Identification of a yellow pigment formed in maize roots upon mycorrhizal colonization

Klingner, A.; Bothe, Hermann; Wray, Victor; Marner, Franz‐Josef

doi:10.1016/0031-9422(94)00538-5

Cited by 104 publications

(75 citation statements)

References 8 publications

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“…the glucosyl-and the glucuronosyltransferases, and eventually the dioxygenase involved in the biosynthesis of the aglycone blumenol C. Dioxygenase activity is believed to catalyze the rate-limiting cleavage of a carotenoid as a potential precursor in the biosynthetic route of the structurally related phytohormone ABA (Parry and Horgan, 1991). The present results and related studies of induction of the accumulation of ABA (Danneberg et al, 1992) and a C,, carotenoid in maize (Klingner et al, 1995a) and some other gramineous plants (Klingner et al, 1995b) suggest that mycorrhiza formation in members of the grass family (Poaceae) is somehow correlated with the terpenoid metabolism of the roots. Future studies will localize the transcripts encoding the enzymes catalyzing blumenin formation, in analogy to a study by Harrison and Dixon (1994).…”

Section: Discussionsupporting

confidence: 65%

Levels of a Terpenoid Glycoside (Blumenin) and Cell Wall-Bound Phenolics in Some Cereal Mycorrhizas

et al. 1995

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~Four cereals, Hordeum vulgare (barley), Triticum aestivum (wheat), Secale cereale (rye), and Avena safiva (oat), were grown in a defined nutritional medium with and without the arbuscular mycorrhizal fungus Glomus intraradices. Levels of soluble and cell wall-bound secondary metabolites in the roots of mycorrhizal and nonmycorrhizal plants were determined by high-performance liquid chromatography during the first 6 to 8 weeks of plant development. Whereas there was no difference in the levels of the cell wall-bound hydroxycinnamic acids, 4-coumaric and ferulic acids, there was a fungus-induced change of the soluble secondary root metabolites. The most obvious effect observed in all four cereals was the induced accumulation of a terpenoid glycoside. This compound was isolated and identified by spectroscopic methods (nuclear magnetic resonance, mass spectrometry) to be a cyclohexenone derivative, i.e. blumenol C 9-0(2'-D~-glucuronosyl)-~-glucoside. The level of this compound was found to be directly correlated with the degree of root colonization.Arbuscular mycorrhizas are universally found symbiotic associations between plant roots and certain fungi, and there is ample evidence that these symbioses are of significant benefit for plants (reviewed by Powell and Bagyaraj, 1984; Gianinazzi and Schüepp, 1994). These benefits include enhanced nutrient supply (e.g. phosphate) and increased resistance to pathogen attack (e.g. root pathogenic fungi) or stress (e.g. drought). Despite increasing efforts in research on arbuscular mycorrhiza at the cellular and molecular levels within the last years Dixon, 1993, 1994;Dumas-Gaudot et al., 1994), very little is known about the basic biochemical interactions between the symbionts leading to formation of arbuscular mycorrhiza and maintenance of an active symbiotic relationship. This is in sharp contrast to our knowledge about pathogenic plantfungus interactions .There is increasing evidence that secondary compounds in particular play a significant role in the interactions occurring between plants and their natural environment (Harborne, 1988). In this respect, secondary metabolites of roots might play an important role in mycorrhizal symbiosis. It has been documented, for example, that flavonoids promote spore germination of arbuscular mycorrhizal 'This work was supported by the Fonds der Chemischen * Corresponding author; fax 49-345-5582-106.Industrie.fungi (Gianinazzi-Pearson et al., 1989;Tsai and Phillips, 1991). Colonization of plants with arbuscular mycorrhizal fungi may lead to marked systemic reactions in terpenoid metabolism. Thus, Glomus intraradices induces accumulation of significant amounts of leaf sesquiterpenoids in Citrus jambkiri (Nemec and Lund, 1990). The sesquiterpenoid ABA reaches considerably higher levels in Glomus-colonized maize than in control plants (Danneberg et al., 1993).As part of our studies of arbuscular mycorrhizal fungiinduced changes in secondary metabolism of cereals, we report here quantitative changes of root secondary products during form...

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Section: Discussionsupporting

confidence: 65%

Levels of a Terpenoid Glycoside (Blumenin) and Cell Wall-Bound Phenolics in Some Cereal Mycorrhizas

et al. 1995

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“…1C). Similarly, levels of AM-induced plant secondary metabolites, such as cyclohexenone derivatives (Maier et al, 2000) and mycorradicin derivatives (also called yellow pigment; Klingner et al, 1995), which accumulate in mycorrhizal roots and are suggested to play a functional role in AM (Fester et al, 2002;Strack et al, 2003), were not affected by the increased invertase activity (Table I). In nonmycorrhizal plants these metabolites could not be detected (data not shown; see also Fester et al, 2002Fester et al, , 2005Schliemann et al, 2006).…”

Section: Effect Of Root-specific Enhancement Of Apoplastic Invertase mentioning

confidence: 94%

Regulation of Arbuscular Mycorrhization by Carbon. The Symbiotic Interaction Cannot Be Improved by Increased Carbon Availability Accomplished by Root-Specifically Enhanced Invertase Activity

