Abstract Replant disease refers to the poor growth of trees when attempting to establish the same or related species on old orchard sites. The use of pre-plant Brassicaceae seed meal (SM) soil amendments in combination with apple replant disease-tolerant rootstock genotypes has been shown to be a promising strategy for the control of apple replant disease (ARD). However, optimizing microorganism-driven protection of apple roots from infection by multiple soil-borne pathogens requires a more comprehensive understanding of how “effective” vs. “ineffective” Brassicaceae seed meal × rootstock genotype disease control systems modulate the composition of rhizosphere microbial communities. In particular, the community of oomycetes associated with the apple rhizosphere remains relatively unexplored compared with bacteria and fungi. To address these issues, we sequenced the root associated bacterial, fungal, and oomycete communities of apple replant disease tolerant (G.210) and susceptible (M.26) rootstocks when grown in an orchard replant soil amended with different Brassicaceae seed meal formulations (Brassica juncea + Sinapis alba, B. juncea, and Brassica napus) previously shown to provide varying levels of replant disease control. Multiple microbial components were associated with observed growth differences between “effective” and “ineffective” disease control systems including the absolute abundance of Ilyonectria/Cylindrocarpon in fine root tissue. Amplicon sequencing provided a more detailed picture of the genetic diversity of oomycete groups in the apple rhizosphere than previously appreciated, and highlighted the variability in oomycete community structure between different rootstock × seed meal disease control systems. In Brassica juncea + Sinapis alba SM-structured rhizospheres, the ARD-tolerant rootstock (G.210) harbored higher relative abundances of Peronosporales with reduced potential to infect apple roots and incite replant disease (such as Peronospora destructor and P. acanthicum), whereas the Peronosporales community associated with the sensitive rootstock (M.26) was dominated by the ARD-specific pathogen Phytophthora cactorum. In addition, Brassica juncea + Sinapis alba SM-structured microbiomes were characterized by numerous bacterial and fungal taxa with the potential for biocontrol, biodegradation and bioremediation. Taken together, these results support the hypothesis that particular Brassicaceae SM soil amendments not only provide “effective” disease control, but also promote microbiomes which are likely to contribute to long-term orchard soil health in many other ways. Overall, this comprehensive analysis highlights the significance of the rootstock × seed meal interaction on bacterial, fungal, and oomycete communities within the apple rhizosphere of “effective” vs. “ineffective” disease control systems and the potential influence of these elements on the dynamics of apple replant disease.

中文翻译：

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同一土壤/植物系统中不同芸苔籽粕和砧木对苹果根际生物群落的综合分析

摘要 重植病害是指在旧果园场地上尝试建立相同或相关物种时树木生长不良。使用种植前十字花科种子粉 (SM) 土壤改良剂与苹果再植抗病砧木基因型相结合，已被证明是控制苹果再植病 (ARD) 的有前途的策略。然而，优化微生物驱动的苹果根部免受多种土壤传播病原体感染的保护需要更全面地了解“有效”与“无效”十字花科种子粉×砧木基因型疾病控制系统如何调节根际微生物群落的组成。特别是，与细菌和真菌相比，与苹果根际相关的卵菌群落仍然相对未开发。为了解决这些问题，我们对苹果再植抗病 (G.210) 和易感 (M.26) 砧木的根相关细菌、真菌和卵菌群落进行了测序、B. juncea 和 Brassica napus) 先前显示可提供不同水平的再植病害控制。多种微生物成分与观察到的“有效”和“无效”疾病控制系统之间的生长差异有关，包括细根组织中 Ilyonectria/Cylindrocarpon 的绝对丰度。扩增子测序提供了比以前认为的更详细的苹果根际卵菌群遗传多样性的图景，并强调了不同砧木×种粉病害控制系统之间卵菌群落结构的变异性。在芥菜 + 白芥菜 SM 结构的根际，耐 ARD 砧木 (G.210) 具有相对丰度较高的霜孢子目，其感染苹果根和引发再植病害的可能性较低（如霜霉病菌和 P. acanthicum），而与敏感砧木 (M.26) 相关的 Peronosporales 群落由 ARD 特异性病原体 Phytophthora cactorum 主导。此外，芥菜 + 白芥子 SM 结构的微生物组的特征是众多细菌和真菌类群，具有生物防治、生物降解和生物修复的潜力。综合起来，这些结果支持了这样的假设，即特定的十字花科 SM 土壤改良剂不仅可以提供“有效”的疾病控制，而且还可以促进微生物群落，这些微生物群落可能以许多其他方式促进果园土壤的长期健康。总体而言，这项综合分析强调了砧木 × 种粉相互作用对“有效”与“无效”疾病控制系统的苹果根际内细菌、真菌和卵菌群落的重要性，以及这些元素对细菌、真菌和卵菌群落的潜在影响。苹果再植病。