No Home without Hormones: How Plant Hormones Control Legume Nodule Organogenesis

Abstract

The establishment of symbiotic nitrogen fixation requires the coordination of both nodule development and infection events. Despite the evolution of a variety of anatomical structures, nodule organs serve a common purpose in establishing a localized area that facilitates efficient nitrogen fixation. As in all plant developmental processes, the establishment of a new nodule organ is regulated by plant hormones. During nodule initiation, regulation of plant hormone signaling is one of the major targets of symbiotic signaling. We review the role of major developmental hormones in the initiation of the nodule organ and argue that the manipulation of plant hormones is a key requirement for engineering nitrogen fixation in non-legumes as the basis for improved food security and sustainability.

Keywords: hormones; legume; nitrogen fixation; nodule; symbiosis.

Figure 1

Nodule Development and Signaling Pathways. (A) Comparison of the initiation sites and structures of lateral roots and several major nodule types. The first cell division (red) can vary within and between nodule types from the pericycle to the outer cortex. Vascular patterning and persistence of meristematic cells also differ. (B) Major events during nodule organogenesis. Development of a determinate-type nodule as found in the model legume Lotus japonicus is exemplified. The establishment of cortical cytokinin (CK) and auxin signaling domains are major requirements for pre-infection signaling to stimulate nodule initiation and growth. NF, Nod factor; ET, ethylene; IT, Infection thread; IAA, indole-3-acetic acid (auxin).

Figure 2

CK Biosynthesis, Metabolism, and Signaling. Intensity of signaling output at different developmental stages is depicted based on reporter studies, transcriptome experiments, and signaling mutant phenotypes. Following the perception of rhizobia, CK level and signaling is rapidly induced in the cortex. Cortical CK remains increased during nodule initiation and growth, while surrounding tissue and epidermal responses are restricted. Mature nodules retain CK signaling in the vasculature, with reduced signaling in infected cells. Core biosynthesis, metabolism, and signaling components are depicted at the right, along with species-specific components, where known. NF-induced/repressed components are indicated with a brown arrow (up or down, respectively).

Figure 3

Auxin Biosynthesis, Metabolism, and Signaling. Intensity of signaling output at different developmental stages is depicted based on reporter studies, transcriptome experiments, and signaling mutant phenotypes. Following rhizobia perception, auxin levels increase, and signaling output is initiated in the epidermis. Auxin biosynthesis and transport regulation contribute to increased signaling associated with nodule initiation and growth and are maintained until nodule maturity. Generally known biosynthesis, metabolism, and signaling components are depicted at the right with species-specific components, where known. A dotted line indicates IAA transport by AUX/LAX/PIN proteins. Factors through which NIN induces YUC are marked with a triangle. ARFs acting as negative regulators of nodulation are depicted with asterisks. NF-induced/repressed components are indicated with a brown arrow (up or down, respectively).

Figure 4

Ethylene Biosynthesis, Metabolism, and Signaling. Following perception of rhizobia, ethylene levels and signaling are rapidly induced; however, precise localization has not been achieved, and signaling intensity at different developmental stages is depicted based on mutant phenotypes, indicating roles at all stages of nodule development and in nodule positioning. Core biosynthesis, metabolism, and signaling components are depicted in black at the right, together with species-specific components, where known. NF-induced/repressed components are indicated with a brown arrow (up or down, respectively).

Figure 5

GA Biosynthesis, Metabolism, and Signaling. Intensity of signaling output at different developmental stages is depicted based on transcriptome experiments and signaling mutant phenotypes; however, it has not been precisely localized using reporter studies. Following rhizobia perception, GA level/signaling accompanies the activation of symbiotic signaling. Core biosynthesis, metabolism, and signaling components are depicted in black/gray at the right with species-specific components shown where they have been investigated. NF-induced/repressed components are indicated with a brown arrow (up or down, respectively).

Figure 6

Peptide Hormones as Systemic Regulators of Nodulation. CK associated with nodule initiation induces NIN and production of CLE-RS peptides. CLE-RS2 is also induced by nitrate via NLP4. Although CLE-RS2 participates in systemic regulation, NLP1 locally inhibits nodulation through competition with NIN for downstream regulatory elements. Processed CLE-RS peptides are transported to, and perceived in, the shoot by HAR1. HAR1 then inhibits miRNA2111 abundance to prevent negative regulation of TML, establishing AON. Nitrogen starvation responses are integrated into this pathway by CEP/CRA2 signaling, which acts antagonistically to HAR1 on miRNA2111 levels.