New Insights into the Shikimate and Aromatic Amino Acids Biosynthesis Pathways in Plants

Molecular Plant

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Volume 3

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Number 6

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Pages 956–972

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November 2010

REVIEW ARTICLE

New Insights into the Shikimate and Aromatic Amino Acids Biosynthesis Pathways in Plants Vered Tzin and Gad Galili1 Department of Plant Sciences, The Weizmann Institute of Science, Rehovot 76100, Israel

Key words: Carbon metabolism; metabolomics; metabolic regulation; primary metabolism; secondary metabolism— phenylpropanoids and phenolics; volatiles.

INTRODUCTION The aromatic amino acids (AAA), phenylalanine (Phe), tyrosine (Tyr), and tryptophan (Trp) are central molecules in plant metabolism. These amino acids are also essential compounds in the diets of humans and monogastric livestock, which are unable to synthesize them (Galili and Hoefgen, 2002; Li and Last, 1996). In particular, Trp contributes to the nutritional quality of plant-based foods, along with the other essential amino acids lysine, methionine, and threonine (Wakasa and Ishihara, 2009). The AAA are also industrially used for the production of the low-calorie sweetener aspartame and of the monoamine neurotransmitters serotonin, dopamine (the anti-Parkinson’s disease drug L-dopa), epinephrine, and norepinephrine in the central and peripheral nervous systems of most mammalian species (Facchini et al., 2000; Wakasa and Ishihara, 2009). The biosynthetic pathways of AAA and their regulation have been extensively explored in bacteria because of their utility in the food and drug industry. In bacteria, fungi, and plants, the three AAA are synthesized from the common precursor metabolite chorismate, which originates from the shikimate pathway (Figure 1). In bacteria, this AAA pathway is almost exclusively used to for protein synthesis, but in plants, the AAA also serve as precursors for a variety of plant hormones, such as auxin and salicylate, as well as for a very wide range of aromatic secondary metabolites with multiple biological functions and biotechno-

logical values (Bartel, 1997; Vogt, 2010). Additionally, the shikimate pathway enzyme 5-enolpyruvylshikimate-3-phospate synthase (EPSPS) is the target of the glyphosate herbicide, and non-plant EPSPS provides the herbicide-resistance trait in a number of commercial transgenic crops (Duke and Powles, 2008). These important properties account for the major motivation to elucidate the regulation of the shikimate and AAA biosynthesis pathways in plants. Despite the extreme significance of the AAA to the lifecycles of plants, the regulation their biosynthesis via the shikimate and AAA biosynthesis pathways has been largely ignored and even not reviewed in the last decade. The present review focuses on new insights into the regulation of the shikimate pathway and AAA biosynthesis. A more extensive background on the biochemistry of the shikimate and AAA biosynthesis pathways is available in the following outstanding and most recent reviews dating to the years 1995 and 1999: Herrmann (1995) and Herrmann and Weaver (1999). 1 To whom correspondence should be addressed. E-mail gad.galili@ weizmann.ac.il, fax +972-8-9344181, tel. +972-8-9343511.

ª The Author 2010. Published by the Molecular Plant Shanghai Editorial Office in association with Oxford University Press on behalf of CSPP and IPPE, SIBS, CAS. doi: 10.1093/mp/ssq048, Advance Access publication 3 September 2010 Received 18 June 2010; accepted 2 August 2010

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ABSTRACT The aromatic amino acids phenylalanine, tyrosine, and tryptophan in plants are not only essential components of protein synthesis, but also serve as precursors for a wide range of secondary metabolites that are important for plant growth as well as for human nutrition and health. The aromatic amino acids are synthesized via the shikimate pathway followed by the branched aromatic amino acids biosynthesis pathway, with chorismate serving as a major intermediate branch point metabolite. Yet, the regulation and coordination of synthesis of these amino acids are still far from being understood. Recent studies on these pathways identified a number of alternative cross-regulated biosynthesis routes with unique evolutionary origins. Although the major route of Phe and Tyr biosynthesis in plants occurs via the intermediate metabolite arogenate, recent studies suggest that plants can also synthesize phenylalanine via the intermediate metabolite phenylpyruvate (PPY), similarly to many microorganisms. Recent studies also identified a number of transcription factors regulating the expression of genes encoding enzymes of the shikimate and aromatic amino acids pathways as well as of multiple secondary metabolites derived from them in Arabidopsis and in other plant species.

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Enzyme names are given on the right of the arrows, with their shortened names given inside parentheses. The metabolites are indicated above the first arrow, in between the intermediate arrows and in the bottom of the last arrow.

THE SHIKIMATE PATHWAY: CONNECTING PRIMARY METABOLISM TO AROMATIC AMINO ACIDS BIOSYNTHESIS Enzymes of the Shikimate Pathway in Plants The shikimate pathway initiates from phosphoenolpyruvate (PEP) and erythrose 4-phosphate (E-4P) and comprises seven reactions catalyzed by six enzymes to produce chorismate. PEP and E-4P are respectively derived from the glycolysis and the non-oxidative branch of the pentose phosphate pathways, thus connecting the shikimate pathway to central carbon metabolism. The first enzyme of the shikimate pathway, 3-deoxy-d-arabino-heptulosonate-7-phosphate synthase (DAHPS; EC 2.5.1.54), catalyzes the formation of 3dehydroquaianate from PEP and E4-P (Figure 2). This enzyme requires Mn2+ and reduced thioredoxin (TRX) for activity, thereby linking carbon flow into the shikimate pathway to electron flow from photosystem I (Entus et al., 2002). In Arabidopsis plants, the DAHPS1 gene is induced by physical wounding and methyl-jasmonate (Devoto et al., 2005; Yan et al., 2007) infiltration with pathogenic Pseudomonas syringae strains (Keith et al., 1991), redox state (Entus et al., 2002), and ABA (Catala et al., 2007; Leonhardt et al., 2004). The next enzyme is 3-dehydroquinate synthase (DHQS; EC 4.2.3.4), which

