Strigolactones Are Transported through the Xylem and Play a Key Role in Shoot Architectural Response to Phosphate Deficiency in Nonarbuscular Mycorrhizal Host Arabidopsis

Strigolactones affect development in primitive plants. The missing link between plants and arbuscular mycorrhizal fungi?

Structure and Activity of Strigolactones: New Plant Hormones with a Rich Future

Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots.

Host plant-derived strigolactones trigger hyphal branching in arbuscular mycorrhizal (AM) fungi, initiating a symbiotic interaction between land plants and AM fungi. However, our previous studies revealed that gibberellin-treated lisianthus (Eustoma grandiflorum, Gentianaceae) activates rhizospheric hyphal branching in AM fungi using unidentified molecules other than strigolactones. In this study, we analyzed independent transcriptomic data of E. grandiflorum and found that the biosynthesis of gentiopicroside (GPS) and swertiamarin (SWM), characteristic monoterpene glucosides in Gentianaceae, was upregulated in gibberellin-treated E. grandiflorum roots. Moreover, these metabolites considerably promoted hyphal branching in the Glomeraceae AM fungi Rhizophagus irregularis and Rhizophagus clarus. GPS treatment also enhanced R. irregularis colonization of the monocotyledonous crop chive (Allium schoenoprasum). Interestingly, these metabolites did not provoke the germination of the root parasitic plant common broomrape (Orobanche minor). Altogether, our study unveiled the role of GPS and SWM in activating the symbiotic relationship between AM fungi and E. grandiflorum.

Strigolactones are a group of terpenoid lactones that act as a host-derived signal in the rhizosphere communication of plants with arbuscular mycorrhizal (AM) fungi and root parasitic weeds as well as an endogenous plant hormone regulating shoot branching in plants. Strigolactones induce hyphal branching in AM fungi at very low concentrations, suggesting a highly sensitive perception system for strigolactones present in AM fungi. However, little is known about the structural requirements of strigolactones for hyphal branching in AM fungi. Here, we tested a series of natural and synthetically modified strigolactones as well as non-strigolactone-type germination stimulants for hyphal branching-inducing activity in germinating spores of the AM fungus Gigaspora margarita. All tested compounds with a tricyclic lactone coupled to a methylbutenolide via an enol ether bond showed activity, but differed in the active concentration and in the branching pattern of hyphae. Truncation of the A- and AB-rings in the tricyclic ABC lactone of strigolactones resulted in a drastic reduction in hyphal branching activity. Although the connection of the C-ring in the tricyclic lactone to the methylbutenolide D-ring was shown to be essential for hyphal branching, the bridge structure in the C–D part was found not necessarily to be enol ether, being replaceable with either alkoxy or imino ethers. These structural requirements in AM fungi are very similar but not identical to those observed in root parasitic weeds, especially with respect to the enol ether bridge in the C–D part.

Fungal metabolites active for insects were obtained from fermentation products using okara media. The mechanisms of action of these compounds against insects were clarified using voltage clamp electrophysiology. The branching factor inducing hyphal branching in arbuscular mycorrhizal (AM) fungi was isolated from the root exudates of Lotus japonicus and identified as 5-deoxystrigol. Strigolactones were originally identified as seed germination stimulants of parasitic weeds; therefore, synthetic strigolactones were developed to exhibit the inducing activity of hyphal branching in AM fungi and diminish the stimulating activity of seed germination of parasitic weeds. Signaling molecules, acylhomoserine lactones (AHLs), in quorum sensing were identified in the fungal strain Mortierella alpina A-178, and the true producer of AHLs was clarified as symbiotic bacteria in the fungus. Since acyl-(S)-adenosylmethionine analogs may be good candidates for competitive inhibitors of AHL synthases, intermediate mimics in the biosynthesis of AHLs have been synthesized.

