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CROP BREEDING, GENETICS & CYTOLOGY

The Role of Pericarp Cell Wall Components in Maize Weevil Resistance

^a CIMMYT, Apdo Postal 6-641, 06600 Mexico D.F., Mexico
^b Dep. of Biology, Univ. of Ottawa, Ontario, Canada, K1N 6N5
^c Dep. Ciencias de la Salud, Univ. Autonoma Metropolitana, Apdo Postal 55-5350, 09340 Mexico, D.F., Mexico

^* Corresponding author (d.bergvinson{at}cgiar.org).

	ABSTRACT

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The maize weevil (MW), Sitophilus zeamais (Motsch.), is a storage pest that causes serious losses in maize (Zea mays L.) in developing countries. This study was conducted to investigate the role of pericarp cell wall components as factors that contribute to MW resistance in nine genotypes of tropical maize. Six susceptibility parameters to MW were measured and related to cell wall components such as simple phenolic acids, diferulic acids (DiFAs), hydroxyproline-rich glycoproteins (HRGPs), and nutritional and physical traits. Weevil susceptibility was negatively correlated (P < 0.001) with total DiFAs (r = –0.77), HRGPs (r = –0.82), grain hardness (r = –0.87), pericarp/whole kernel (P/K) ratio (r = –0.68), and pericarp thickness (r = –0.86). A detailed analysis of phenolics indicated the presence of trans-ferulic acid (FA), p-coumaric acid (CA), and four isomers of DiFA. The most prominent were 5,5'-DiFA, 8-O-4-DiFA, and 8,5'-DiFA benzofuran form (DiFAb). On the basis of regression models, 5,5'-DiFA, 8-O-4-DiFA, trans-FA, and p-CA were the most important phenolic components of resistance. Grain hardness was correlated (P < 0.001) with cell wall bound HRGPs (r = 0.61) and DiFAs (r = 0.75). Cell wall cross-linking components could contribute to MW resistance by fortification of the pericarp cell wall as well as increase grain hardness. This structurally based mechanism should be considered in the development of hybrids and varieties where storage pests are prevalent.

Abbreviations: CA, coumaric acid • CIMMYT, International Maize and Wheat Improvement Center • DiFA, diferulic acid • FA, ferulic acid • HRGP, hydroxyproline-rich glycoprotein • MDT, median development time • MW, maize weevil • P, population

	INTRODUCTION

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THE MAIZE WEEVIL is a destructive insect feeding on stored maize throughout the world. Subsistence farmers in tropical and subtropical agroecosystems often experience grain damage exceeding 30% during on-farm storage (Tigar et al., 1994). The use of insect resistant varieties of grain has been proposed in the past (Dobie, 1977) as part of an integrated pest management strategy to reduce losses and maintain grain quality.

Several maize varieties, including local landraces, have been characterized as sources of resistance to MW (Dobie, 1977; Widstrom et al., 1983; Giga and Mazarura, 1991; Arnason et al., 1994) and some sources of resistance have been incorporated into elite maize lines (Bergvinson, 2001). In maize, various biochemical and physical characteristics have been identified as mechanisms of kernel resistance to MW (Dobie, 1977, Serratos et al., 1987; Tipping et al., 1988; Arnason et al., 1994, 1997).

Phenolic acids have been studied extensively as biochemical components correlated with resistance and found to act in two ways: through mechanical resistance (cell wall bound hydroxycinnamic acids) and antibiosis (phenolic acid amides) in the pericarp and aleurone layer, respectively (Arnason et al., 1997). The pericarp of MW resistant maize has a higher concentration of hydroxycinnamic acids (Serratos et al., 1987). The major components are trans-FA (the most abundant) and p-CA (Classen et al., 1990), which are not found as free acids. In the maize cell wall, these phenolic acids are ester-linked to cell wall polysaccharides, as well as phenolic dimers, such as DiFA (Fry, 1986; Ishii, 1997). Arnason et al. (1994) has demonstrated that MW resistant genotypes have higher concentrations of total DiFAs. Cross-linking of polysaccharides by DiFAs is considered particularly important in fortification of the pericarp cell wall, and these dimers probably contribute to the observed correlations between phenolic acid content and grain hardness (Classen et al., 1990; Arnason et al., 1997). Recently, several isomers of DiFAs have been identified and characterized within the maize pericarp and aleurone and proposed as a structural component of the cell wall (Saulnier and Thibault, 1999) and resistance factors to Fusarium ear rot, caused by Fusarium graminearum (Schwabe) (Bily et al., 2003).

