Root-knot nematodes (Meloidogyne spp.) are widely spread root parasites that infect thousands of vascular plant species. These highly polyphagous nematodes engage in sophisticated interactions with host plants that results in the formation of knot-like structures known as galls whose ontogeny remains largely unknown. Here, we determined transcriptome changes and alternative splicing variants induced by Megalaima incognita in galls and neighboring root cells at two distinct infective stages. M. incognita induced substantial transcriptome changes in tomato roots both locally in galls and systemically in neighboring cells. A considerable parallel regulation of gene expression in galls and neighboring cells were detected, indicative of effective intercellular communications exemplified by suppression of basal defense responses particularly during the early stage of infection. The transcriptome analysis also revealed that M. incognita exerts a tight control over the cell cycle process as a whole that results in an increase of ploidy levels in the feeding sites and accelerated mitotic activity of the gall cells. Alternative splicing analysis indicated that M. incognita significantly modulates pre-mRNA splicing as a total of 9064 differentially spliced events from 2898 genes were identified where intron retention and exon skipping events were largely suppressed. Furthermore, a number of differentially spliced events were functionally validated using transgenic hairy root system and found to impact gall formation and nematode egg mass production. Together, our data provide unprecedented insights into the transcriptome and spliceome reprogramming induced by M. incognita in tomato with respect to gall ontogeny and nematode parasitism.

中文翻译：

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番茄根结线虫 Meloidogyne incognita 诱导的局部和系统转录组和剪接组重编程


根结线虫 （Meloidogyne spp.） 是广泛传播的根寄生虫，可感染数千种维管植物物种。这些高度多食性线虫与寄主植物进行复杂的相互作用，导致形成称为瘿的结状结构，其个体发育在很大程度上仍然未知。在这里，我们确定了在两个不同的感染阶段，Megalaima incognita 在瘿和邻近根细胞中诱导的转录组变化和可变剪接变异。M. incognita 在番茄瘿根中局部和邻近细胞中诱导了番茄根的显着转录组变化。在瘿和邻近细胞中检测到基因表达的相当大的平行调节，表明有效的细胞间通讯，例如抑制基础防御反应，尤其是在感染的早期阶段。转录组分析还显示，M. incognita 对整个细胞周期过程施加严格控制，导致摄食部位倍性水平增加和胆细胞有丝分裂活性加速。选择性剪接分析表明，M. incognita 显着调节前 mRNA 剪接，因为总共鉴定了来自 2898 个基因的 9064 个差异剪接事件，其中内含子保留和外显子跳跃事件在很大程度上受到抑制。此外，使用转基因毛状根系统对许多差异剪接事件进行了功能验证，并发现会影响瘿形成和线虫卵的大量生产。总之，我们的数据为番茄中 M. incognita 诱导的转录组和剪接组重编程在瘿个体发育和线虫寄生方面提供了前所未有的见解。