Journal of Heredity 2004:95(3):225-233
© 2004 The American Genetic Association
Salmon Silk Genes Contribute to the Elucidation of the Flavone Pathway in Maize (Zea mays L.)
From the Plant Genetics Research Unit, Agricultural Research Service, U.S. Department of Agriculture, Columbia, MO 65211 (McMullen, Houchins, and Coe); Department of Agronomy, Plant Sciences Unit, University of Missouri, Columbia, MO 65211 (McMullen, Kross, Cortés-Cruz; Musket, and Coe); and the Department of Plant Pathology, University of Georgia, Athens, GA 30601 (Snook). M. Cortés-Cruz is currently at the Waksman Institute, Rutgers University, Piscataway, NJ 08854.
Address correspondence to M. D. McMullen, 302 Curtis Hall, University of Missouri, Columbia, MO 65211, or e-mail: mcmullenm{at}missouri.edu.
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Abstract |
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We utilized maize (Zea mays L.) lines expressing the salmon silk (sm) phenotype, quantitative trait locus analysis, and analytical chemistry of flavone compounds to establish the order of undefined steps in the synthesis of the flavone maysin in maize silks. In addition to the previously described sm1 gene, we identified a second sm locus, which we designate sm2, located on the long arm of maize chromosome 2. Our data indicate that the sm1 gene encodes or controls a glucose modification enzyme and sm2 encodes or controls a rhamnosyl transferase. The order of intermediates in the late steps of maysin synthesis was established as luteolin
isoorientin rhamnosylisoorientin maysin.
In maize (Zea mays L.), "the genetics of pigment control is more fully elaborated than that of any other character" (Coe et al. 1988). However, in contrast to the extensive research that has been conducted using the anthocyanin pathway in maize, our understanding of the enzymatic steps involved in the synthesis of other classes of flavonoids, such as the flavones and the 3-deoxyanthocyanins, is still incomplete.
E. G. Anderson (1921) first described the "factor Sm" for salmon silk color in maize. Homozygous recessive sm plants displayed salmon-colored silks, while plants of the Sm/_ genotype produced green silks. Pigment accumulated throughout the shaft of the silks and was not limited to the silk hairs as is typical of anthocyanin pigmentation. Anderson (1921) showed sm to be linked to y (yellow endosperm) and pl (purple plant), genes known to reside on maize chromosome 6. He also reported that expression of the salmon silk phenotype required a functional p allele. Despite these early observations, the biochemical basis of the salmon silk phenotype has remained unresolved.
The p locus encodes a transcriptional factor that regulates the synthesis of flavonoid compounds in specific maize tissues (Grotewold et al. 1994). The p locus controls the color phenotype of the pericarp and cob by regulating the synthesis of phlobaphenes (Grotewold et al. 1994) and the browning phenotype of silks by regulating the synthesis of maysin and related flavones (Byrne et al. 1996a). Using flavone synthesis as a model quantitative trait locus (QTL) system, Byrne et al. (1996b, 1997) showed that in a population segregating for functional and nonfunctional p alleles, the p locus was the gene underlying the major QTL for maysin concentration and antibiosis to the corn earworm (Helicoverpa zea Boddie). Four phenotypic classes of p alleles direct flavone synthesis in silks: p-rrb (red pericarp, red cob, browning silks), p-wrb (colorless pericarp, red cob, browning silks), p-rwb (red pericarp, white cob, browning silks), and p-wwb (colorless pericarp, white cob, browning silks). The fifth class of allele, p-www (colorless pericarp, white cob, nonbrowning silks), is considered nonfunctional for flavone synthesis in maize silks (Byrne et al. 1996a). This complex tissue specificity is made possible because the p locus may consist of duplicate factors p1 and p2 (Zhang et al. 2000, 2003). Interest in the role of the C-glycosyl flavones, particularly maysin, in conferring natural resistance in maize silks to larvae of various lepidopteran insect pests has resulted in an experimental merger of agronomic trait analysis and classic maize genetics (McMullen et al. 1998).
Although maysin is the predominate flavone in silk tissue of most maize lines and varieties, other flavones may be present (Snook et al. 1994). Widstrom and Snook (1998) reported that the maize inbred line T218 contained high levels of the flavone isoorientin and that a single recessive gene controlled isoorientin accumulation. Upon growing T218 in the field in Columbia, Missouri, we noted that T218 plants exhibited a striking salmon silk phenotype. This observation prompted us to examine the relationship of salmon silk phenotypes with flavone synthesis.