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catalyzes the formation of 3-dehydroquinate from 3-deoxy-darabino-heptulosonate-7-phosphate. The third and fourth enzymatic steps are catalyzed by the bi-functional enzyme 3dehydroquinate dehydratase/shikimate 5-dehydrogenase (DHQ/SDH; EC 4.2.1.10 and EC 1.1.1.25), leading to the formation of shikimate. The Arabidopsis AtDHQ/SDH gene was shown to be required for female gametophyte development and function (Pagnussat et al., 2005), connecting the shikimate pathway to plant reproduction. The crystal structure of Arabidopsis DHQ/ SDH with shikimate bound at the SDH site and tartrate at the DHQ site has recently been elucidated (Singh and Christendat, 2006). The interactions observed in the DHQ–tartrate complex reveal a conserved mode for substrate binding between the plant and microbial DHQ dehydratase family of enzymes. The arrangement of the two functional domains of this enzyme also suggests that the control of metabolic flux through the shikimate pathway is achieved by increasing the effective concentration of the intermediate substrate, 3-dehydroshikimate, through the proximity of the two sites (Singh and Christendat, 2006). While Arabidopsis plants possess only a single DHQ/SDH gene, tobacco plants possess two genes (Bonner and Jensen, 1994). RNAi-mediated suppression of either of the two tobacco NtDHQ/SDH1 and NtDHQ/SDH2 genes altered the steady state levels of the pathway substrates dehydroquinate and shikimate (Ding et al., 2007). Tomato possesses two alternatively spliced DHQ/SDH transcripts that differ by 57 bp within the coding regions. The longer transcript constitutes only 1–2% of total DHQ/SDH transcripts and cannot complement E. coli DHQ/ SDH-null mutants, implying that this transcript is non-functional in planta (Bischoff et al., 2001). Shikimate kinase (SK; EC 2.7.1.71) catalyzes the fifth reaction of the shikimate pathway, converting shikimate to shikimate 3-phosphate (Figure 1). Arabidopsis plants possess two SK isoforms—AtSK1 and AtSK2—as well as two non-catalytic homologs, which have been present in all major plant lineages for over 400 million years. It has been suggested that these two genes may have evolved a new enzymatic function that is not related to the shikimate pathway (Fucile et al., 2008). Rice plants (Oryza sativa) possess three SK genes that are deferentially expresses: OsSK1 and OsSK2 are induced in rice calli by treatment with the elicitor N-acetylchitoheptaose, and expression of OsSK1 and OsSK3 is up-regulated specifically during the heading stage of panicle development (Kasai et al., 2005). 5-Enolpyruvylshikimate 3phosphate synthase (EPSPS; CE 2.5.1.19), which catalyzes the formation of enolpyruvylshikimate 3-phosphate (EPSP), is the next enzymatic reaction (Klee et al., 1987). The expression of the EPSPS gene is induced in response to infection by the necrotrophic fungal pathogen Botrytis cinerea (Ferrari et al., 2007) and by sulfate starvation (Nikiforova et al., 2003). Importantly, the plant EPSPS enzymes are competitively inhibited by the herbicide N-phosphonomethylglycine (glyphosphate, an analog of PEP), the consequence of which is a diminished flux of the shikimate pathway (Healy-Fried et al., 2007). Therefore, this enzyme has been broadly studied for the last ;30 years due to its association with resistance to the herbicide glyphosphate,

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Figure 1. The Shikimate Pathway Converting Phosphoenolpyruvate and Erythrose 4-Phosphate into Chorismate in Higher Plants.

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Evolutionary Origins and Cell Compartment of the Shikimate Pathway in Plants Genes encoding enzymes of the entire shikimate pathway have been identified in Arabidopsis and other plant species,

Figure 2. Summary of the Evolution of the Shikimate Pathway and Its Intracellular Compartmentation in the Eukaryotic Plants. The top rectangle depicts the structural organization of the shikimate pathway enzymes and their cytosolic localization in the common eukaryotic ancestor of plants and animals. The middle rectangle summarizes the evolution of the shikimate pathway enzymes leading to the last common ancestor of plants before the speciation of lower and higher plants. The bottom right and left rectangles depict the current organization of the shikimate pathway enzymes in algae (right) and higher plants (left). The evolutionary processes included: (1) conversion of the AroM pentafunctional polypeptide containing DHQS-DHQ-SDH-SK-EPSPS enzymes (top panel), a bi-functional polypeptide containing linked DHQ- SDH plus five polypeptides each containing the single enzymes DAHPS (class I), DHQS, SK, EPSPS, CS enzymes; and (2) evolution of a plastid transit peptide in the C-terminal domain of all seven polypeptides to direct these enzymes into the organelle where the shikimate pathway operates in higher plants. Modified and simplified from Richards et al. (2006).

mostly due to their homology genes from microbial organisms. However, it is noteworthy that genes of the shikimate pathway in plants apparently do not originate from a single prokaryotic ancestor of cyanobacterial origin, but are likely derived from at least three different sources. A complex, multi-step shuffling of loss and gain of function occurred during phylogeny of this pathway, which might explain the multiple factors contributing to the genomic organization and expression of the pathway genes in plants (Figure 2) (Richards et al., 2006). The last eukaryotic common ancestor possessed DHAP class I and II enzymes, CS, and a long polypeptide that includes five enzyme activities of the shikimate pathway (penta-functional polypeptide named AroM; enzymatic steps 2–6; Figure 2). The Arom polypeptide and DHAP class I genes were lost during evolution and do not appear in many eukaryotic lineages, including plants. Therefore, the seven genes of the shikimate pathway in plants have been serially acquired by endosymbiotic gene transfer (EGT) and horizontal gene transfer (HGT). Two of the phylogenies suggest a derivation of the plant genes from the cyanobacterial plastid progenitor genome, but if the full plant pathway was originally of cyanobacterial origin, then the five other shikimate pathway genes were obtained from a minimum of two other eubacterial genomes (Figure 2). Thus, the phylogenies demonstrate the occurrence of both separate and shared derived HGTs either by primary HGT transfer or secondarily via the plastid progenitor genome in plants evolution (Figure 2) (Moustafa et al., 2008; Richards et al., 2006). A portion of the proteins that are targeted to plastids in higher plants do not seem to have been acquired from cyanobacteria, but rather to have evolved from the host eukaryotic genome (Timmis et al., 2004). In addition, following the endosymbiotic event, new shikimate pathway enzymes containing plastid transit peptide involved in protein targeting from the cytosol into plastids as well as metabolites transport mechanisms have been evolved (Tyra et al., 2007; Vothknecht and Soll, 2005). Therefore, the shikimate enzymes of higher plants are generally synthesized as precursors containing a plastid transit peptide that directs them to the plastid (Figure 2) (Mustafa and Verpoorte, 2005; Weber et al., 2005; Zybailov et al., 2008). In addition, two shikimate pathway enzymes are chimaric: DHQ/SDH (Richards et al., 2006). A similar evolutionary chimerism of enzymes has been found in other plastidic metabolic pathways, such as the calvin cycle (Martin and Schnarrenberger, 1997; Reyes-Prieto and Bhattacharya, 2007) and methylerythritol phosphate pathway (Matsuzaki et al., 2008). Conversely, the excavate Euglenozoa possesses two DAHPS (class II) paralogs (Simpson, 2003). The species Euglena gracilis possesses two DAHPSs class II enzymes that are differentially expressed during light-induced chloroplast development and known to possess both a cytosolic and a plastid-associated shikimate pathway (Reinbothe et al., 1994).

