Strigolactones were originally identified as stimulators of the germination of root-parasitic weeds 1 that pose a serious threat to resource-limited agriculture 2 . They are mostly exuded from roots and function as signalling compounds in the initiation of arbuscular mycorrhizae 3 , which are plant-fungus symbionts with a global effect on carbon and phosphate cycling 4 . Recently, strigolactones were established to be phytohormones that regulate plant shoot architecture by inhibiting the outgrowth of axillary buds 5,6 . Despite their importance, it is not known how strigolactones are transported. ATP-binding cassette (ABC) transporters, however, are known to have functions in phytohormone translocation [7][8][9] . Here we show that the Petunia hybrida ABC transporter PDR1 has a key role in regulating the development of arbuscular mycorrhizae and axillary branches, by functioning as a cellular strigolactone exporter. P. hybrida pdr1 mutants are defective in strigolactone exudation from their roots, resulting in reduced symbiotic interactions. Above ground, pdr1 mutants have an enhanced branching phenotype, which is indicative of impaired strigolactone allocation. Overexpression of Petunia axillaris PDR1 in Arabidopsis thaliana results in increased tolerance to high concentrations of a synthetic strigolactone, consistent with increased export of strigolactones from the roots. PDR1 is the first known component in strigolactone transport, providing new opportunities for investigating and manipulating strigolactone-dependent processes.Strigolactones are a new class of carotenoid-derived 10 phytohormone in land plants. In addition to their role in shoot branching, strigolactones are exuded into the rhizosphere under phosphorus-limiting conditions 5 and act as growth stimulants of arbuscular mycorrhizal fungi 3 . To identify efflux carriers of arbuscular-mycorrhiza-promoting factors such as strigolactones, we used a degenerate primer approach ( Supplementary Fig. 2a) to isolate full-size PDR-type transporters (also known as ABC subtype G (ABCG) transporters) of P. hybrida that are abundant in phosphate-starved or mycorrhizal roots. The rationale behind the focus on these transporters, of which there are 15 in Arabidopsis 11 , 23 in Oryza sativa (rice) 11 and 23 putative factors in Solanum lycopersicum (tomato) ( Supplementary Fig. 3a), was that they are plasma membrane proteins often found in roots 12 , they are implicated in below-ground plantmicrobe interactions 13,14 , and they have affinities for compounds that are structurally related to strigolactones 8,9,15 . Of six primary candidates, only P. hybrida PDR1 had increased expression in roots that were subjected to either phosphate starvation (Fig. 1a) or colonization by the arbuscular mycorrhizal fungus Glomus intraradices (Fig. 1b). Furthermore, PDR1 transcript levels increased in response to treatment with the synthetic strigolactone analogue GR24 or the auxin analogue 1-naphthaleneacetic acid (NAA) (Fig. 1c). Auxin has been shown to upregulate strigolactone-bi...
Carbohydrate import into seeds directly determines seed size and must have been increased through domestication. However, evidence of the domestication of sugar translocation and the identities of seed-filling transporters have been elusive. Maize ZmSWEET4c, as opposed to its sucrose-transporting homologs, mediates transepithelial hexose transport across the basal endosperm transfer layer (BETL), the entry point of nutrients into the seed, and shows signatures indicative of selection during domestication. Mutants of both maize ZmSWEET4c and its rice ortholog OsSWEET4 are defective in seed filling, indicating that a lack of hexose transport at the BETL impairs further transfer of sugars imported from the maternal phloem. In both maize and rice, SWEET4 was likely recruited during domestication to enhance sugar import into the endosperm.
Strigolactones, first discovered as germination stimulants for parasitic weeds [1], are carotenoid-derived phytohormones that play major roles in inhibiting lateral bud outgrowth and promoting plant-mycorrhizal symbiosis [2-4]. Furthermore, strigolactones are involved in the regulation of lateral and adventitious root development, root cell division [5, 6], secondary growth [7], and leaf senescence [8]. Recently, we discovered the strigolactone transporter Petunia axillaris PLEIOTROPIC DRUG RESISTANCE 1 (PaPDR1), which is required for efficient mycorrhizal colonization and inhibition of lateral bud outgrowth [9]. However, how strigolactones are transported through the plant remained unknown. Here we show that PaPDR1 exhibits a cell-type-specific asymmetric localization in different root tissues. In root tips, PaPDR1 is co-expressed with the strigolactone biosynthetic gene DAD1 (CCD8), and it is localized at the apical membrane of root hypodermal cells, presumably mediating the shootward transport of strigolactone. Above the root tip, in the hypodermal passage cells that form gates for the entry of mycorrhizal fungi, PaPDR1 is present in the outer-lateral membrane, compatible with its postulated function as strigolactone exporter from root to soil. Transport studies are in line with our localization studies since (1) a papdr1 mutant displays impaired transport of strigolactones out of the root tip to the shoot as well as into the rhizosphere and (2) DAD1 expression and PIN1/PIN2 levels change in plants deregulated for PDR1 expression, suggestive of variations in endogenous strigolactone contents. In conclusion, our results indicate that the polar localizations of PaPDR1 mediate directional shootward strigolactone transport as well as localized exudation into the soil.