It is well established that plants grown under limited phosphorus (Pi) conditions are more readily colonized by arbuscular mycorrhizal (AM) fungi. It is also known that certain components of host root exudates can stimulate hyphal growth and branching of AM fungi and these compounds are elevated when the host is grown under Pi stress. To obtain a more general picture of the types of compounds exuded by host roots that effect the growth of AM fungi, a global analysis was performed on crude exudates of Ri TDNA-transformed carrot roots grown in the presence and absence of Pi. The results show that there is a distinct population of exudate compounds that are elevated in the absence versus the presence of Pi. Putative identifications were made for some of these compounds from data obtained by Fourier Transform Ion Cyclotron Mass Spectrometry (FTMS). The results were then compared to components of biologically active fractions purified by two dimensional thin layer chromatography (2D TLC). The data selection was restricted to compounds that were initially identified to be elevated in the crude – Pi exudate. The categories of compounds, such as plant growth regulators, phenols, flavonoids, and sesquiterpenoids were selected that had the most relevance to AM fungal/host interactions. The previous results with some of these compounds will be discussed in relation to new results obtained from FTMS and their involvement in presymbiotic growth of AM fungi. None of the reported strigolactones which stimulate AM fungi hyphal were found although several sesquiterpene lactones were identified. A number of hydroxy fatty acids were also found, and they were elevated in the – Pi crude exudate and found to be present in 2D TLC fractions. One hydroxy fatty acid, 2-hydroxytetradecanoic acid, stimulated lateral branching of the primary germ tube of Gigaspora gigantea, when applied to Petri dishes in amounts as low as 1–10 ng.

* Strigolactones are rhizosphere signalling compounds that mediate host location in arbuscular mycorrhizal (AM) fungi and parasitic plants. Here, the regulation of the biosynthesis of strigolactones is studied in tomato (Solanum lycopersicum). * Strigolactone production under phosphate starvation, in the presence of the carotenoid biosynthesis inhibitor fluridone and in the abscisic acid (ABA) mutant notabilis were assessed using a germination bioassay with seeds of Orobanche ramosa; a hyphal branching assay with Gigaspora spp; and by liquid chromatography coupled to tandem mass spectrometry (LC-MS/MS) analysis. * The root exudates of tomato cv. MoneyMaker induced O. ramosa seed germination and hyphal branching in AM fungi. Phosphate starvation markedly increased, and fluridone strongly decreased, this activity. Exudates of notabilis induced approx. 40% less germination than the wild-type. The LC-MS/MS analysis confirmed that the biological activity and changes therein were due to the presence of several strigolactones; orobanchol, solanacol and two or three didehydro-orobanchol isomers. * These results show that the AM branching factors and parasitic plant germination stimulants in tomato root exudate are strigolactones and that they are biosynthetically derived from carotenoids. The dual activity of these signalling compounds in attracting beneficial AM fungi and detrimental parasitic plants is further strengthened by environmental conditions such as phosphate availability.

Both root parasitic plants and arbuscular mycorrhizal (AM) fungi take advantage of strigolactones, released from plant roots as signal molecules in the initial communication with host plants, in order to commence parasitism and mutualism, respectively. In this study, strigolactones in root exudates from 12 Fabaceae plants, including hydroponically grown white lupin (Lupinus albus), a nonhost of AM fungi, were characterized by comparing retention times of germination stimulants on reverse-phase high-performance liquid chromatography (HPLC) with those of standards and by using tandem mass spectrometry (LC/MS/MS). All the plant species examined were found to exude known strigolactones, such as orobanchol, orobanchyl acetate, and 5-deoxystrigol, suggesting that these strigolactones are widely distributed in the Fabaceae. It should be noted that even the nonmycotrophic L. albus exuded orobanchol, orobanchyl acetate, 5-deoxystrigol, and novel germination stimulants. By contrast to the mycotrophic Fabaceae plant Trifolium pratense, in which phosphorus deficiency promoted strigolactone exudation, neither phosphorus nor nitrogen deficiency increased exudation of these strigolactones in L. albus. Therefore, the regulation of strigolactone production and/or exudation seems to be closely related to the nutrient acquisition strategy of the plants.

Strigolactones (SLs) are essential host recognition signals for both root-parasitic plants and arbuscular mycorrhizal (AM) fungi in the rhizosphere, and in planta SLs or their metabolites function as a novel class of plant hormones that regulate various aspects of plant growth through crosstalk with other hormones. Although nutrient availability is one of the important factors influencing SL production and exudation, and phosphate (Pi) deficiency significantly promotes SL production and exudation in host plants of AM fungi, how nutrient availability modulates SL production and exudation remains elusive. Cytokinin (CK), a canonical plant hormone, has extensively been studied as a shoot branching promoter and its biosynthesis is also influenced by mineral nutrients, especially nitrate, indicating that CK might be another key factor that affect SL production and exudation. In the present study, we show that CKs (t-zeatin, benzyladenine, kinetin, and CPPU) applied to hydroponic culture media significantly suppressed the SL levels in both the root exudates and the root tissues of rice plants grown under Pi deficiency. In a split-root system, CK suppressed SL production locally, while Pi affected SL production systemically, suggesting that Pi and CK act on SL production independently in rice plants.