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which is the basis for the Roundup-Ready transgenic crops (Duke and Powles, 2008; Singer and McDaniel, 1985; Smart et al., 1985). The last step of the shikimate pathway is catalyzed by chorismate synthase (CS; CE 4.2.3.5), which converts EPSP to chorismate (Figure 1). Arabidopsis possesses a single CS gene in contrast to tomato plants, which possess two differentially expressed CS genes, termed LeCS1 and LeCS2 (Gorlach et al., 1993). Chorismate is a central metabolite in plant cells, serving as a precursor for the synthesis of the three AAA and also as an initiator substrate for the synthesis of a number of other metabolites, such as: tetrahydrofolate (vitamin B9) (Basset et al., 2004; Waller et al., 2010), isochorismate 3 on route to the production of salicylate (Garcion et al., 2008; Wildermuth et al., 2001), phylloquinone (vitamin K1), and a number of pigments (Gross et al., 2006; Kim et al., 2008).

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ENZYME AND METABOLIC ROUTES IN THE BIOSYNTHESIS OF PLANT AROMATIC AMINO ACIDS The Biosynthesis of Phe

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arogenate has been reported in plants (De-Eknamkul and Ellis, 1988; Siehl et al., 1986), no gene encoding such an activity has so far been reported. An in silico data-mining approach identified six putative ADT genes in Arabidopsis and biochemical characterization of their recombinant enzymes suggested that all of them possess arogenate dehydratase activity, converting arogenate into Phe (Figure 3) (Cho et al., 2007). Yet, three of them (ADT1, ADT2, and ADT6) can also utilize prephenate as a substrate and convert it to PPY (Figure 3), even though they exhibit a major preference for arogenate (Cho et al., 2007). A rice 5-methyl-Trp-resistant mutant, called Mtr1, which overaccumulates Phe, Trp, and several phenylpropanoids in callus tissue and leaves, appeared to result from a point mutation in a gene encoding an enzyme possessing primarily ADT and also some minor PDT activities, rending these activities insensitive to feedback inhibition by Phe (Yamada et al., 2008). Recently, three genes encoding ADT isozymes, which preferentially use arogenate, but can also use at a lower efficiency prephenate as substrates, were also characterized in petunia (Petunia hybrida), supporting the preferential utilization of the arogenate route rather than the PPY route for Phe biosynthesis in plants (Maeda et al., 2010). Interestingly, feeding shikimate into petunia petals with suppressed expression of ADT1 (the major ADT enzyme in petunia) led to the accumulation of prephenate as well as PPY, and also to partial recovery of the reduced Phe level, strongly indicating that petunia plants can also synthesize Phe via the PPY route, although at very low efficiency. To study the consequence of producing PPY in plants by metabolic engineering, we have expressed in transgenic

Figure 3. The Biosynthesis Pathways of the Aromatic Amino Acids in Plants. Enzyme names are given next to the arrows, with their shortened names given inside parentheses. The metabolites are indicated above the first arrow, in between the intermediate arrows and in the bottom of the last arrow. The major route of Tyr and Phe biosynthesis from arogenate is indicated by wider arrows, while the still questionable route of Phe biosynthesis via phenypyruvate and Tyr biosynthesis via p-hydroxyphenylpyruvate are indicated by narrower arrows.

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The first committed step of Phe biosynthesis from chorismate is catalyzed by chorismate mutase (CM) (CE 5.4.99.5), which converts chorismate to prephenate (Figure 3). Three CM genes have so far been described in Arabidopsis (AtCM1-3) (Mobley et al., 1999). These AtCM genes are differentially expressed in various tissues and the expression of only AtCM1 is induced by various elicitors and pathogens (Ehlting et al., 2005; Mobley et al., 1999). The activities of the three Arabidopsis CM isoforms were identified by the fact that they can complement E. coli and yeast CM-deficient strains (Eberhard et al., 1996, 1993). The activities of AtCM1 and AtCM3 are inhibited by Phe and Tyr, whereas the activity of AtCM2 appears to be insensitive to these amino acids (Eberhard et al., 1996). The last two enzymatic steps converting prephenate to Phe in plants are still not entirely elucidated. The major route involves the conversion of chorismate via prephenate and arogenate to Phe, catalyzed by respective enzymes prephenate aminotransferase (PAT; CE 2.6.1.79) and arogenate dehydratase (ADT; CE 4.2.1.49) (Cho et al., 2007; Maeda et al., 2010; Yamada et al., 2008) (Figure 3). Yet, it is still questionable whether plants can also convert some minor amount of prephenate via phenylpyruvate (PPY) to Phe, using enzymes with prephenate dehydratase (PDT) and Phe aminotransferase activities in a similar manner to E. coli and various other microorganisms. Although the enzymatic activity of PAT of converting prephenate into

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The Biosynthesis of Tyr The major route of Tyr biosynthesis initiates from chorismate, using the same first two enzymes of Phe biosynthesis, namely CM and PAT, to produce arogenate (Figure 3). Arogenate is then converted into Tyr by arogenate dehydrogenase (TyrA; CE 1.3.1.43; Figure 3), whose activity has been demonstrated in tobacco (Gaines et al., 1982), maize (Byng et al., 1981), sorghum (Connelly and Conn, 1986), and Arabidopsis (Rippert and Matringe, 2002a; Rippert et al., 2009). An alternative route of Tyr biosynthesis has also been suggested, which includes the conversion of prephenate to p-hydroxyphenylpyruvate (p-hydroxyPPY) by prephenate dehydrogenase (PDH; CE 1.3.1.43), which may be catalyzed by TyrA2 (Rippert and Matringe, 2002a). Subsequently, p-hydroxyPPY is converted into Tyr by a broad range aromatic amino acid aminotransferase (AAAAT; Figure 2). Nevertheless, at a non-saturating concentration of prephenate, the TyrA2 enzymatic activity is 2000 times less efficient in catalyzing the reaction with prephenate than with arogenate (Rippert and Matringe, 2002b), and therefore it is still questionable if such an alternative route for Tyr biosynthesis using PDH does exist in plants. The enzymes of the Phe and Tyr biosynthesis pathways are generally localized in the plastid (Mustafa and Verpoorte, 2005; Rippert et al., 2009; Weber et al., 2005; Zybailov et al., 2008), with two potential exceptions: CM2 and ADT3. A tobacco polypeptide suggested to contain CM2 activity was shown to be localized in the cytosol (d’Amato et al., 1984), but whether this polypeptide indeed possesses CM activity has not been confirmed. Although in vitro studies showed that the Arabidopsis AtCM2 possesses CM activity (Eberhard et al.,

1996, 1993), the physiological significance of AtCM2 still remains questionable (Rippert et al., 2009). In addition, an Arabidopsis polypeptide termed PDT1 (which corresponds to the ADT3 isozyme of Phe biosynthesis, characterized by Cho et al. 2007), was suggested to be a component of the heterotrimeric G-protein complex that is associated with the plasma membrane (Warpeha et al., 2006). This observation is in contrast to a more recent report using an in situ microscopy analysis, which showed that all of the Arabidopsis ADT isozymes are localized in the plastid (Rippert et al., 2009). Thus, the current dogma implies that all ADT isozymes are generally localized to the plastid, although it cannot be ruled out that under specific growth stages or physiological conditions, ADT3 may also be associated with other complexes before it is post-translationally transported into the plastid.

