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Local and systemic transcriptome and spliceome reprogramming induced by the root-knot nematode Meloidogyne incognita in tomato
Horticulture Research ( IF 7.6 ) Pub Date : 2024-07-24 , DOI: 10.1093/hr/uhae206 Selin Ozdemir 1 , Sarbottam Piya 1 , Valeria S Lopes-Caitar 1 , Nicole Coffey 1 , J Hollis Rice 1 , Tarek Hewezi 1
Horticulture Research ( IF 7.6 ) Pub Date : 2024-07-24 , DOI: 10.1093/hr/uhae206 Selin Ozdemir 1 , Sarbottam Piya 1 , Valeria S Lopes-Caitar 1 , Nicole Coffey 1 , J Hollis Rice 1 , Tarek Hewezi 1
Affiliation
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:
番茄根结线虫诱导的局部和全身转录组和剪接组重编程
根结线虫(Meloidogyne spp.)是广泛传播的根部寄生虫,可感染数千种维管植物。这些高度多食性的线虫与寄主植物进行复杂的相互作用,导致形成被称为虫瘿的结状结构,其个体发育仍然很大程度上未知。在这里,我们确定了南方巨贝在两个不同感染阶段的虫瘿和邻近根细胞中诱导的转录组变化和选择性剪接变异。南方根结线虫在番茄根部的瘿中和邻近细胞中引起了显着的转录组变化。在虫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,特别是在感染的早期阶段。转录组分析还表明,南方根结线虫对整个细胞周期过程进行严格控制,导致摄食部位倍性水平增加,并加速胆细胞的有丝分裂活动。选择性剪接分析表明南方根结线虫显着调节前体 mRNA 剪接,共鉴定出来自 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,并发现其影响虫瘿形成和线虫卵大量生产。总之,我们的数据为番茄中南方根结线虫诱导的转录组和剪接组重编程提供了前所未有的见解,涉及瘿个体发育和线虫寄生。
更新日期:2024-07-24
中文翻译:
番茄根结线虫诱导的局部和全身转录组和剪接组重编程
根结线虫(Meloidogyne spp.)是广泛传播的根部寄生虫,可感染数千种维管植物。这些高度多食性的线虫与寄主植物进行复杂的相互作用,导致形成被称为虫瘿的结状结构,其个体发育仍然很大程度上未知。在这里,我们确定了南方巨贝在两个不同感染阶段的虫瘿和邻近根细胞中诱导的转录组变化和选择性剪接变异。南方根结线虫在番茄根部的瘿中和邻近细胞中引起了显着的转录组变化。在虫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,特别是在感染的早期阶段。转录组分析还表明,南方根结线虫对整个细胞周期过程进行严格控制,导致摄食部位倍性水平增加,并加速胆细胞的有丝分裂活动。选择性剪接分析表明南方根结线虫显着调节前体 mRNA 剪接,共鉴定出来自 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,并发现其影响虫瘿形成和线虫卵大量生产。总之,我们的数据为番茄中南方根结线虫诱导的转录组和剪接组重编程提供了前所未有的见解,涉及瘿个体发育和线虫寄生。