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Published on November 30, 2007; 10.1104/pp.107.108431

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Received August 29, 2007
Accepted November 16, 2007

Metabolomics Reveals Novel Pathways, Differential Mechanistic and Elicitor-Specific Responses in Phenylpropanoid and Isoflavonoid Biosynthesis in Medicago truncatula Cell Cultures

Mohamed A. Farag , David V. Huhman , Richard A. Dixon , and Lloyd W. Sumner *

Plant Biology Division, The Samuel Roberts Noble Foundation, Ardmore, OK 73401; Pharmacognosy Department, Faculty of Pharmacy, Kasr El-Aini St., P.B. 11562, Cairo University, Egypt

* Corresponding author; email: lwsumner{at}noble.org.

High performance liquid chromatography coupled to UV photodiode array detection and ion-trap mass spectrometry (HPLC-PDA-ESI-ITMS) was used to analyze the intra- and extracellular secondary product metabolome of Medicago truncatula cell suspension cultures responding to yeast elicitor (YE) or methyl jasmonate (MeJA). Data analysis revealed three phases of intracellular response to YE: a transient response in mainly (iso)flavonoid metabolites such as formononetin and biochanin A that peaked at 12-18 h following elicitation and then declined; a sustained response through 48 h for compounds such as medicarpin and daidzin; and a lesser delayed and protracted response starting at 24 h post-elicitation, e.g. genistein diglucoside. In contrast, most compounds excreted to the culture medium reached maximum levels at 6-12 h post-elicitation and returned to basal levels by 24 h. The response to MeJA differed significantly from that to YE. Although both resulted in accumulation of the phytoalexin medicarpin, coordinated increases in isoflavonoid precursors were only observed for YE and not MeJA-treated cells. However, MeJA treatment resulted in a correlated decline in isoflavone glucosides, and did not induce the secretion of metabolites into the culture medium. Three novel methylated isoflavones, 7-hydroxy-6,4'-dimethoxyisoflavone (afrormosin), 6-hydroxy-7,4'-dimethoxyisoflavone (alfalone), and 5,7-dihydroxy-4',6-dimethoxy isoflavone (irisolidone), were induced by YE, and labeling studies indicated that the first two were derived from formononetin. Our results highlight the metabolic flexibility within the isoflavonoid pathway, suggest new pathways for complex isoflavonoid metabolism, and indicate differential mechanisms for medicarpin biosynthesis depending on the nature of elicitation.




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