Schaarschmidt

González²,

Roitsch³

et al. 2007

PLANT PHYSIOLOGY

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The mutualistic interaction in arbuscular mycorrhiza (AM) is characterized by an exchange of mineral nutrients and carbon. The major benefit of AM, which is the supply of phosphate to the plant, and the stimulation of mycorrhization by low phosphate fertilization has been well studied. However, less is known about the regulatory function of carbon availability on AM formation. Here the effect of enhanced levels of hexoses in the root, the main form of carbohydrate used by the fungus, on AM formation was analyzed. Modulation of the root carbohydrate status was performed by expressing genes encoding a yeast (Saccharomyces cerevisiae)-derived invertase, which was directed to different subcellular locations. Using tobacco (Nicotiana tabacum) alcTcwINV plants, the yeast invertase was induced in the whole root system or in root parts. Despite increased hexose levels in these roots, we did not detect any effect on the colonization with Glomus intraradices analyzed by assessment of fungal structures and the level of fungus-specific palmitvaccenic acid, indicative for the fungal carbon supply, or the plant phosphate content. Roots of Medicago truncatula, transformed to express genes encoding an apoplast-, cytosol-, or vacuolar-located yeastderived invertase, had increased hexose-to-sucrose ratios compared to b-glucuronidase-transformed roots. However, transformations with the invertase genes did not affect mycorrhization. These data suggest the carbohydrate supply in AM cannot be improved by root-specifically increased hexose levels, implying that under normal conditions sufficient carbon is available in mycorrhizal roots. In contrast, tobacco rolCTppa plants with defective phloem loading and tobacco pyk10TInvInh plants with decreased acid invertase activity in roots exhibited a diminished mycorrhization.Arbuscular mycorrhiza (AM) represents a widespread mutualistic association between soil-born fungi of the phylum Glomeromycota and most land plants. The AM interaction enables the plant to improve its supply of water and mineral nutrients, mainly phosphate. In return, the obligate biotrophic AM fungi are provided with carbon. In the Arum-type interaction, as analyzed here between Glomus sp. and tobacco (Nicotiana tabacum) or Medicago truncatula, the AM fungus colonizes the cortical cells by formation of intra-and intercellular hyphae and very characteristic haustorialike structures, the highly branched intracellular arbuscules. When the carbon supply is sufficient, lipid-rich vesicles are formed intercellularly within the cortex, as fungal storage organs. Intracellular fungal structures are separated from the plant cytoplasm by an extension of the plasma membrane, forming the periarbuscular membrane surrounding the arbuscule. The greatly increased surfaces of host and arbuscule plasma membranes offers optimized conditions for effective nutrient exchange via the established symbiotic interface (for review, see Gianinazzi-Pearson et al., 1996;Harrison, 1999).The exchange of phosphate via the periarbuscular interface and th...

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“…In plant roots the C 14 dialdehyde is converted to dicarboxylic acid derivatives (mycorradicins), which are yellow and cause the yellow colour of mycorrhizal roots (Klingner et al 1995;Fester et al 2002;Walter et al 2000). Why the bacterial colonies do not turn yellow (Fig.…”

Section: Characterisation Of Maize Ccd1 Cdnas Transcripts and Recombmentioning

confidence: 99%

“…The derivatives of the apocarotenoids mycorradicin (an acyclic C 14 polyene) and C 13 cyclohexenones accumulate during colonisation of roots by arbuscular mycorrhizal (AM) fungi, with the former causing the yellow colour of maize roots that are colonised by AM fungi (Klingner et al 1995;Fester et al 2002). These apocarotenoids are predicted to originate from an unknown C 40 carotenoid precursor by cleavage at positions 9, 10 and 9Ј, 10Ј by an unknown carotenoid cleavage enzyme (Walter et al 2000;Fester et al 2002;Strack and Fester 2006) (Fig.…”

Section: Introductionmentioning

confidence: 99%

Cloning and characterisation of a maize carotenoid cleavage dioxygenase (ZmCCD1) and its involvement in the biosynthesis of apocarotenoids with various roles in mutualistic and parasitic interactions

Sun¹,

Hans

Walter

et al. 2008

Planta

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Colonisation of maize roots by arbuscular mycorrhizal (AM) fungi leads to the accumulation of apocarotenoids (cyclohexenone and mycorradicin derivatives). Other root apocarotenoids (strigolactones) are involved in signalling during early steps of the AM symbiosis but also in stimulation of germination of parasitic plant seeds. Both apocarotenoid classes are predicted to originate from cleavage of a carotenoid substrate by a carotenoid cleavage dioxygenase (CCD), but the precursors and cleavage enzymes are unknown. A Zea mays CCD (ZmCCD1) was cloned by RT-PCR and characterised by expression in carotenoid accumulating E. coli strains and analysis of cleavage products using GC-MS. ZmCCD1 eYciently cleaves carotenoids at the 9, 10 position and displays 78% amino acid identity to Arabidopsis thaliana CCD1 having similar properties. ZmCCD1 transcript levels were shown to be elevated upon root colonisation by AM fungi. Mycorrhization led to a decrease in seed germination of the parasitic plant Striga hermonthica as examined in a bioassay. ZmCCD1 is proposed to be involved in cyclohexenone and mycorradicin formation in mycorrhizal maize roots but not in strigolactone formation.

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Identification of a yellow pigment formed in maize roots upon mycorrhizal colonization

Cited by 104 publications

References 8 publications

Levels of a Terpenoid Glycoside (Blumenin) and Cell Wall-Bound Phenolics in Some Cereal Mycorrhizas

Levels of a Terpenoid Glycoside (Blumenin) and Cell Wall-Bound Phenolics in Some Cereal Mycorrhizas

Regulation of Arbuscular Mycorrhization by Carbon. The Symbiotic Interaction Cannot Be Improved by Increased Carbon Availability Accomplished by Root-Specifically Enhanced Invertase Activity

Cloning and characterisation of a maize carotenoid cleavage dioxygenase (ZmCCD1) and its involvement in the biosynthesis of apocarotenoids with various roles in mutualistic and parasitic interactions

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