The Biosynthesis in Trp The first committed step of Trp biosynthesis includes a transfer of an amino group of Gln to chorismate to generate anthranilate and pyruvate, catalyzed by anthranilate synthase (AS; CE 4.1.3.27; Figure 3). Purified plant AS holoenzymes are suggested to be heterotetramers composed of two alpha and two beta subunits (Niyogi et al., 1993; Poulsen et al., 1993). The a subunit possesses the catalytic activity, while the b subunit possesses an aminotransferase activity, which transfers an amino group from Gln to the a subunit. AS activity in plants is feedback inhibited by Trp through binding of Trp to the a subunit. Expression of mutated genes encoding feedbackinsensitive AS enzymes in a variety of plant species generally increases the production of free Trp and secondary metabolites derived from it (Hughes et al., 2004; Li and Last, 1996; Tozawa et al., 2001). The trp4 mutation in the gene encoding the Arabidopsis ASb1 suppresses the accumulation of the product of this enzyme, anthranilate (Niyogi et al., 1993). Anthranilate possesses a strong blue fluorescence under UV light—a characteristic that was used as a phenotypic marker for indentifying Arabidopsis mutants in Trp biosynthesis enzymes (Radwanski and Last, 1995; Radwanski et al., 1995; Rose et al., 1992). The second enzyme in the Trp biosynthesis pathway is anthranilate phosphoribosylanthranilate transferase (PAT1; CE 2.4.2.18), converting anthranilate and phosphoribosylpyrophosphate into phosphoribosylanthranilate and inorganic pyrophosphate (Figure 3). Expression of the Arabidopsis PAT1 gene is apparently controlled by regulatory elements located inside introns, as inclusion of introns was shown to enhance the expression of stably transformed PAT1–GUS fusion constructs in Arabidopsis (Rose and Beliakoff, 2000). The third enzyme in the Trp biosynthesis pathway is phosphoribosylanthranilate isomerase (PAI) (CE 5.3.1.24), converting phosphoribosylanthranilate into l-(O-carboxyphenylamino)-l-deoxyribulose-5-phosphate (CDRP) (Figure 3). The Columbia ecotype of Arabidopsis possesses three genes encoding PAI isoforms: PAI1 (At1g07780), PAI2 (At5g05590), and PAI3 (At1g29410). Expression of these three Arabidopsis genes is differentially regulated under normal growth

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Arabidopsis plants a mutant E. coli PheA* gene encoding a feedback-insensitive bi-functional CM/PDT enzyme that converts chorismate via prephenate to PPY (Tzin et al., 2009). PheA* expression caused a significant increase in the level of Phe, with no measurable increase in the level of PPY. Although it is likely that a considerable amount of the prephenate, produced by the CM activity of the bacterial CM/PDT enzyme, was converted via arogenate to Phe using the ADT enzyme (Figure 3), the fact that these plants showed no increased level of PPY implies that Arabidopsis apparently possesses an endogenous aromatic amino acid aminotransferase (AAAAT) activity that can covert the PPY produced by the bacterial enzyme into Phe (Tzin et al., 2009) (Figure 3). Yet, no gene encoding an AAAAT that can specifically convert PPY into Phe (CE 2.6.1.57) has so far been identified in plants. Hence, taken together, the studies described above imply that plants use primarily the arogenate route for the synthesis of Phe, although some minor function of the PPY route in Phe biosynthesis cannot be ruled out. This is also supported by the observation that a number of plant species contain PPY, which also serves as a precursor for a number of volatile compounds such as phenylacetaldehyde, 2-phenylethanol, and 2-phenylethyl b-d glucopyranoside (Kaminaga et al., 2006; Watanabe et al., 2002).

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generally synthesized as precursors containing a plastid transit peptide, implying their localization in this organelle (Mustafa and Verpoorte, 2005; Weber et al., 2005; Zybailov et al., 2008).

POST-TRANSLATIONAL REGULATION BY ENZYME FEEDBACK-INHIBITION LOOPS The activities of DAHPS enzymes from various microorganisms are generally regulated by allosteric feedback inhibition by the different AAA (Byng et al., 1983; Knaggs, 2001). In contrast, there is no published evidence showing that plant DAHPS enzymes are strongly allosterically inhibited in vivo by any of the AAA (Gilchrist and Kosuge, 1980; Herrmann and Weaver, 1999). Yet, the in vitro activities of DAHPSs from different plant species are weakly inhibited by Trp (Graziana and Boudet, 1980; Rubin and Jensen, 1985) and Tyr (Reinink and Borstap, 1982), or weakly activated by either Trp or Tyr (Pinto et al., 1986; Suzich et al., 1984) (Figure 4A). The activity of Vigna radiate (bean) DAHPS is weakly inhibited by the precursor metabolites of Phe and Tyr biosynthesis, prephenate and arogenate (Rubin and Jensen, 1985), but whether this is due to inhibition of enzyme level or activity is still unknown (Herrmann, 1995). Hence, the results obtained so far imply that the shikimate pathway in plants is mostly regulated at the gene expression level rather than by post-translational level. The AAA biosynthesis pathway in plants was so far shown to possess four allosterically regulated enzymes, namely ASa, CM, ADT/PDT, and TyrA (Figure 4A). Arabidopsis trp5 mutants, producing an ASa1 subunit that is insensitive to feedback inhibition by Trp, were extensively studied during the 1990s (Kreps et al., 1996; Li and Last, 1996). Arabidopsis and rice mutants with a feedback-insensitive ASa generally accumulate Trp, but not Phe or Tyr (Ishihara et al., 2006; Tozawa et al., 2001). The naturally occurring feedback-insensitive ASa2 gene was isolated from a tobacco suspension culture cell line that was resistant to the Trp analog, 5MT (Cho et al., 2004; Song et al., 1998; Tsai et al., 2005). In addition, overexpression of this gene was possessed in hairy roots of two legume plants, Astragalus sinicus (Cho et al., 2000) and soybean (Glycine max) (Cho et al., 2004; Inaba et al., 2007). CM is normally feedback-inhibited by Phe and Tyr and induced by Trp (Eberhard et al., 1996). To investigate the enzymatic properties of the three Arabidopsis CM isoforms, each of the AtCM cDNAs were expressed in yeast (Mobley et al., 1999). The activities of both AtCM1 and AtCM3 isozymes were feedback-inhibited by Phe and Tyr, while stimulated by Trp in contrast to AtCM2 activity that was insensitive to allostericregulated by any of the AAA (Mobley et al., 1999). Another regulated enzyme is ADT, whose activity is positively regulated by Tyr and negatively regulated by Phe. These regulations were detected in tobacco, spinach, and Sorghum bicolor (Jung et al., 1986; Siehl et al., 1986) but have not yet been characterized in Arabidopsis plants (Cho et al., 2007). The rice ADT is negatively regulated by Phe (Yamada et al., 2008), while its potential regulation by Tyr has not yet been elucidated. Finally,

