Reciprocal interactions between the sorghum root microbiome and the parasitic weed Striga hermonthica

The soil microbiome can protect plants against fungal and bacterial pathogens, nematodes, and insect pests. However, the impact of the soil microbiome on interactions between plants and parasitic weeds remains largely elusive. Here, susceptible sorghum accession was grown in 22 field soils infested with the root parasitic weed Striga hermonthica seeds. Significant variation in Striga incidence was observed across these soils. Gamma-irradiation of the most Striga-suppressive soil led to a considerable increase in Striga attachments, exemplifying the importance of the soil microbiome in disrupting the parasite's infection cycle. In the presence of the soil microbiome, the Striga susceptible sorghum genotype showed comparable performance to three Striga-resistant sorghum genotypes. This phenotype was lost upon elimination of the soil microbiome by gamma-irradiation. Joint probabilistic model-based analysis revealed that Striga substantially impacts the sorghum rhizosphere microbiome and growth. The sorghum rhizosphere mycobiome and bacteriome members strongly correlated with Striga attachment. Further analyses revealed that some members of the mycobiome were detected in the sorghum rhizosphere only upon challenge with Striga seeds. Subsequent profiling of the Striga seed microbiome and cultivation-based fungal isolation and characterization indicated that most of these fungal taxa detected in the sorghum rhizosphere originated from the Striga seeds. Interestingly, these fungi are characterized as major sorghum pathogens suggesting a potential partnership between the root parasitic weed Striga and fungal pathogens to invade their shared host. In conclusion, our results showed that the soil microbiome affects Striga infection and sorghum performance in a genotype-dependent manner and that the microbiome of Striga seeds determines, at least in part, the sorghum rhizosphere microbiome composition.

土壤微生物组（soil microbiome）可保护植物抵御真菌病原菌、细菌病原菌、线虫及虫害。然而，土壤微生物组对植物与寄生性杂草间互作的影响目前仍未完全明确。本研究将列当易感高粱种质（susceptible sorghum accession）种植于22份被寄生性杂草列当（Striga hermonthica）种子侵染的田间土壤中。结果显示，不同土壤的列当侵染率存在显著差异。对列当抑制效果最强的土壤进行γ辐照（gamma-irradiation）处理后，列当的附着量显著提升，这印证了土壤微生物组在干扰该寄生杂草侵染循环中的关键作用。在土壤微生物组存在的条件下，列当易感高粱基因型与3份抗列当高粱基因型的生长表现相当；而通过γ辐照去除土壤微生物组后，这一表型便不复存在。基于联合概率模型（joint probabilistic model）的分析表明，列当会显著影响高粱根际微生物组（rhizosphere microbiome）及其生长状况。高粱根际真菌群落（mycobiome）与细菌群落（bacteriome）的组成与列当附着量呈显著相关。进一步分析发现，部分真菌类群仅在受到列当种子侵染胁迫时，才会在高粱根际中被检测到。后续对列当种子微生物组的群落结构分析，以及基于培养的真菌分离与鉴定实验显示，高粱根际中检测到的这些真菌类群大多源自列当种子。值得注意的是，这些真菌被鉴定为主要的高粱病原菌，这暗示寄生性杂草列当与真菌病原菌可能存在潜在的协同侵染共享宿主的关系。综上，本研究结果表明，土壤微生物组会以基因型依赖的方式影响列当侵染及高粱生长表现，且列当种子的微生物组至少在一定程度上决定了高粱根际微生物组的组成。