Our objectives in this study were to use a combination of classical genetics, QTL mapping, and analytical chemistry to define the genetic and biochemical basis of the salmon silk phenotype and to define steps in the biochemical pathway for maysin synthesis.
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Materials and Methods |
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sm*-Brawn Lines: Complementation Tests
Eight sm*-Brawn stocks (containing sm alleles collected by R. I. Brawn)—sm*-Brawn168, -178, -180, -184, -188, -189, -190, and -191—were obtained from the Maize Genetics Cooperation Stock Center. Plants of these lines, along with the sm1 stock line 611A and line T218, were grown at the University of Missouri Bradford Research and Extension Center (BREC) near Columbia, Missouri, during the summer of 1998. The line 611A represents the reference sm1 allele (sm1-ref) from the Maize Genetics Cooperation Stock Center and was obtained from the collection of E. H. Coe. Silk color was recorded and silk tissue collected from plants for each line. Each sm*-Brawn line was crossed to both 611A and T218. Plants from each of the sm*-Brawn lines, the testers 611A and T218, and the F1 testcrosses were grown in the greenhouse during the winter 1998/1999. Silk color was recorded and 2-day-old silk tissue was collected from two to nine plants per genotype. Once allelic relationships were established the sm*-Brawn alleles were renamed to reflect the appropriate locus (Maize GDB, http://www.maizegdb.org/).
Silk Chemical Analysis
Freeze-dried silk samples were shipped to the Richard B. Russell Research Center, USDA-ARS, Athens, Georgia, for chemical analysis. Methanol silk extract concentrations for flavones were determined by reverse-phase high-performance liquid chromatography (HPLC) and expressed as the percent fresh silk weight, as previously described (Snook et al. 1989, 1993). The flavones maysin, isoorientin, luteolin, de-rhamnosylmaysin, and rhamnosylisoorientin (Figure 1) were identified based on ultraviolet (UV) spectral analysis, acid hydrolysis studies, 1H- and 13C- nuclear magnetic resonance, and fast-atom bombardment mass spectrophotometric methods.
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QTL Experiment 1: Mapping the Second Salmon Gene, Epistasis with P
The mapping population included 285 F2 individuals derived from the cross of the inbred lines T218 and GT119. T218 has salmon silks and is homozygous for the P-wrb allele. GT119 has green silks and produces no flavones due to its nonfunctional P-www allele (Byrne et al. 1996b). T218, GT119, F1, and F2 plants were grown at the Maize Genetics Farm near Columbia, Missouri, during the summer of 1998. Two-day-old silk masses were collected and analyzed for flavone type and concentration. Leaf tissue was collected from F2 individuals at the midwhorl stage of plant development and DNA extracted by standard procedures (Saghai-Maroof et al. 1984). Restriction fragment length polymorphism (RFLP) (Byrne et al. 1996b) and simple sequence repeat (SSR) (Sharopova et al. 2002) analyses were performed to genotype each of the F2 individuals. A linkage map consisting of 95 loci was constructed using MapMaker/Exp 3.0b (Lander et al. 1987). Composite interval mapping was performed using QTL Cartographer, version 1.16c (Basten et al. 1994; Zeng 1994). Cofactors for composite interval mapping were identified by the SRmapqtl function using forward/backward regression with P(F-in) and P(F-out) equal to.01. A series of 1000 permutations (Churchill and Doerge 1994) was used to establish an experiment-wise significance level at P =.05 of the likelihood of odds (LOD) that across traits and populations average LOD equals 3.5. Therefore this significance threshold was used for all traits and experiments.
QTL Experiment 2: Pathway Analysis
The mapping population included 256 F2 individuals derived from two self-pollinated F1 plants from the cross 611A x T218. Plants of the parents, F1, and F2 individuals were grown at the University of Missouri BREC near Columbia, Missouri, in the summer of 1999 and silks were collected and analyzed as for experiment 1. The genotypes of the F2 individuals were determined and a linkage map consisting of 91 SSR loci was constructed. QTL analysis was performed by composite interval mapping as described for experiment 1.
