Blumenols as shoot markers of root symbiosis with arbuscular mycorrhizal fungi

Wang, Ming; Schäfer, M.; Li, Dapeng; Halitschke, Rayko; Dong, Chuanfu; McGale, Erica; Paetz, Christian; Song, Yuanyuan; Li, Suhua; Dong, Junfu; Heiling, Sven; Groten, Karin; Franken, Philipp; Bitterlich, Michael; Harrison, Maria J.; Paszkowski, Uta; Baldwin, Ian T.

doi:10.7554/elife.37093

Cited by 65 publications

(112 citation statements)

References 70 publications

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“…Population geneticists have long utilized the genetic variance derived from natural populations to query the genetic architecture underlying traits of interest. Recently, the allelic diversity in the genome of two natural accessions collected from Utah and Arizona (Glawe et al ., ; Wu et al ., ) has been utilized to create an advanced intercross recombinant inbred line (AI‐RIL) population to identify genetic components of indirect defense (Zhou et al ., ) and arbuscular mycorrhizal interactions (Wang et al ., ). This AI‐RIL approach has recently been extended by creating a 26‐parent Multiparent Advanced Generation Inter‐Cross (MAGIC) population which we describe in the next section.…”

Section: Natural Variation In Ja Signaling In N Attenuata Populationsmentioning

confidence: 97%

Using natural variation to achieve a whole‐plant functional understanding of the responses mediated by jasmonate signaling

Ray

Halitschke

et al. 2019

The Plant Journal

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Summary The dramatic advances in our understanding of the molecular biology and biochemistry of jasmonate (JA) signaling have been the subject of several excellent recent reviews that have highlighted the phytohormonal function of this signaling pathway. Here, we focus on the responses mediated by JA signaling which have consequences for a plant's Darwinian fitness, i.e. the organism‐level function of JA signaling. The most diverse module in the signaling cascade, the JAZ proteins, and their interactions with other proteins and transcription factors, allow this canonical signaling cascade to mediate a bewildering array of traits in different tissues at different times; the functional coherence of these diverse responses are best appreciated in an organismal/ecological context. From published work, it appears that jasmonates can function as the ‘Swiss Army knife’ of plant signaling, mediating many different biotic and abiotic stress and developmental responses that allow plants to contextualize their responses to their frequently changing local environments and optimize their fitness. We propose that a deeper analysis of the natural variation in both within‐plant and within‐population JA signaling components is a profitable means of attaining a coherent whole‐plant functional perspective of this signaling cascade, and provide examples of this approach from the Nicotiana attenuata system.

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Section: Natural Variation In Ja Signaling In N Attenuata Populationsmentioning

confidence: 97%

Using natural variation to achieve a whole‐plant functional understanding of the responses mediated by jasmonate signaling

Ray

Halitschke

et al. 2019

The Plant Journal

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“…Here, we took advantage of AMF-indicative blumenol leaf markers (Wang, Schäfer, et al, 2018) and measured the contents of hydroxyblumenol C-glucoside in leaves to obtain an overview of root colonization of all plants at different time points of the experiment and selected mesocosms, which had similar root AMF colonization rates. This analysis also provided key parameters for the N. attenuata system such as the intensity of root colonization required to establish a sufficiently strong CMN (hydroxyblumenol C-glucoside, about 100 ng/g FW relative to d 6 -ABA; Figure 3g (Figures 4 and S2).…”

Section: Discussionmentioning

confidence: 99%

“…of the 31st generation inbred line were used. Seed germination and plant growth were performed as described (Krugel, Lim, Gase, Halitschke, & Baldwin, 2002;Wang, Schäfer, et al, 2018). N. attenuata seeds were sterilized and germinated on agar with Gamborg B5 (Duchefa, the Netherlands, http://www.duchefa.com) after soaking for 1 hr in a 1:50 (v/v) diluted liquid smoke (House of Herbs, Passaic, NY, USA) supplemented with 1 mM of gibberellic acid (GA 3 ).…”

Section: N Attenuata Seed Germination and Growthmentioning

confidence: 99%

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Priming and filtering of antiherbivore defences among Nicotiana attenuata plants connected by mycorrhizal networks

