Genomic and Coexpression Analyses Predict Multiple Genes Involved in Triterpene Saponin Biosynthesis in <i>Medicago truncatula</i>

Naoumkina, Marina; Modolo, Luzia V.; Huhman, David V.; Urbańczyk-Wochniak, Ewa; Tang, Yuhong; Sumner, Lloyd W.; Dixon, Richard A.

doi:10.1105/tpc.109.073270

Cited by 169 publications

(156 citation statements)

References 81 publications

Supporting

Mentioning

154

Contrasting

Order By: Relevance

“…Incomplete glycosylation of the triterpene glycoside (i.e., saponin) avenacin results in degeneration of the epidermis and altered root hair development in oat (Mylona et al, 2008). Moreover, M. truncatula growth is severely affected by alterations in glycosylation of the saponin hederagenin (Naoumkina et al, 2010). More specifically for tomato SAs, Hoagland (2009) showed that tomatidine had a greater effect than a-tomatine in electrolyte leakage tests performed on leaves of a number of plant species.…”

Section: Phytotoxicity Observed In Game1-silenced Plants and Their Ramentioning

confidence: 99%

“…Whereas a-tomatine damages tissues within an array of plant species (Hoagland, 2009), its toxic effects in tomato fruit and leaves were suggested to be negligible due to the presence in cell membranes of sterol glycosides and acetylated sterol glycosides rather than sterols such as cholesterol, containing a free 3b-OH group (with which a-tomatine forms insoluble complexes) (Roddick, 1976a;Steel and Drysdale, 1988;Blankemeyer et al, 1997). Glycosylation of membrane steroids serves a protective function against toxic compounds, including saponins (Naoumkina et al, 2010). Incomplete glycosylation of the triterpene glycoside (i.e., saponin) avenacin results in degeneration of the epidermis and altered root hair development in oat (Mylona et al, 2008).…”

Section: Phytotoxicity Observed In Game1-silenced Plants and Their Ramentioning

confidence: 99%

“…Glycosylation of SAs is believed to reduce the toxicity of a-tomatine to the plant cell, as treatment of leaf disks from four plant species demonstrated that a-tomatine caused more severe electrolyte leakage than did its aglycone tomatidine (Hoagland, 2009). In addition, studies of triterpene saponins in oat (Avena sativa) and Medicago truncatula pointed to the same role of glycosylation (Mylona et al, 2008;Naoumkina et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

GLYCOALKALOID METABOLISM1 Is Required for Steroidal Alkaloid Glycosylation and Prevention of Phytotoxicity in Tomato

et al. 2011

View full text Add to dashboard Cite

Steroidal alkaloids (SAs) are triterpene-derived specialized metabolites found in members of the Solanaceae family that provide plants with a chemical barrier against a broad range of pathogens. Their biosynthesis involves the action of glycosyltransferases to form steroidal glycoalkaloids (SGAs). To elucidate the metabolism of SGAs in the Solanaceae family, we examined the tomato (Solanum lycopersicum) GLYCOALKALOID METABOLISM1 (GAME1) gene. Our findings imply that GAME1 is a galactosyltransferase, largely performing glycosylation of the aglycone tomatidine, resulting in SGA production in green tissues. Downregulation of GAME1 resulted in an almost 50% reduction in a-tomatine levels (the major SGA in tomato) and a large increase in its precursors (i.e., tomatidenol and tomatidine). Surprisingly, GAME1-silenced plants displayed growth retardation and severe morphological phenotypes that we suggest occur as a result of altered membrane sterol levels caused by the accumulation of the aglycone tomatidine. Together, these findings highlight the role of GAME1 in the glycosylation of SAs and in reducing the toxicity of SA metabolites to the plant cell.

show abstract

Section: Phytotoxicity Observed In Game1-silenced Plants and Their Ramentioning

confidence: 99%

Section: Phytotoxicity Observed In Game1-silenced Plants and Their Ramentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

GLYCOALKALOID METABOLISM1 Is Required for Steroidal Alkaloid Glycosylation and Prevention of Phytotoxicity in Tomato

et al. 2011

View full text Add to dashboard Cite

show abstract

“…Phylogenetic analysis indicated that Sg-1 a and Sg-1 b are classified in a phylogenetic group known as cluster IIIa represented by flavonoid 7-O-glycosyltransferases (Noguchi et al, 2008) (Figure 5C). More importantly, this cluster was found to include a subcluster composed of various triterpene/ phytosterol-related glycosyltransferases from Fabaceae and Solanaceae (e.g., M. truncatula UGT73K1 and UGT73F3; soybean SGT2/UGT73P2 for saponin; tomato [Solanum lycopersicum] GAME1 [UGT73L5], GAME2 [UGT73L4], and GAME3 [UGT73L6]; potato [Solanum tuberosum] SGT1, SGT2, and SGT3; and Solanum aculeatissimum GT4A for steroidal saponin) (Moehs et al, 1997;Achnine et al, 2005;Kohara et al, 2005;McCue et al, 2005McCue et al, , 2006McCue et al, , 2007Naoumkina et al, 2010;Shibuya et al, 2010;Itkin et al, 2011). Sg-1 a (UGT73F4) and Sg-1 b (UGT73F2) genes apparently show structural similarity to M. truncatula saponin glucosyltransferase UGT73F3 (Naoumkina et al, 2010).…”

