Heterogeneity of xylem- and phloem-pole pericycle cells determines their competence for lateral root initiation. Outgrowth of lateral roots from competent phloem-pole pericycle cells allows them to forage for soil resources. Arbuscular mycorrhizal (AM) fungi play an important role in triggering the developmental program of their host roots. The present study aims to decipher the mechanisms of post-embryonic lateral root initiation and their interaction with AM fungi in maize.
Systemic histological and histochemical analyses of the lateral root defective mutants lateral rootless 1 (lrt1) and rootless with undetectable meristem 1 (rum1), revealed excessive cell wall lignification of phloem-pole pericycle cells in these mutants. We surveyed the transcriptome signatures of xylem- and phloem-pole pericycle cells of these mutants isolated during different stages of lateral root initiation by laser capture microdissection (LCM)-based RNA-seq. We demonstrated that cell wall biogenesis and organization are key processes controlling pericycle cell competence.
We further determined 12 inbred lines with disparate lateral root initiation frequency from the intermated B73-by-Mo17 (IBM) population. In general, lines with few lateral (FL) roots displayed higher cell wall lignification in pericycle cells. Comparative transcriptome profiling of manually dissected steles revealed that genes involved in ubiquitination and phenylpropanoid biosynthesis were exclusively enriched in FL lines.
To explore the role of AM fungi on lateral root initiation, we demonstrated that AM fungi (Rhizophagus irregularis) exclusively induce lateral root formation in FL lines and lrt1. Tissue-specific metabolome (GC-MS) and proteome (iTRAQ) analyses of lrt1, demonstrated that AM fungi induce lateral root formation by interfering with biosynthetesis of phenylpropanoid-related compounds. Moreover, the transcriptomes of isolated phloem-pole pericycle cells from AM-treated and non-AM-treated lrt1 plants showed diverse regulation of cell wall-related genes. Taken together, these results highlight a novel role of phenylpropanoid-related cell wall biosynthesis in lateral root initiation by interacting with AM fungi in maize.