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conditions, with PAI1 and PAI3 being the dominant isozymes, and PAI2 showing an ;10-fold lower expression level than PAI1 and PAI3 (He and Li, 2001). Expression of these three PAI genes is also differentially regulated by environmental stresses, such as UV irradiation and treatment with the abiotic elicitor silver nitrate in a tissue- and cell-type-specific manner (He and Li, 2001; Li et al., 1995b). Deletion of the Arabidopsis PAI1 gene caused some abnormal growth (He and Li, 2001), indicating its predominant importance in Trp biosynthesis. Interestingly, the Arabidopsis PAI gene family is regulated by methylation in the Wassilewskija, but not Columbia ecotypes (Bender and Fink, 1995; Melquist et al., 1999). The four PAI genes of Wassilewskija (PAI1–PAI4) contain inverted repeats, which trigger their methylation (Bartee and Bender, 2001; Melquist and Bender, 2003). The fourth enzyme of the Trp biosynthesis pathway is Indole-3-glycerol phosphate synthase (IGPS; EC 4.1.1.48), which catalyzes the formation of indole3-glycerol phosphate from 1-(O- carboxyphenylamino)-1deoxyribulose-5-phosphate (Figure 3) (Li et al., 1995a). IGPS provides an important enzymatic step in the biosynthesis of Trp and the hormone indole-3-acetic acid (IAA; auxin) because it is the only known enzyme that catalyzes the formation of the indole ring. Quantitative comparison of the relative levels of Trp and IAA content in different Arabidopsis Trp biosynthesis mutants as well as in transgenic plants expression an IGPS antisense construct indicates that indole-3-glycerol phosphate is the branch-point metabolite for a de novo Trp-independent biosynthesis of IAA in Arabidopsis (Ouyang et al., 2000). Notably, the IGPS enzymes of both fungi and bacteria are synthesized as fusion proteins containing one or two other enzymes of the Trp biosynthesis pathway (Li et al., 1995a). In contrast, plant IGPS enzymes generally appear as mono-functional enzymes based on cDNA sequence and functional complementation analyses (Li et al., 1995a). The Arabidopsis gene encoding IGPS of Trp biosynthesis (Figure 3) is regulated by the hormones jasmonate (Dombrecht et al., 2007; Sasaki-Sekimoto et al., 2005) and salicylate (Rajjou et al., 2006), and also in seeds and seedlings by various defense mechanisms (Chibani et al., 2006; Job et al., 2005). The last two steps of Trp biosynthesis are catalyzed by Trp synthase (TS) (CE 4.2.1.20), which contains both a (TSa) and beta (TSb) subunits. Indole-3-glycerol phosphate is cleaved by TSa to indole and glyceraldehyde-3-phosphate (a-reaction). Then, indole is transported to TSb, which catalyzes its condensation with serine (b-reaction) to produce Trp (Miles, 2001; Weber-Ban et al., 2001). The function of TSa1 and TSb1 was demonstrated by the facultative Trp auxotroph mutants trp3 and trp2, respectively (Last et al., 1991), suggesting that the TSa1 and TSb1 subunits form an active heterodimer (Radwanski et al., 1995). The Arabidopsis TSa1 gene was cloned by functional complementation of an E. coli mutant and suggested to function as a monomer (Bohlmann et al., 1995; Radwanski and Last, 1995; Radwanski et al., 1995). Yet, whether TS activity operates as a monomer or as a multi-enzyme complex is still controversial (Kriechbaumer et al., 2008). All the enzymes of the Trp biosynthesis pathways are

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Enzyme abbreviations are as in Figure 3. Solid black lines represent established feedback inhibition loops. Solid gray arrows represent positive regulation. Dashed black and gray lines represent suggested, but not clearly proven, negative and positive regulation, respectively. This figure was modified from Berry (1996) and Sprenger (2006).

the activity of TyrA is feedback-inhibited by Tyr in Arabidopsis (Rippert and Matringe, 2002b) and Sorghum bicolor (Connelly and Conn, 1986). In comparison to plants, in many bacterial species, the AAA feedback inhibits the DAHPs activities in vivo and this inhibition is a major regulatory mechanism of this pathway (Ogino et al., 1982). In addition, enzymes converting chorismate on route to the synthesis of the AAA were evolved to be allosterically regulated by the AAA end products: Phe inhibiting CM/PDT (PheA), Tyr inhibiting CM/PDH (TyrA), and Trp inhibiting AS/PAT (TrpED) in E. coli (Berry, 1996; Ikeda, 2006; Sprenger, 2006). Interestingly, similar enzymatic committed steps are feedback-inhibited by AAA commonly in plants and bacteria; however, positive regulation was not detected in bacteria (Figure 4B).

ROOT-KNOT NEMATODES USE THE CHORISMATE MUTASE ENZYME AS A PART OF THEIR PATHOGENIC MACHINERY The shikimate pathway does not exist in animals, except for a secreted form of CM that is present in the root-knot nematode (Doyle and Lambert, 2003; Lambert et al., 1999) and potato cyst nematode (Jones et al., 2003). Although these species of nematodes possess either a single or two CM genes, they still lack the other genes of the shikimate and AAA biosynthesis pathways (Bekal et al., 2003; Lambert et al., 1999; Popeijus et al., 2000). These organisms specifically express these CM genes in the esophageal glands (Bekal et al., 2003; Lambert et al., 1999; Popeijus et al., 2000). Transgenic expression of the Meloidogyne javanica nematode MjCM1gene in plant roots suppresses lateral root formation and the development of the vascular system, which can be rescued by exogenous ap-

plication of IAA, suggesting that the expression of MjCM1 reduces auxin levels (Doyle and Lambert, 2003). Since chorismate is also a precursor for the synthesis of the plant hormones auxin and salicylate, the expression of the MjCM1 in plant cells apparently competitively reduces the fluxes towards (1) the synthesis of Trp and its downstream hormone auxin, and (2) the synthesis of salicylate directly from chorismate. Because plants have the shikimate pathway and nematodes have a secreted form of CM, this nematode enzyme is thought to be involved in the alteration of the plant’s pathway (Yan et al., 1998). Several parasitism genes isolated from sedentary plant-parasitic nematodes have been identified as putative candidates for horizontal gene transfer from bacteria including b-1,4-endoglucanases (cellulases), pectinases, CM, glutamine and polyglutamate synthetases, l-threonine aldolase, and Nod factors (Scholl et al., 2003; Yan et al., 1998).