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Complementation Tests with sm*-Brawn Lines Establish Two sm Loci
High-performance liquid chromatographic analyses of the flavones present in silks of 611A (sm1 stock line), T218, and the sm*-Brawn lines revealed two distinct patterns of predominant flavone compounds (Table 1). The salmon silks of the sm1 stock line 611A contained rhamnosylisoorientin and maysin. In contrast, the salmon silks of T218 contained neither maysin nor rhamnosylisoorientin, but instead contained isoorientin and de-rhamnosylmaysin. Silks of the F1 progeny of 611A x T218 were green in color instead of salmon, and essentially all of the flavone was maysin. Silks of the sm*-Brawn lines 168, 178, and 184 are characteristic of the 611A type, as indicated by the presence of rhamnosylisoorientin. The sm*-Brawn lines 188, 189, 190, and 191 exhibit the second silk chemistry pattern, similar to T218, characterized by the presence of isoorientin and de-rhamnosylmaysin. These results prompted an investigation of the genetic basis of the salmon silk phenotype and the relationship of genetic loci to the flavones.
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The F1 progeny of crosses of sm*-Brawn lines 168, 178, and 184 to 611A exhibited the salmon silk phenotype and a 611A-type flavone profile. When the sm*-Brawn lines 168, 178, and 184 were crossed to T218, the F1 progeny displayed green silks and accumulated maysin, similar to the F1 cross of 611A x T218. The F1 progeny of crosses of sm*-Brawn lines 188, 189, 190, and 191 to T218 exhibited salmon silks and accumulated isoorientin and de-rhamnosylmaysin. The F1 progeny of crosses of these lines to 611A produced green silks and maysin. Based on these results, the sm*-Brawn lines 168, 178, and 184 were assigned the sm1/sm1 genotype, the same as the sm1 stock line 611A, whereas T218 and the sm*Brawn lines 188, 190, and 191 were assigned the sm2/sm2 genotype, representing a novel sm locus.
In addition to chemical compounds described above, additional novel peaks were detected by HPLC in silks with sm phenotypes. Partial characterization and structural determination using a combination of UV spectra, acid hydrolysis, thin-layer chromatography retention factor (Rf), 13C nuclear magnetic resonance, and fast-atom bombardment mass spectrophotometric analysis suggested that two of these compounds represented a diglucosylbiflavone (molecular weight = 882) and a rhamnosyldiglucosylbiflavone (molecular weight = 1028). The diglucosylbiflavone is present in sm2 lines and the rhamnosyldiglucosylbiflavone is present in sm1 lines. These compounds are previously unreported for maize. Experiments to obtain definitive proof of the structure of diglucosylbiflavone and rhamnosyldiglucosylbiflavone are in progress (Snook ME, unpublished data).
QTL Experiment 1: Mapping the Second Salmon Silk Gene and Epistasis with P
To elucidate the genetic basis of isoorientin and de-rhamnosylmaysin synthesis in T218, we conducted QTL analysis on the population (T218 x GT119)F2. The parental line T218 accumulated isoorientin and de-rhamnosylmaysin at approximately 0.2–0.3% fresh silk weight for each compound (Table 2). GT119 accumulated a barely detectable level of maysin. Silks of the F1 were green and contained maysin, indicating that although GT119 does not produce maysin due to a nonfunctional p allele, the line must contain a functional Sm2 allele to complement the sm2 allele in T218. The linkage map for the (T218 x GT119)F2 population includes 95 loci, covering a total genome length of 1505 cM, with an average interval length of 18 cM. The linkage map for this population is available on the MaizeGDB website (http://www.maizegdb.org/) under the name "T218 x GT119 F2 1997."
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For the compounds isoorientin and de-rhamnosylmaysin, we detected two QTLs (Table 3). The major one, with LOD scores greater than 27 and R2 values of more than 55%, is located on chromosome 2. Because the peak LOD maps to position 129 (centiMorgans from the top of the short arm) for both of these compounds, we assume the data reflect a single, common QTL. The genetic effect of the T218 allele is to direct an increase in both isoorientin and de-rhamnosylmaysin. The gene action is recessive for the synthesis of isoorientin and de-rhamnosylmaysin. The second QTL for isoorientin and de-rhamnosylmaysin mapped to chromosome 1; its position ranged from 64 to 66 cM for these compounds. Again, we consider this to be the same QTL for both compounds. The T218 allele increases flavone concentrations.
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We detected three QTLs for maysin. The largest one corresponds to the previously discussed QTL on chromosome 1. With a LOD score of 39.6, it accounts for 44% of the phenotypic variation and its genetic effect is an increase of 0.179% silk fresh weight maysin by the T218 allele. The second largest QTL for maysin corresponds to the QTL detected on chromosome 2. While the T218 allele at the QTL increased concentrations of isoorientin and de-rhamnosylmaysin, it has the opposite effect on maysin, decreasing the concentration by 0.093%. A third minor QTL (LOD = 4.3) mapped to chromosome 3.
