Abstract
Research on the interaction between the non-nodule-forming bacterial endophytes and their host plants is still in its infancy. Especially the understanding of plant control mechanisms which govern endophytic colonization is very limited. The current study sets out to determine which hormonal signaling pathway controls endophytic colonization in rice, and whether the mechanisms deviate for a pathogen. The endophyte Azoarcus olearius BH72—rice model was used to investigate root responses to endophytes in comparison to the recently established pathosystem of rice blight Xanthomonas oryzae pv. oryzae PXO99 (Xoo) in flooded roots. In the rice root transcriptome, 523 or 664 genes were found to be differentially expressed in response to Azoarcus or Xoo colonization, respectively; however, the response was drastically different, with only 6% of the differentially expressed genes (DEGs) overlapping. Overall, Xoo infection induced a much stronger defense reaction than Azoarcus colonization, with the latter leading to down-regulation of many defense related DEGs. Endophyte-induced DEGs encoded several enzymes involved in phytoalexin biosynthesis, ROS (reactive oxygen species) production, or pathogenesis-related (PR) proteins. Among putative plant markers related to signal transduction pathways modulated exclusively during Azoarcus colonization, none overlapped with previously published DEGs identified for another rice endophyte, Azospirillum sp. B510. This suggests a large variation in responses of individual genotypic combinations. Interestingly, the DEGs related to jasmonate (JA) signaling pathway were found to be consistently activated by both beneficial endophytes. In contrast, the salicylate (SA) pathway was activated only in roots infected by the pathogen. To determine the impact of SA and JA production on root colonization by the endophyte and the pathogen, rice mutants with altered hormonal responses were employed: mutant cpm2 deficient in jasmonate synthesis, and RNA interference (RNAi) knockdown lines of NPR1 decreased in salicylic acid-mediated defense responses (NPR1-kd). Only in cpm2, endophytic colonization of Azoarcus was significantly increased, while Xoo colonization was not affected. Surprisingly, NPR1-kd lines showed slightly decreased colonization by Xoo, contrary to published results for leaves. These outcomes suggest that JA but not SA signaling is involved in controlling the Azoarcus endophyte density in roots and can restrict internal root colonization, thereby shaping the beneficial root microbiome.
Highlights
For land plants the primary site of interactions with microbes are roots; here the tissues commonly harbor the largest numbers of microbes (Reinhold-Hurek et al, 2015)
The high density of bacterial colonization calls for a reduced sensitivity of roots toward microbial molecules and of defense responses, which may account for deviating hormonal responses in below- and above-ground tissues
Different panels of host gene transcription are induced during root colonization by beneficial or detrimental microbes (Plett and Martin, 2018)
Summary
For land plants the primary site of interactions with microbes are roots; here the tissues commonly harbor the largest numbers of microbes (Reinhold-Hurek et al, 2015). Among the root and rhizosphere microbes, endophytic bacteria are expected to have a tight interaction with their host plant. They reside within the living tissue of a plant without substantively harming it, in a symptomless association which remained for a long time undetected. Endophytic bacteria are of high interest to study fundamental questions of molecular interactions but are a mostly untapped reservoir for agro-biotechnological applications, e.g., for improvement of plant growth and health (Berendsen et al, 2012; Khare et al, 2018), phytoremediation (Barac et al, 2004), or as biofertilizer
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