AROMATIC AMINO ACIDS CATABOLISM IN PLANTS Phe: A Substrate of a Large Array of Multiple Functional Secondary Metabolites Phe serves as a precursor for a large array of multiple functional secondary metabolites, including phenylpropanoids, flavonoids, cell wall lignin, anthocyanins, and numerous other metabolites. The metabolite composition of the phenylpropanoids, which possess multiple functions, particularly protecting against various abiotic and biotic stresses (Casati and Walbot, 2005; Dixon, 2001), has been recently discussed in several excellent reviews, examples of which are Boudet (2007), D’Auria and Gershenzon (2005), Pichersky and Gang (2000), Vogt (2010), and Weisshaar and Jenkins (1998). The first step

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Figure 4. Post-Transcriptional Regulation of the Shikimate and Aromatic Amino Acid Biosynthesis Pathways in Plants (Panel A) and E. coli (Panel B).

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phenylacetaldoxime, the precursor of benzylglucosinolate (Wittstock and Halkier, 2000).

Tyr: A Precursor for Tocochromanols, Tyramine, and Important Non-Protein Amino Acids Tyr serves as a precursor of several families of secondary metabolites, including, for example, tocochromanols (vitamin E), plastoquinones, isoquinoline alkaloids, several non-protein amino acids, and perhaps also some phenylpropanoids (Figure 5). The tocochromanols (tocopherols and tocotrienols) are essential antioxidants in the diets of human and farm animals (DellaPenna and Pogson, 2006; Mene-Saffrane and Dellapenna, 2009; Schneider, 2005). Tyr-aminotransferase (TAT; CE 2.6.1.5) is the committed enzyme of tocochromanols biosynthesis (Lopukhina et al., 2001), converting Tyr into phydroxyPPY (Garcia et al., 1999; Norris et al., 1995). It has been suggested that p-hydroxyPPY can also be synthesized from prephenate via an alternative biosynthesis pathway (Figure 5) (Rippert and Matringe, 2002a; Rippert et al., 2004). If such a pathway indeed naturally exists, then p-hydroxyPPY can also be used for tocochromanols biosynthesis, bypassing Tyr. In some plant species, the second metabolite of the phenylpropanoid pathway, namely coumarate, may not only be synthesized from Phe, but may also be synthesized directly from Tyr by Tyr ammonia-lyase (TAL; EC 4.3.1) (MacDonald and D’Cunha, 2007; Neish, 1961). Evidence supporting the presence of TAL activity was described in several plant species, including tobacco (Beaudoin-Eagan and Thorpe, 1985), wheat (Guerra et al., 1985), maize (Rosler et al., 1997), soybean (Khan et al., 2003), and Arabidopsis (Cochrane et al., 2004; Watts et al., 2006). Interestingly, expression of the bacterial Rhodobacter sphaeroides TAL gene in Arabidopsis enhanced the metabolic flux into the phenylpropanoid pathway and resulted in

Figure 5. Major Classes of Secondary Metabolites Derived from Chorismate, Phe, Tyr, and Trp.

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of Phe catabolism is catalyzed by Phe-ammonia lyase (PAL; CE 4.3.1.5), whose encoding genes are generally highly regulated in various plant species by different biotic and abiotic stresses, as well as by conditions that demand increased production of the cell wall component lignin (Anterola and Lewis, 2002). Mutations affecting the synthesis of PAL are generally associated with significant alterations in the levels of multiple phenylpropanoids (Rohde et al., 2004; Shadle et al., 2003). An Arabidopsis double mutant lacking PAL1 and PAL2 activities was shown to possess an ;100-fold increase in Phe and a four-fold increase in Trp levels (Rohde et al., 2004). This pal1 and pal2 double mutant is also associated with an altered transcription level of genes connected to the AAA biosynthesis network as well as genes associated with phenylpropanoid secondary metabolites (Rohde et al., 2004). Genomics approaches have been used to decipher new organ-specific metabolic routes of Phe catabolism, such as the formation of tapetum-specific trisacyl–polyamine conjugates of Arabidopsis flower buds (Alves-Ferreira et al., 2007; Ehlting et al., 2008; Fellenberg et al., 2009; Matsuno et al., 2009). Examples of important steps in phenylpropanoid biosynthesis that were resolved only recently include: (1) the involvement of 2-hydroxylation in coumarate biosynthesis (Kai et al., 2008); (2) the independent regulation of flavonoids and lignin biosynthesis in Arabidopsis plants exhibiting growth retardation due to repressed lignin biosynthesis (Li et al., 2010); (3) genomics approaches also revealed new organ-specific pathways, such as the formation of tapetum-specific trisacyl–polyamine conjugates of Arabidopsis flower buds (Alves-Ferreira et al., 2007; Ehlting et al., 2008; Fellenberg et al., 2009; Matsuno et al., 2009); and (4) an alternative biochemical pathway of syringyl–lignin biosynthesis in higher plants (Weng et al., 2010). Nearly 1% of the secondary metabolites derived from Phe are volatile compounds involved in plant reproduction and defense response. Nearly 20% of these volatile metabolites are aromatic components of phenylpropanoids, benzenoids, phenylpropenes, and nitrogen-containing aromatics (Dudareva et al., 2006; Kaminaga et al., 2006; Schaller, 2008). Other groups of Phe-derived volatile compounds include methylbenzoate, phenylethylacetate, 2-phenylethanol, and isoeugenol (Baldwin et al., 2004; Ben Zvi et al., 2008; Gonda et al., 2010; Klee, 2010; Schuurink et al., 2006; Tieman et al., 2006; Verdonk et al., 2003; Watanabe et al., 2002). Another class of sulfur-rich Phe-derived secondary metabolites includes the Phe-glucosinolates, whose basic skeleton consists of a bthioglucose residue, an N-hydroxyiminosulfate moiety, and a variable side chain (Reichelt et al., 2002). Phe-glucosinolates are generally not widespread in Arabidopsis, but some Arabidopsis ecotypes do synthesize these compounds, such as phenylethyl-glucosinolate in the leaves (Mikkelsen et al., 2004) and benzoyloxy-glucosinolates in seeds (Kliebenstein et al., 2007). The committing gene in the biosynthesis of Phe-glucosinolates is the cytochrome P450 CYP79A2 (CE 1.14.13) encoding an N-hydroxylase that converts Phe into

