Abstract

Microbes living in plant tissues—endophytes—are mainly studied in crop plants where they typically colonize the root apoplast. Trees—a large carbon source with a high capacity for photosynthesis—provide a variety of niches for endophytic colonization. We have earlier identified a new type of plant–endophyte interaction in buds of adult Scots pine, where Methylorubrum species live inside the meristematic cells. The endosymbiont Methylorubrum extorquens DSM13060 significantly increases needle and root growth of pine seedlings without producing plant hormones, but by aggregating around host nuclei. Here, we studied gene expression and metabolites of the pine host induced by M. extorquens DSM13060 infection. Malic acid was produced by pine to potentially boost M. extorquens colonization and interaction. Based on gene expression, the endosymbiont activated the auxin- and ethylene (ET)-associated hormonal pathways through induction of CUL1 and HYL1, and suppressed salicylic and abscisic acid signaling of pine. Infection by the endosymbiont had an effect on pine meristem and leaf development through activation of GLP1-7 and ALE2, and suppressed flowering, root hair and lateral root formation by downregulation of AGL8, plantacyanin, GASA7, COW1 and RALFL34. Despite of systemic infection of pine seedlings by the endosymbiont, the pine genes CUL1, ETR2, ERF3, HYL, GLP1-7 and CYP71 were highly expressed in the shoot apical meristem, rarely in needles and not in stem or root tissues. Low expression of MERI5, CLH2, EULS3 and high quantities of ononitol suggest that endosymbiont promotes viability and protects pine seedlings against abiotic stress. Our results indicate that the endosymbiont positively affects host development and stress tolerance through mechanisms previously unknown for endophytic bacteria, manipulation of plant hormone signaling pathways, downregulation of senescence and cell death-associated genes and induction of ononitol biosynthesis.

中文翻译：

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与分生组织相关的内共生体 Methylorubrum extorquens DSM13060 重新编程松树幼苗的发育和应激反应

摘要

生活在植物组织中的微生物——内生菌——主要在农作物中进行研究，它们通常在根质外体定殖。树木——一种具有高光合作用能力的大型碳源——为内生菌定植提供了多种生态位。我们早先在成年苏格兰松的芽中发现了一种新型的植物-内生菌相互作用，其中甲基红花属物种生活在分生细胞内。内共生体Methylorubrum extorquens DSM13060 在不产生植物激素的情况下，通过聚集在宿主细胞核周围显着增加松树幼苗的针和根生长。在这里，我们研究了由M. extorquens DSM13060 感染诱导的松树宿主的基因表达和代谢物。苹果酸是由松树产生的，以潜在地促进M. extorquens殖民化和互动。基于基因表达，内共生体通过诱导CUL1和HYL1激活生长素和乙烯 (ET) 相关的激素通路，并抑制松树的水杨酸和脱落酸信号传导。内共生菌感染通过激活GLP1-7和ALE2影响松树分生组织和叶片发育，并通过下调AGL8、车前蓝素、GASA7、COW1和RALFL34抑制开花、根毛和侧根形成。尽管内共生体对松树幼苗进行全身感染，但松树基因CUL1、ETR2、ERF3、HYL、GLP1-7和CYP71在茎尖分生组织中高度表达，很少在针叶中表达，而在茎或根组织中则没有。MERI5、CLH2、EULS3和大量 ononitol的低表达表明内共生菌促进了活力并保护松树幼苗免受非生物胁迫。我们的研究结果表明，内共生体通过以前未知的内生细菌机制、植物激素信号通路的操纵、衰老和细胞死亡相关基因的下调以及 ononitol 生物合成的诱导，对宿主发育和胁迫耐受性产生积极影响。