The ability to link soil microbial diversity to soil processes requires technologies that differentiate active microbes from extracellular DNA and dormant cells. Here, we use BONCAT (bioorthogonal non-canonical amino acid tagging) to measure translationally active cells in soils. We compare the active population of two soil depths from Oak Ridge (Tennessee, USA) and find that a maximum of 25–70% of the extractable cells are active. Analysis of 16S rRNA sequences from BONCAT-positive cells recovered by fluorescence-activated cell sorting (FACS) reveals that the phylogenetic composition of the active fraction is distinct from the total population of extractable cells. Some members of the community are found to be active at both depths independently of their abundance rank, suggesting that the incubation conditions favor the activity of similar organisms. We conclude that BONCAT-FACS is effective for interrogating the active fraction of soil microbiomes in situ and provides a new approach for uncovering the links between soil processes and specific microbial groups.
Beneficial plant-microbe interactions offer a sustainable biological solution with the potential to boost low-input food and bioenergy production. A better mechanistic understanding of these complex plant-microbe interactions will be crucial to improving plant production as well as performing basic ecological studies investigating plant-soil-microbe interactions. Here, a detailed description for ecosystem fabrication is presented, using widely available 3D printing technologies, to create controlled laboratory habitats (EcoFABs) for mechanistic studies of plant-microbe interactions within specific environmental conditions. Two sizes of EcoFABs are described that are suited for the investigation of microbial interactions with various plant species, including Arabidopsis thaliana, Brachypodium distachyon, and Panicum virgatum. These flow-through devices allow for controlled manipulation and sampling of root microbiomes, root chemistry as well as imaging of root morphology and microbial localization. This protocol includes the details for maintaining sterile conditions inside EcoFABs and mounting independent LED light systems onto EcoFABs. Detailed methods for addition of different forms of media, including soils, sand, and liquid growth media coupled to the characterization of these systems using imaging and metabolomics are described. Together, these systems enable dynamic and detailed investigation of plant and plant-microbial consortia including the manipulation of microbiome composition (including mutants), the monitoring of plant growth, root morphology, exudate composition, and microbial localization under controlled environmental conditions. We anticipate that these detailed protocols will serve as an important starting point for other researchers, ideally helping create standardized experimental systems for investigating plant-microbe interactions.
Summary There is a dynamic reciprocity between plants and their environment: soil physiochemical properties influence plant morphology and metabolism, and root morphology and exudates shape the environment surrounding roots. Here, we investigate the reproducibility of plant trait changes in response to three growth environments. We utilized fabricated ecosystem (Eco FAB ) devices to grow the model grass Brachypodium distachyon in three distinct media across four laboratories: phosphate‐sufficient and ‐deficient mineral media allowed assessment of the effects of phosphate starvation, and a complex, sterile soil extract represented a more natural environment with yet uncharacterized effects on plant growth and metabolism. Tissue weight and phosphate content, total root length, and root tissue and exudate metabolic profiles were consistent across laboratories and distinct between experimental treatments. Plants grown in soil extract were morphologically and metabolically distinct, with root hairs four times longer than with other growth conditions. Further, plants depleted half of the metabolites investigated from the soil extract. To interact with their environment, plants not only adapt morphology and release complex metabolite mixtures, but also selectively deplete a range of soil‐derived metabolites. The Eco FAB s utilized here generated high interlaboratory reproducibility, demonstrating their value in standardized investigations of plant traits.
Summary Strigolactones (SLs) are carotenoid‐derived phytohormones shaping plant architecture and inducing the symbiosis with endomycorrhizal fungi. In Petunia hybrida, SL transport within the plant and towards the rhizosphere is driven by the ABCG‐class protein PDR1. PDR1 expression is regulated by phytohormones and by the soil phosphate abundance, and thus SL transport integrates plant development with nutrient conditions.We overexpressed PDR1 (PDR1 OE) to investigate whether increased endogenous SL transport is sufficient to improve plant nutrition and productivity. Phosphorus quantification and nondestructive X‐ray computed tomography were applied. Morphological and gene expression changes were quantified at cellular and whole tissue levels via time‐lapse microscopy and quantitative PCR. PDR1 OE significantly enhanced phosphate uptake and plant biomass production on phosphate‐poor soils. PDR1 OE plants showed increased lateral root formation, extended root hair elongation, faster mycorrhization and reduced leaf senescence. PDR1 overexpression allowed considerable SL biosynthesis by releasing SL biosynthetic genes from an SL‐dependent negative feedback.The increased endogenous SL transport/biosynthesis in PDR1 OE plants is a powerful tool to improve plant growth on phosphate‐poor soils. We propose PDR1 as an as yet unexplored trait to be investigated for crop production. The overexpression of PDR1 is a valuable strategy to investigate SL functions and transport routes.
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