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and plant–pathogen interactions, and also recently attracted attention as cancer-preventive agents in humans (Halkier, 1999). Glucosinolates are found almost exclusively in the Brassicales and have been widely studied in Arabidopsis and in other species of the Brassicaceae family (Rask et al., 2000; Reichelt et al., 2002; Yatusevich et al., 2009). The IAOx, described above, is also channeled by the oxime-metabolizing CYP83B1 enzyme into the biosynthetic pathway of indole glucosinolates (Naur et al., 2003). Camalexin, the major indolic phytoalexin accumulating in Arabidopsis upon infection with plant pathogens and abiotic elicitors is also derived from Trp (Bottcher et al., 2009; Zhao and Last, 1996). In a genetic screen for camalexin-deficient mutants, phytoalexin deficient3 (pad3) was isolated (Glazebrook and Ausubel, 1994) and subsequently shown to be defective in another cytochrome P450 enzyme, CYP71B15, which catalyzes the final step of camalexin biosynthesis (Schuhegger et al., 2006). Extensive studies of the pad3 mutant led to the proposition that camalexin contributes to resistance against necrotrophic pathogens but not against biotrophs (Glazebrook, 2005; Kliebenstein, 2004). In addition, Trp catabolism also leads to the synthesis of indole alkaloids via tryptamine. An example of the Trp-derived indole alkaloids is vindoline, an important metabolite in human health (Facchini et al., 2004, 2000; Sugawara et al., 2009).

Trp: A Major Precursor for Multifunctional Indole Compounds Trp is catabolized into many indole-containing secondary metabolites, such as indole-3-acetic acid (IAA, auxin) (Ostin et al., 1998), indole glucosinolates (Halkier, 1999), phytoalexins (Pedras et al., 2000), terpenoid indole alkaloids (De Luca and St Pierre, 2000; Facchini et al., 2004), and tryptamine derivatives (Facchini et al., 2000) (Figure 5). Auxins are some of the key metabolites synthesized from Trp (Gibson et al., 1972; Tsurusaki et al., 1997; Wright et al., 1991), but the biosynthetic route(s) leading to the main auxin compound, IAA, are still not entirely solved. Several different routes of IAA biosynthesis from Trp have been proposed (Quittenden et al., 2009; Strader and Bartel, 2008). These include: (1) the indole-3-acetaldoxime (IAOx) pathway catalyzed by two cytochrome P450s (CYP79B2 and CYP79B3; CE 1.14.13) (Bartel et al., 2001; Hull et al., 2000); (2) the indoleacetamide pathway, which initiates from the same P450s enzymes (Pollmann et al., 2002); (3) the tryptamine (YUCCA) pathway catalyzed by Trp decarboxylase (CE 4.1.1.28) (Facchini et al., 2000; Quittenden et al., 2009); and (4) the indole-3-pyruvate pathway catalyzed by Trp aminotransferase (CE 2.6.1.1) (Stepanova et al., 2008; Tao et al., 2008). In addition, a possible additional, Trp-independent pathway of IAA biosynthesis directly from indole has been proposed (Normanly et al., 1993; Radwanski et al., 1996). Trp is also the precursor for the synthesis of a number of glucosinolates, which are amino acid-derived natural plant products containing a thio-Glc moiety and a sulfonate moiety bound to an oxime function (Halkier and Gershenzon, 2006). The glucosinolates are associated with plant–insect

TRANSCRIPTIONAL REGULATON OF THE SHIKIMATE PATHWAY AND AROMATIC AMINO ACID METABOLISM The exposure of plants to various stresses generally induces the expression of genes encoding shikimate pathway and AAA metabolism enzymes. For example, ligogalacturonides that are released from plant cell walls upon infection with the Botrytis cinerea pathogen stimulate a number of genes encoding enzymes of the shikimate and AAA biosynthesis pathways, as well as genes encoding enzymes of secondary metabolites derived from the AAA (Ferrari et al., 2007). During infection, bacterial pathogens deliver a constellation of type III effector proteins (TTEs), which are predicted to collectively suppress plant basal defenses and redirect normal host metabolism to facilitate pathogen multiplication and nutrition (Abramovitch and Martin, 2004; Alfano and Collmer, 2004). Transcripts associated with several metabolic pathways, particularly plastidbased primary carbon metabolism, pigment biosynthesis, and AAA metabolism, are significantly modified by the bacterial challenge within the first 12 h post inoculation (Truman et al., 2006). This basal defense response also includes various cell wall modifications that are likely needed to restrict the passage of nutrients and water from the plant to the invading bacteria (Kocal et al., 2008; Truman et al., 2006). Several transcription factors (TFs) encoding genes of the shikimate and AAA biosynthesis pathways were described. Overexpression of AtMYB15 in Arabidopsis plants elevates the

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increased accumulation of flavonoids and phenylpropanoids (Nishiyama et al., 2010). The Tyr catabolism pathway also synthesizes isoquinoline alkaloids, a large, diverse group of natural products that are produced in ;20% of all plant species (Facchini et al., 2004). In Arabidopsis, Tyr is also catabolized into tyramine by Tyr/ L–dopa decarboxylase (TYDC; EC 4.1.1.25) on route for the production of benzyl-isoquinoline alkaloids, as well as of cell wallbound hydroxycinnamic acid amides (Facchini et al., 2000). Tyramine has also been suggested to be involved in the Arabidopsis defense response (Trezzini et al., 1993). Meta-Tyr (m-Tyr) is a non-protein amino acid that is naturally synthesized in some plant species, such as fescue grasses (Festuca spp.). Exposure to m-Tyr inhibits the growth of a wide range of plant species by slowing down root development (Bertin et al., 2007). This inhibition can be explained by the possibility that m-Tyr can be mis-incorporated into proteins in position of Phe by eukaryotic Phe-tRNA synthetases (Duchene et al., 2005; Klipcan et al., 2009). Recently, an Arabidopsis mutant resistant to the phytotoxic amino acid m-Tyr was isolated (Huang et al., 2010). This resistance is due to a dominant point mutation in the regulatory domain of ADT2 and is also associated with altered levels of several primary and secondary compounds (Huang et al., 2010).

