Strigolactones are a structurally diverse class of plant hormones that control many aspects of shoot and root growth. Strigolactones are also exuded by plants into the rhizosphere, where they promote symbiotic interactions with arbuscular mycorrhizal fungi and germination of root parasitic plants in the Orobanchaceae family. Therefore, understanding how strigolactones are made, transported, and perceived may lead to agricultural innovations as well as a deeper knowledge of how plants function. Substantial progress has been made in these areas over the past decade. In this review, we focus on the molecular mechanisms, core developmental roles, and evolutionary history of strigolactone signaling. We also propose potential translational applications of strigolactone research to agriculture.

The default mineral nutrient acquisition strategy of land plants is the symbiosis with arbuscular mycorrhiza (AM) fungi. Research into the cell and developmental biology of AM revealed fascinating insights into the plasticity of plant cell development and of interorganismic communication. It is driven by the prospect of increased exploitation of AM benefits for sustainable agriculture. The plant cell developmental program for intracellular accommodation of AM fungi is activated by a genetically defined signaling pathway involving calcium spiking in the nucleus as second messenger. Calcium spiking is triggered by chitooligosaccharides released by AM fungi that are probably perceived via LysM domain receptor kinases. Fungal infection and calcium spiking are spatiotemporally coordinated, and only cells committed to accommodating the fungus undergo high-frequency spiking. Delivery of mineral nutrients by AM fungi occurs at tree-shaped hyphal structures, the arbuscules, in plant cortical cells. Nutrients are taken up at a plant-derived periarbuscular membrane, which surrounds fungal hyphae and carries a specific transporter composition that is of direct importance for symbiotic efficiency. An elegant study has unveiled a new and unexpected mechanism for specific protein localization to the periarbuscular membrane, which relies on the timing of gene expression to synchronize protein biosynthesis with a redirection of secretion. The control of AM development by phytohormones is currently subject to active investigation and has led to the rediscovery of strigolactones. Nearly all tested phytohormones regulate AM development, and major insights into the mechanisms of this regulation are expected in the near future.

Knowledge about signaling in arbuscular mycorrhizal (AM) symbioses is currently restricted to the common symbiosis (SYM) signaling pathway discovered in legumes. This pathway includes calcium as a second messenger and regulates both AM and rhizobial symbioses. Both monocotyledons and dicotyledons form symbiotic associations with AM fungi, and although they differ markedly in the organization of their root systems, the morphology of colonization is similar. To identify and dissect AM-specific signaling in rice (Oryza sativa), we developed molecular phenotyping tools based on gene expression patterns that monitor various steps of AM colonization. These tools were used to distinguish common SYMdependent and -independent signaling by examining rice mutants of selected putative legume signaling orthologs predicted to be perturbed both upstream (CASTOR and POLLUX) and downstream (CCAMK and CYCLOPS) of the central, calciumspiking signal. All four mutants displayed impaired AM interactions and altered AM-specific gene expression patterns, therefore demonstrating functional conservation of SYM signaling between distant plant species. In addition, differential gene expression patterns in the mutants provided evidence for AM-specific but SYM-independent signaling in rice and furthermore for unexpected deviations from the SYM pathway downstream of calcium spiking.

Arbuscular mycorrhiza (AM) symbioses contribute to global carbon cycles as plant hosts divert up to 20% of photosynthate to the obligate biotrophic fungi. Previous studies suggested carbohydrates as the only form of carbon transferred to the fungi. However, de novo fatty acid (FA) synthesis has not been observed in AM fungi in absence of the plant. In a forward genetic approach, we identified two Lotus japonicus mutants defective in AM-specific paralogs of lipid biosynthesis genes (KASI and GPAT6). These mutants perturb fungal development and accumulation of emblematic fungal 16:1ω5 FAs. Using isotopolog profiling we demonstrate that 13C patterns of fungal FAs recapitulate those of wild-type hosts, indicating cross-kingdom lipid transfer from plants to fungi. This transfer of labelled FAs was not observed for the AM-specific lipid biosynthesis mutants. Thus, growth and development of beneficial AM fungi is not only fueled by sugars but depends on lipid transfer from plant hosts.DOI: http://dx.doi.org/10.7554/eLife.29107.001

In terrestrial ecosystems, plants take up phosphate predominantly via association with arbuscular mycorrhizal fungi (AMF). We identified loss of responsiveness to AMF in the rice (Oryza sativa) mutant hebiba, reflected by the absence of physical contact and of characteristic transcriptional responses to fungal signals. Among the 26 genes deleted in hebiba, DWARF 14 LIKE is, the one responsible for loss of symbiosis . It encodes an alpha/beta-fold hydrolase, that is a component of an intracellular receptor complex involved in the detection of the smoke compound karrikin. Our finding reveals an unexpected plant recognition strategy for AMF and a previously unknown signaling link between symbiosis and plant development.