的细胞机制，以及 See1 作为诱导维管束鞘细胞增殖的效应因子，是理解玉米黑粉菌诱导肿瘤形成的重要步骤。此外，细胞类型特异性的玉米黑粉菌转录组数据是科学界的宝贵资源。