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enzymes of the phenylpropanoid pathway (Spitzer-Rimon et al., 2010). The TF MYB12 of Arabidopsis is a specific activator of flavonoid biosynthesis, regulating the expression of genes encoding various enzymes of flavonoid biosynthesis, including chalcone synthase, chalcone flavanone isomerase, flavanone 3-hydroxylase, and flavonol synthase (Mehrtens et al., 2005). Recent studies of the pink-colored Solanum lycopersicum (tomato) fruit ‘y’ mutation, known to result in colorless epidermis, suggested that SlMYB12 is a likely candidate for the y mutation (Adato et al., 2009; Ballester et al., 2010). TFs regulating the biosynthesis of glucosinolates, a class of secondary metabolites derived mainly from Trp and Met, have also been recently identified. Two clades of Arabidopsis TF genes, encoding ‘altered Trp regulation1’ [ATR1]-like and MYB28-like (MYB29, MYB34, MYB51, MYB76 and MYB122) were shown to be involved in the biosynthesis of glucosinolates. Overexpression of these TFs in Arabidopsis stimulates the expression of specific genes encoding enzymes of both the shikimate pathway, Trp biosynthesis pathway, as well as enzymes of Trp-derived glycosinolates (Gigolashvili et al., 2007; Malitsky et al., 2008). In bacterial species, the genes encoding Phe and Tyr biosynthesis enzymes are located in close regions on the chromosome, distinct from the location of the genes encoding the operon-Trp biosynthesis pathway (Berry, 1996; Ikeda, 2006; Sprenger, 2006). This suggests a separate regulation of the Phe/Tyr branch and the Trp branch of AAA biosynthesis. Interestingly, the Phe/Tyr branch and the Trp branch in plants also appear to be under separate control. A bioinformatic approach has recently shown that UV stress stimulates only the catabolic PAL and TAT genes, but not genes encoding the biosynthesis enzymes of these AAA. In contrast, this same stress stimulates the expression level of genes encoding both biosynthesis and catabolic enzymes of the Trp pathway (Less and Galili, 2008).

FUTURE PROSPECT Despite the identification of entire genes and enzymes of the shikimate pathway in plants, studies concerning the regulation of this pathway and its network interaction with other metabolic pathways are still in their infancies, requiring future studies. Similarly, despite the significant advancement in the elucidation of genes and enzymes associated with biosynthesis of the AAA, there are still missing links and debates about some key regulatory steps that need to be elucidated. In addition, the network interactions of the shikimate and AAA metabolic pathways with other networks of the core primary metabolism, including, for example, glycolysis, are still mostly unknown, requiring future studies. Additional research is also needed to elucidate the fine regulation of the flux balance in the conversion of shikimate to chorismate and the further conversion of chorismate into Trp and Phe/Tyr. Although a number of transcription factors have been proven to control different

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expression of almost all the genes involved in the shikimate pathway, implying that it is a direct regulator of this pathway (Chen et al., 2006). Furthermore, the Arabidopsis shikimate pathway genes are also induced by wounding. The compound transcriptional regulation of phenylpropanoid biosynthesis is achieved by combinatorial actions of TFs, expressed in a spatially and temporally controlled manner as exemplified in the following reports: Lepiniec et al. (2006), Ramsay and Glover (2005), and Stracke et al. (2007). Recent molecular and genetic studies in Arabidopsis have provided important insights into mechanisms underlying the transcriptional regulation of secondary cell wall biosynthesis. It has been proposed that a transcriptional network encompassing a cascade of transcription factors is involved in the coordinated regulation of secondary cell wall biosynthesis in fibers and vessels (Zhong and Ye, 2007). A group of closely related NAC domain TFs, namely SND1 (also called NST3/ANAC012), NST1, NST2, VND6, and VND7, function at the top of this network to activate the entire secondary wall biosynthetic program (Kubo et al., 2005; McCarthy et al., 2009). Several R2R3-MYB TFs, such as MYB58, MYB63, MYB46, and its redundant gene MYB83, operate as downstream components in the SND1-mediated transcriptional network. These MYBs are phylogenetically distinct from other characterized MYBs, which were shown to be associated with secondary cell wall formation or phenylpropanoid metabolism (McCarthy et al., 2009; Zhou et al., 2009). Production of anthocyanins, an important class of phenylpropanoids, is stimulated by expression of the MYB75/PAP1 TF (Borevitz et al., 2000; Tohge et al., 2005), whose expression is induced by sucrose (Teng et al., 2005). Furthermore, expression of the Arabidopsis AtPAP1 gene in petunia flowers caused a dramatic increase in both anthocyanins and volatiles derived from the phenypropanoid/benzenoid pathways (Ben Zvi et al., 2008). Another study on the regulation of fragrance production in petunia identified another novel TF (ODORANT1) regulating the production of volatile benzenoids through activating various genes including genes encoding enzymes of the shikimate pathway and AAA biosynthesis: DAHPS, EPSPS, CM, and PAL (Colquhoun et al., 2010a; Colquhoun et al., 2010b; Schuurink et al., 2006; Verdonk et al., 2005, 2003). Interestingly, overexpression of ODORANT1in petunia flowers had no effect on the production of anthocyanins, indicating that the production of anthocyanin is under a separate regulatory control (Verdonk et al., 2005). A new R2R3MYB TF, named EMISSION OF BENZENOIDS II (EOBII), has also been recently shown to regulate phenylpropanoid volatile biosynthesis, in petunia flowers. EOBII was found to be flower-specific and temporally and spatially associated with scent production/emission. Suppression of EOBII expression led to significant reduction in the levels of volatiles accumulating and emitted by flowers, such as benzaldehyde, phenylethyl alcohol, benzylbenzoate, and isoeugenol. Down-regulation of EOBII affected transcript levels of several biosynthetic floral scent-related genes encoding enzymes of the shikimate pathway and AAA biosynthesis, such as CS, CM, and additional

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FUNDING

Bartel, B., LeClere, S., Magidin, M., and Zolman, B.K. (2001). Inputs to the active indole-3-acetic acid pool: de novo synthesis, conjugate hydrolysis, and indole-3-butyric acid b-oxidation. J. Plant Growth Regul. 20, 198–216. Basset, G., et al. (2004). Folate synthesis in plants: the p-aminobenzoate branch is initiated by a bifunctional PabA–PabB protein that is targeted to plastids. Proc. Natl Acad. Sci. U S A. 101, 1496–1501. Beaudoin-Eagan, L.D., and Thorpe, T.A. (1985). Tyrosine and phenylalanine ammonia lyase activities during shoot initiation in tobacco callus cultures. Plant Physiol. 78, 438–441. Bekal, S., Niblack, T., and Lambert, K. (2003). A chorismate mutase from the soybean cyst nematode Heterodera glycines shows polymorphisms that correlate with virulence. Mol. Plant Microbe Interact. 16, 439–446. Ben Zvi, M.M., et al. (2008). Interlinking showy traits: co-engineering of scent and colour biosynthesis in flowers. Plant Biotechnol. J. 6, 403–415. Bender, J., and Fink, G.R. (1995). Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of Arabidopsis. Cell. 83, 725–734.

This Study was supported by a Magnet Program of the Israeli Ministry of Industry, Trade and Labor and the Israeli Bio-TOV Consortium including HAZERA GENETICS Ltd., Evogene Ltd., FRUTAROM Ltd., RAHAN MERISTEM (1998) Ltd. and ZERAIM GEDERA Ltd. No conflict of interest declared.

Berry, A. (1996). Improving production of aromatic compounds in Escherichia coli by metabolic engineering. Trends Biotechnol. 14, 250–256.

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