Strigolactones (SLs) are terpenoid lactones produced mainly in plant roots and initially identified as seed germination stimulants for parasitic weeds. In 2005, they were described also as boosters of hyphal branching in arbuscular mycorrhizal fungi, and thereby as promoters of arbuscular mycorrhizal symbiosis. In 2008, they emerged as a new class of plant hormones controlling plant architecture through repression of shoot branching. Since then, several new roles were discovered for SLs: in the adaptive responses to a number of environmental stimuli (including light, osmotic stress, interaction with pathogens and nodulating bacteria), and in several aspects of plant development (including seed germination for nonparasitic plants, hypocotyl elongation, reproduction, leaf senescence and nodulation). The biosynthetic and perception/transduction systems of SLs are being elucidated, and the first mechanistic models presented. Key Concepts: Strigolactones are the key nutrient allocators regulating plant development at the interface between plants, beneficial and detrimental (micro)organisms, and abiotic factors. Strigolactones induce hyphal branching in AM fungi and facilitate the establishment of symbiosis. Strigolactones inhibit shoot branching. Strigolactones affect root architecture and root development depending on nutrients availability. Synthetic SLs (analogues and mimics) are used in pharmacological applications to plants and fungi to decipher the structure–activity relationship. Structure–activity relationship (SAR): Different structures are tested for bioactivity in order to pinpoint which part of the molecule is essential for bioactivity and which can be considered only ‘decoration’.

Strigolactones (SLs), a novel class of plant hormones, are key regulator of plant architecture and mediator of biotic interactions in the rhizosphere. Root-released SLs initiate the establishment of arbuscular mycorrhizal (AM) symbiosis by inducing spore germination and hyphal branching in AM fungi (AMF). However, these compounds also trigger the germination of root parasitic weeds, paving the way for deleterious infestation. Availability of SLs is required for investigating of their functions and also for application in agriculture. However, natural SLs are difficult to synthesize due to their complex structure and cannot be isolated at large scale, as they are released at very low concentrations. Therefore, there is a need for synthetic SL analogs. Recently, we reported on the development of simple SL analogs, methyl phenlactonoates (MPs), which show high SL activity in plants. Here, we investigate the effect of MP1, MP3 and the widely used SL-analog GR24 on AMF spore germination and host root colonization. Our results show that MP1 and MP3 inhibit AMF spore germination, but promote the intra-radical root colonization, both more efficiently than GR24. These results indicate that field application of MP1 and MP3 does not have negative impact on mycorrhizal fungi. In conclusion, our data together with the previously reported simple synthesis, high activity in regulating plant architecture and inducing Striga seed germination, demonstrate the utility of MP1 and MP3 as for field application in combating root parasitic weeds by inducing germination in host's absence.

Origins and evolution of the dual functions of strigolactones as rhizosphere signaling molecules and plant hormones

Strigolactone and analogues: A new generation of plant hormones with multifactorial benefits in environmental sustainability

Strigolactones (SLs) were initially identified as rhizosphere signals that trigger germination of parasitic weeds and promote branching in arbuscular mycorrhizal fungi. More recently, SLs have been characterized as a class of carotenoid-derived plant hormones that regulate plant architecture and stress responses. This review systematically summarizes their diverse functions in shaping shoot architecture and root development, as well as their ability to mediate acclimation to various abiotic and biotic stresses. It also discusses the canonical signaling module composed of D14, MAX2/D3, and D53/SMXLs and its extensive interactions with other hormonal pathways. Finally, this review suggests that future research should focus on elucidating the dynamic responses to environmental stress mediated by the SL pathway, decoding the functional diversification of SLs in different plant species, and leveraging SLs as rhizosphere signals to control parasitic weeds. Precise spatiotemporal modulation of SL activity is crucial for balancing its functional complexity and will contribute to designing crops with optimized plant architectures and enhanced stress resilience.