In terrestrial ecosystems, plant leaves provide the largest biological habitat for highly diverse microbial communities, known as the phyllosphere microbiota. However, the underlying mechanisms of host-driven assembly of these ubiquitous communities remain largely elusive. Here, we conduct a large-scale and in-depth assessment of the rice phyllosphere microbiome aimed at identifying specific host-microbe links. A genome-wide association study reveals a strong association between the plant genotype and members of four bacterial orders, Pseudomonadales, Burkholderiales, Enterobacterales and Xanthomonadales. Some of the associations are specific to a distinct host genomic locus, pathway or even gene. The compound 4-hydroxycinnamic acid (4-HCA) is identified as the main driver for enrichment of bacteria belonging to Pseudomonadales. 4-HCA can be synthesized by the host plant’s OsPAL02 from the phenylpropanoid biosynthesis pathway. A knockout mutant of OsPAL02 results in reduced Pseudomonadales abundance, dysbiosis of the phyllosphere microbiota and consequently higher susceptibility of rice plants to disease. Our study provides a direct link between a specific plant metabolite and rice phyllosphere homeostasis opening possibilities for new breeding strategies.

在陆地生态系统中，植物叶子为高度多样化的微生物群落（称为叶际微生物群）提供了最大的生物栖息地。然而，这些无处不在的群落的宿主驱动组装的潜在机制在很大程度上仍然难以捉摸。在这里，我们对水稻叶际微生物组进行了大规模和深入的评估，旨在识别特定的宿主-微生物联系。一项全基因组关联研究揭示了植物基因型与四个细菌目（假单胞菌目、伯克霍尔德菌目、肠杆菌目和黄单胞菌目）的成员之间存在很强的关联。一些关联是特定于不同的宿主基因组位点、通路甚至基因的。化合物 4-羟基肉桂酸 （4-HCA） 被确定为属于假单胞菌的细菌富集的主要驱动因素。4-HCA 可由寄主植物的 OsPAL02 从苯丙烷生物合成途径合成。OsPAL02 的敲除突变体导致假单胞菌丰度降低，叶状细胞微生物群失调，因此水稻植物对疾病的易感性更高。我们的研究提供了特定植物代谢物与水稻叶际稳态之间的直接联系，为新的育种策略提供了可能性。