The p locus, as detected by the RFLP probe p-umc185, mapped to position 64.2 on chromosome 1 in this population. Based on map position, gene action, and consistency with results from other populations (Byrne et al. 1996b; McMullen et al. 1998, 2001), we assign the gene p as the candidate gene for the QTL mapping to chromosome 1. The gene action of the QTL on chromosome 2 is consistent with this QTL being sm2, as identified in the complementation tests. Based on QTL position for isoorientin and de-rhamnosylmaysin, this QTL/gene maps to position 119–129 cM on chromosome 2, near the RFLP locus asg20. Consistent with the interaction between p and sm1, as reported by Anderson (1921), p and sm2 exhibit an epistatic interaction in the (T218 x GT119)F2 population (Figure 2). In the presence of at least one functional p allele (the p-wrb allele from T218), plants homozygous recessive for the sm2/sm2 genotype display salmon-colored silks and a flavonoid profile consisting of isoorientin and de-rhamnosylmaysin. Any combination of functional P/_ and Sm1/_ results in the synthesis of maysin with the associated green silk phenotype. In silks with the nonfunctional p/p genotype, the level of all flavone compounds is near zero. While the gene action of p is additive for any flavone class, the gene action of sm1 is dominant for maysin and recessive for isoorientin and de-rhamnosylmaysin.
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QTL Experiment 2: Defining the Pathway
To further define the relationship of sm1 and sm2 to specific flavones and to understand the order of the enzyme steps in the flavone pathway, we conducted QTL analysis on a population, (611A x T218)F2, designed to segregate at both sm1 and sm2. We constructed a linkage map of 91 SSR loci, covering a total genome length of 1508 cM, with an average interval length of 18 cM (Figure 3). This map is available on the MaizeGDB website under the name "611A x T218 F2 1998."
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We conducted QTL analysis for four compounds (Table 3). For isoorientin and de-rhamnosylmaysin, the QTL on chromosome 2 was the major QTL detected. For rhamnosylisoorientin, the major QTL detected was located on chromosome 6. For maysin, two major QTLs, consistent with the positions of the QTLs for isoorientin, de-rhamnosylmaysin, and rhamnosylisoorientin, were detected on chromosomes 2 and 6.
Based on mapping information, gene action, and context, we are confident that the QTL on chromosome 2 was the same as sm2 in QTL experiment 1. The T218 allele (recessive sm2) increased concentrations of isoorientin and de-rhamnosylmaysin and decreased maysin. For rhamnosylisoorientin, the major QTL, with an R2 value of 75%, was located on chromosome 6. The map position and gene action of this QTL was consistent with sm1 being the candidate gene for this QTL. The p locus was not detected as a QTL in this population because both parents contributed p alleles that were functional for silk flavone synthesis; 611A a P-rrb allele and T218 a P-wrb allele.
The salmon silk phenotype was seen when either sm1 was homozygous for the 611A allele or sm2 was homozygous for the T218 allele (Table 4). Isoorientin and de-rhamnosylmaysin were only produced in plants homozygous for the sm2 allele from T218 and rhamnosylisoorientin only accumulated to high levels in plants homozygous for the sm1 allele from 611A. None of these three compounds accumulated to very high levels in any genotypes that yielded green silks. In plants homozygous recessive for both sm1 from 611A and sm2 from T218, isoorientin was the only compound that accumulated to high concentrations (Table 4).