Section: Phylogenetics Of Sg-1 Proteinsmentioning

confidence: 99%

The Sg-1 Glycosyltransferase Locus Regulates Structural Diversity of Triterpenoid Saponins of Soybean

et al. 2012

View full text Add to dashboard Cite

Triterpene saponins are a diverse group of biologically functional products in plants. Saponins usually are glycosylated, which gives rise to a wide diversity of structures and functions. In the group A saponins of soybean (Glycine max), differences in the terminal sugar species located on the C-22 sugar chain of an aglycone core, soyasapogenol A, were observed to be under genetic control. Further genetic analyses and mapping revealed that the structural diversity of glycosylation was determined by multiple alleles of a single locus, Sg-1, and led to identification of a UDP-sugar-dependent glycosyltransferase gene (Glyma07g38460). Although their sequences are highly similar and both glycosylate the nonacetylated saponin A0-ag, the Sg-1 a allele encodes the xylosyltransferase UGT73F4, whereas Sg-1 b encodes the glucosyltransferase UGT73F2. Homology models and site-directed mutagenesis analyses showed that Ser-138 in Sg-1 a and Gly-138 in Sg-1 b proteins are crucial residues for their respective sugar donor specificities. Transgenic complementation tests followed by recombinant enzyme assays in vitro demonstrated that sg-1 0 is a loss-of-function allele of Sg-1. Considering that the terminal sugar species in the group A saponins are responsible for the strong bitterness and astringent aftertastes of soybean seeds, our findings herein provide useful tools to improve commercial properties of soybean products.

show abstract

“…An aglycone with this mass had been previously observed in M. truncatula, but its structure was not elucidated. 2,7,30 Only one sapogenin with this molecular formula is known to occur in the genus Medicago, namely, 2β,3β-dihydroxy-23-oxoolean-12-en-28-oic acid. This aglycone contains a C-23 formyl group, which is thought to be the biosynthetic intermediate in the enzymatic oxidation of the C-23 hydroxy group of bayogenin, eventually leading to the carboxylation of medicagenic acid (Figure 4).…”

mentioning

confidence: 99%

Metabolite Profiling of Triterpene Saponins in Medicago truncatula Hairy Roots by Liquid Chromatography Fourier Transform Ion Cyclotron Resonance Mass Spectrometry

et al. 2011

View full text Add to dashboard Cite

L egumes (Fabaceae) are important agricultural crops, characterized by the presence of root nodules that contain symbiotic nitrogen-fixing bacteria. Fixation of atmospheric nitrogen allows reduced fertilizer costs and makes legumes a key player in crop rotation to replenish nitrogen-depleted soil. Furthermore, legumes serve as a major source of proteins and oil for human and animal nutrition. Leguminous crops with a significant economical value include oilseed crops such as soybean (Glycine max) and peanut (Arachis hypogaea), forage and soil-conditioning crops such as alfalfa (Medicago sativa) and clover (Trifolium spp.), and pulses such as beans (Phaseolus spp.), peas (Pisum spp.), and lentils (Lens spp.).The more than 19 400 leguminous species, distributed over 730 genera, produce a vast array of metabolites with diverse structures and biological activities. An important group of legume natural products are triterpene saponins, a class of secondary metabolites that display a wide range of biological activities.1 In plants they serve as allelopathic, antipalatability, anti-insect, or antifungal agents.2 Saponins also have a broad range of pharmaceutical properties, such as anti-inflammatory, antimicrobial, anticancer, or adjuvant activities.3,4 Besides saponins, isoflavonoids, alkaloids, and nonprotein amino acids commonly occur as natural products in several legume species. 1,5 As a model species for legume biology, barrel medic (Medicago truncatula), a close relative of alfalfa, is an excellent system to study secondary metabolism of legumes. 1,6 Consequently, several studies about the metabolite composition of M. truncatula have been published over the past decade. Metabolite profiling using LC-MS-based methods revealed the presence of a complex mixture of triterpene saponins in various M. truncatula tissues. 2,7À9 In accordance with other legumes from the Papilionoideae subfamily, M. truncatula is rich in isoflavonoids. 10,11 Hairy roots are generated by an infection of healthy plant tissue, not necessarily roots, with Agrobacterium rhizogenes. They are characterized by fast growth rates and do not require growth regulators for their cultivation. Furthermore, they have a high genetic stability and a high biosynthetic potential for a longer time than natural roots.12,13 Their potential to produce compounds that are also naturally occurring in wild-type roots in combination with their tolerance to cultivation in large-scale bioreactors makes hairy roots an appealing alternative for the destructive harvesting of wild-type roots, especially those of endangered plant species, to obtain valuable phytochemicals. 14,15 Hairy roots are also a valuable tool to investigate the secondary metabolism in M. truncatula. A prerequisite for the study of secondary metabolism and its application in metabolic engineering projects is the possibility to generate transgenic plant tissue. ABSTRACT: Triterpenes are one of the largest classes of plant natural products, with an enormous variety in structure and bioactivities. Here,...

show abstract

Genomic and Coexpression Analyses Predict Multiple Genes Involved in Triterpene Saponin Biosynthesis in Medicago truncatula

Cited by 169 publications

References 81 publications

GLYCOALKALOID METABOLISM1 Is Required for Steroidal Alkaloid Glycosylation and Prevention of Phytotoxicity in Tomato

GLYCOALKALOID METABOLISM1 Is Required for Steroidal Alkaloid Glycosylation and Prevention of Phytotoxicity in Tomato

The Sg-1 Glycosyltransferase Locus Regulates Structural Diversity of Triterpenoid Saponins of Soybean

Metabolite Profiling of Triterpene Saponins in Medicago truncatula Hairy Roots by Liquid Chromatography Fourier Transform Ion Cyclotron Resonance Mass Spectrometry

Contact Info

Product

Resources

About