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Summary: The plant hormone gibberellin (GA) is required at different stages of legume nodule development, with its spatiotemporal distribution tightly regulated. Transcriptomic and bioinformatic analyses established that several key GA biosynthesis and catabolism enzyme encoding genes are critical to soybean (Glycine max) nodule formation.We examined the expression of several GA oxidase genes and used a Förster resonance energy transfer‐based GA biosensor to determine the bioactive GA content of roots inoculated with DsRed‐labelled Bradyrhizobium diazoefficiens. We manipulated the level of GA by genetically disrupting the expression of GA oxidase genes. Moreover, exogenous treatment of soybean roots with GA3 induced the expression of key nodulation genes and altered infection thread and nodule phenotypes.GmGA20ox1a, GmGA3ox1a, and GmGA2ox1a are upregulated in soybean roots inoculated with compatible B. diazoefficiens. GmGA20ox1a expression is predominately localized to the transient meristem of soybean nodules and coincides with the spatiotemporal distribution of bioactive GA occurring throughout nodule organogenesis. GmGA2ox1a exhibits a nodule vasculature‐specific expression pattern, whereas GmGA3ox1a can be detected throughout the nodule and root. Disruptions in the level of GA resulted in aberrant rhizobia infection and reduced nodule numbers.Collectively, our results establish a central role for GAs in root hair infection by symbiotic rhizobia and in nodule organogenesis. [ABSTRACT FROM AUTHOR]

Legumes control their nodule numbers through the autoregulation of nodulation (AON). Rhizobia infection stimulates the production of root‐derived CLE peptide hormones that are translocated to the shoot where they regulate a new signal. We used soybean to demonstrate that this shoot‐derived signal is miR2111, which is transported via phloem to the root where it targets transcripts of Too Much Love (TML), a negative regulator of nodulation. Shoot perception of rhizobia‐induced CLE peptides suppresses miR2111 expression, resulting in TML accumulation in roots and subsequent inhibition of nodule organogenesis. Feeding synthetic mature miR2111 via the petiole increased nodule numbers per plant. Likewise, elevating miR2111 availability by over‐expression promoted nodulation, while target mimicry of TML induced the opposite effect on nodule development in wild‐type plants and alleviated the supernodulating and stunted root growth phenotypes of AON‐defective mutants. Additionally, in non‐nodulating wild‐type plants, ectopic expression of miR2111 significantly enhanced lateral root emergence with a decrease in lateral root length and average root diameter. In contrast, hairy roots constitutively expressing the target mimic construct exhibited reduced lateral root density. Overall, these findings demonstrate that miR2111 is both the critical shoot‐to‐root factor that positively regulates root nodule development and also acts to shape root system architecture. Our work used soybean to demonstrate that miR2111 is the critical shoot‐to‐root factor that positively regulates root nodule formation in the autoregulation of nodulation pathway and also acts to shape root system architecture via orchestrating the degree of root branching, as well as the length and thickness of lateral roots. This project was initially driven by the incentive to pinpoint the mobile factor that mediates the communication between shoots and roots in the downward signalling pathway of AON. We then aimed to address if miR2111 provides a genetic link for the concomitant aberrant root growth and supernodulation phenotypes seen in those AON‐defective mutants. [ABSTRACT FROM AUTHOR]