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Discussion |
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The dramatic effect of the sm1 and sm2 loci on the flavones present in maize silks suggests that these loci encode or strictly control the expression of enzymes in the pathway from flavanone to maysin. The specific flavones present in homozygous sm1, sm2 and double-mutant plants (Tables 1 and 4) allow us to define and order many of the steps in maysin synthesis (Figure 1). Because isoorientin is the only flavone that accumulates to high levels in plants homozygous recessive at both sm1 and sm2, we conclude this compound is present in the pathway immediately preceding the earliest point of action in the pathway of these loci. That isoorientin also accumulates to high levels in sm2 but is lacking in sm1 plants indicates that isoorientin is the substrate for the protein encoded (or controlled) by sm2. Because rhamnosylisoorientin is the main flavone that accumulates in silks of sm1 plants, we place this compound in the pathway immediately above the point of action of the protein encoded by sm1. These results indicate the order of the late steps in maysin synthesis are isoorientin
rhamnosylisoorientin maysin. Comparison of the flavone structures allows us to define the enzyme functions blocked in sm1 and sm2 plants. The enzyme function lacking in sm2 plants is that of a rhamnosyl transferase. Determining the enzyme function(s) lacking in sm1 plants is more complicated. Modifications are required at both the 4- and 6- carbon positions of the glucose. The 4- carbon position undergoes an oxidation reaction to form a ketone, while the 6- carbon position requires a reduction to the methyl group. Ellinger et al. (1980) has previously proposed independent steps for the 4- and 6- carbon modifications. Intermediate compounds with modification at only one of the positions were not seen in any of the sm1 lines. In the 611A line containing the sm1-ref allele, there are almost equal amounts of maysin and rhamnosylisoorientin (Tables 1 and 2). The presence of maysin could be explained either by a second, duplicate locus partially compensating sm1, or the sm1-ref allele represents only a partial loss of function. Two lines of evidence point to sm1-ref as a partial loss of function. First, the three other independent alleles of sm1, sm1-Brawn168, sm1-Brawn178, and sm1-Brawn184 only accumulate rhamnosylisoorientin and no maysin (Table 1). The second line of evidence comes from analysis of an (sm1-Brawn178 x 611A)F2 population (Ellberg S and McMullen MD, unpublished data). This population segregates for plants that accumulate only rhamnosylisoorientin and plants that accumulate both maysin and rhamnosylisoorientin. This difference maps to the sm1 locus on chromosome 6, with maysin produced only in plants with the 611A allele. That the sm1-ref allele represents only a partial loss of function also helps explain the ambiguities often encountered in classifying sm1 phenotypes in populations segregating for the sm1-ref allele (Coe EH and McMullen MD, personal observations).
The presence of de-rhamnosylmaysin along with isoorientin in sm2 plants indicates that the enzyme encoded by sm1 can also act on isoorientin, but because de-rhamnosylmaysin is never the only flavone, its activity must be less efficient on isoorientin than it is on rhamnosylisoorientin. That the activity converting isoorientin to de-rhamnosylmaysin is encoded by sm1 is evident in the lack of de-rhamnosylmaysin in double-mutant plants (Table 4).
Our results also provide clues to earlier steps in flavone synthesis. Luteolin (the aglycone flavone) is present in trace amounts specifically in sm2 plants (Snook ME, unpublished data), suggesting it is the substrate for the C-glucosyltransferase to synthesize isoorientin. These results indicate that flavone synthase acts on the aglycone and that all the sugar additions and modifications are made on flavone compounds. All the flavone compounds from isoorientin through maysin are predominately dihydroxylated on the B-ring, indicating that F3'H can function efficiently early in the pathway and not as a final step in converting apimaysin (the monohydroxylated form of maysin) to maysin [see Cortés-Cruz et al. (2003) for discussion of possible alternative locations in the pathway for 3' hydroxylation].
Our use of the combination of classical and quantitative genetics, along with analytical chemistry, has enabled us to identify the enzymatic activities that underlie the sm phenotype. However, the vexing question remains as to the identity of the compounds responsible for the pink-orange color of sm silks. Like maysin, purified isoorientin, rhamnosylisoorientin, and de-rhamnosylmaysin are pale white to yellow and cannot be responsible for the sm phenotype. In the results section we mentioned the presence of additional flavone derivatives, including two compounds tentatively identified as diglucosylbiflavone and rhamnosyldiglucosylbiflavone. Again, these compounds are themselves not pink, but a reddish hue to the solution is often detected during their purification/concentration (Snook M, personal observations). Consistent with studies in many plants (Frangne et al. 2002), transformation studies in maize tissue culture cells indicate that the C-glycosyl flavones are normally sequestered into the vacuole (Grotewold et al. 1998). Alterations in the sugar moieties may disrupt the transport mechanisms required for this compartmentalization. The production of the biflavones and whatever compounds are responsible for the color may occur in response to the inability of the cell to properly remove the flavones from the cytoplasmic space to the vacuole.
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Acknowledgments |
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This research was supported by USDA NRI-CGP Plant Genome grants 97-35300-4391 and 2001-35301-10581, and funds provided to U.S. Department of Agriculture-Agricultural Research Service (to M.D.M.). The authors thank Chris Browne for technical assistance. Names of products are necessary to report factually on available data; however, neither the USDA nor the University of Georgia guarantees or warrants the standard of the product, and the use of the name does not imply approval of the product to the exclusion of others that may also be suitable.
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Footnotes |
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Corresponding Editor: William Tracy
Received January 15, 2004
Accepted March 11, 2004
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References |
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