Song

Wang

Zeng

et al. 2019

Plant Cell & Environment

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Arbuscular mycorrhizal fungi (AMF) establish symbiotic associations with a majority of terrestrial plants to form underground common mycorrhizal networks (CMNs) that connect neighbouring plants. Because Nicotiana attenuata plants do not respond to herbivory‐elicited volatiles from neighbours, we used this ecological model system to evaluate if CMNs function in interplant transmission of herbivory‐elicited responses. A mesocosm system was designed to establish and remove CMNs linking N. attenuata plants to examine the herbivory‐elicited metabolic and hormone responses in CMNs‐connected “receiver” plants after the elicitation of “donor” plants by wounding (W) treated with Manduca sexta larval oral secretions (OS). AMF colonization increased constitutive jasmonate (JA and JA‐Ile) levels in N. attenuata roots but did not affect well‐characterized JAs‐regulated defensive metabolites in systemic leaves. Interestingly, larger JAs bursts, and higher levels of several amino acids and particular sectors of hydroxygeranyllinalool diterpene glycoside metabolism were elevated in the leaves of W + OS‐elicited “receivers” with CMN connections with “donors” that had been W + OS‐elicited 6 hr previously. Our results demonstrate that AMF colonization alone does not enhance systemic defence responses but that sectors of systemic responses in leaves can be primed by CMNs, suggesting that CMNs can transmit and even filter defence signalling among connected plants.

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“…Tobacco plants, infected by blue mold accumulated β-ionone levels 50-600-fold higher in non-infected stem tissues adjacent to necrotic lesions (Salt et al 1986), and many norisoprenoids with hydroxyor oxo-functions at C3 position act as plant growth inhibitors and allelochemicals (D'Abrosca et al 2004;Dietz and Winterhalter 1996;Kato-Noguchi et al 2010;Macías et al 2008). Blumenol (3-oxo-α-ionol and its glycosides) accumulates upon arbuscular mycorrhiza (AM) colonization and is probably responsible for systemic suppression of additional AM colonization (Hou et al 2016;Wang et al 2018).…”

Section: Introductionmentioning

confidence: 99%

Glycosylation of bioactive C₁₃-apocarotenols inNicotiana benthamianaandMentha × piperita

Sun

Putkaradze

Bohnacker

et al. 2020

Preprint

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SummaryC13-apocarotenoids (norisoprenoids) are carotenoid-derived oxidation products, which perform important physiological functions in plants. Although their biosynthetic pathways have been extensively studied, their metabolism including glycosylation remains elusive. Candidate uridine-diphosphate glycosyltransferase genes (UGTs) were selected for their high transcript abundance in comparison with other UGTs in vegetative tissues of Nicotiana benthamiana and Mentha × piperita, as these tissues are rich sources of apocarotenoid glucosides. Hydroxylated C13-apocarotenol substrates were produced by P450-catalyzed biotransformation and microbial/plant enzyme systems were established for the synthesis of glycosides. Natural substrates were identified by physiological aglycone libraries prepared from isolated plant glycosides. In total, we identified six UGTs that catalyze the unprecedented glucosylation of C13-apocarotenols, where glucose is bound either to the cyclohexene ring or butane side chain. MpUGT86C10 is a superior novel enzyme that catalyzes the glucosylation of allelopathic 3-hydroxy-α-damascone, 3-oxo-α-ionol, 3-oxo-7,8-dihydro-α-ionol (Blumenol C) and 3-hydroxy-7,8-dihydro-β-ionol, while a germination test demonstrated the higher phytotoxic potential of a norisoprenoid glucoside in comparison to its aglycone. Glycosylation of C13-apocarotenoids has several functions in plants, including increased allelopathic activity of the aglycone, facilitating exudation by roots and allowing symbiosis with arbuscular mycorrhizal fungi. The results enable in-depth analyses of the roles of glycosylated norisoprenoid allelochemicals, the physiological functions of apocarotenoids during arbuscular mycorrhizal colonization and the associated maintenance of carotenoid homeostasis.One-sentence summaryWe identified six transferases in Nicotiana benthamiana and Mentha x piperita, two rich sources of glycosylated apocarotenoids that catalyze the unprecedented glycosylation of a range of hydroxylated α- and β-ionone/ionol derivatives and were able to modify bioactivity by glucosylation.

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Blumenols as shoot markers of root symbiosis with arbuscular mycorrhizal fungi

Cited by 65 publications

References 70 publications

Using natural variation to achieve a whole‐plant functional understanding of the responses mediated by jasmonate signaling

Using natural variation to achieve a whole‐plant functional understanding of the responses mediated by jasmonate signaling

Priming and filtering of antiherbivore defences among Nicotiana attenuata plants connected by mycorrhizal networks

Glycosylation of bioactive C₁₃-apocarotenols inNicotiana benthamianaandMentha × piperita

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Blumenols as shoot markers of root symbiosis with arbuscular mycorrhizal fungi

Cited by 65 publications

References 70 publications

Using natural variation to achieve a whole‐plant functional understanding of the responses mediated by jasmonate signaling

Using natural variation to achieve a whole‐plant functional understanding of the responses mediated by jasmonate signaling

Priming and filtering of antiherbivore defences among Nicotiana attenuata plants connected by mycorrhizal networks

Glycosylation of bioactive C13-apocarotenols inNicotiana benthamianaandMentha × piperita

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Glycosylation of bioactive C₁₃-apocarotenols inNicotiana benthamianaandMentha × piperita