Structural proteins, such as HRGPs or extensin, are another important component of the maize pericarp (Hood et al., 1991; Fritz et al., 1991). Extensins are involved in cell wall organization, development, wound healing, and plant defense mechanisms. Extensins can be cross-linked within the cell wall and their presence has been associated with the tensile strength of the cell wall (Cassab, 1998). However, there is no report of pericarp cell wall extensins having a function in MW resistance.

Susceptibility to MW has also been related to nutritional quality traits such as sugar, protein, fat, and amino acids (Dobie, 1977; Classen et al., 1990). Protein content is negatively correlated with susceptibility to MW (Arnason et al., 1994, 1997). Studies on quality protein maize, which has twice the tryptophan and lysine content, have found no indication that these genotypes are more susceptible to MW than normal maize (Arnason et al., 1993), but it is still unknown if grain quality could be affected in the process of developing MW resistant varieties.

The purpose of the present study was to investigate the role of the pericarp cell wall components in maize within the context of biochemical and physical factors that affect MW resistance. Our objectives were (i) to determine the content of simple phenolic acids, diferulic acids and HRGPs in the pericarp and sugars, nitrogen, and essential amino acids in whole grain of nine tropical maize genotypes and (ii) to correlate putative resistance factors in the pericarp to MW resistance and grain hardness.

	MATERIALS AND METHODS

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Maize Genotypes
Nine maize genotypes available at the International Maize and Wheat Improvement Center (CIMMYT) were used in the current study (Table 1). The seed was increased for evaluation during 1999 and 2000 at CIMMYT's experimental station at Tlaltizapan, Morelos Mexico (18°41'N lat., 940 m above sea level). Seed production during both seasons was achieved by bulk sibbing by collecting pollen from up to 20 plants to pollinate 20 plants in the neighboring row and vice-versa. Seed was then bulked within plots for each genotype. Two lowland tropical landraces, Sinaloa 35 and Yucatan 7, were used as resistant checks based on previous reports (Arnason et al., 1994). Two open-pollinated populations (P) developed at CIMMYT by S₃ intrapopulation improvement under artificial infestation included (i) P80 developed for MW resistance by crossing a quality protein maize variety from Ghana, ‘Ejura’ with Sinaloa 35 and (ii) P84 derived from 20 Caribbean accessions with moderate resistance to the larger grain borer [Prostephanus truncatus ( Horn)]. A third subtropical population, P47, was used in reciprocal crosses with P84, as it is moderately susceptible to MW. All populations had been previously bulk increased with 300 plants used to regenerate seed for the current study. Two tropical maize lines and one highland hybrid were included in this study: Muneng-8128 C0 HC1-18-2-1-1, CML290 [(Pob28xTSR)-33-3-7-3-1-BB] and CML244 x CML349. The last two genotypes were considered as susceptible genotypes on the basis of previous evaluations.

Analysis of Phenolic Compounds by HPLC
During the 1999 season, samples from each genotype were prepared in bulk and in 2000 a sample was prepared from each replicate. Biochemical analysis was performed on pericarp tissue removed from kernels by a pearl mill (Sen et al., 1994). The sample was subjected to alkaline hydrolysis for 4 h (Classen et al., 1990). Phenolic acids were determined by HPLC as described in Arnason et al. (1994) for one replicate. An additional two replicates were quantified by an improved HPLC method and the peak identification was determined by comparison of t_R and spectra with purified compounds (Bily et al., 2003).

Determination of Cell Wall HRGPs and Biochemical Parameters
For both seasons, pericarp samples were prepared from two separate replicates for each genotype consisting of 20 kernels each. Pericarp tissue was removed by hand after imbibing kernels in distilled water for 30 min at 4°C. The samples were dried and ground to a fine powder using a cyclone mill fitted with a 1-mm screen. The cell walls HRGPs were extracted according to the method of Hood et al. (1991). Briefly, pericarp tissue was homogenized in 0.1% (w/v) K-acetate (pH 5.0) and 4 mM Na₂S₂O₅. The pellets were resuspended with 0.5% Nonidet P-40 (Fluka) and 2 mM Na₂S₂O₅ and washed four times in 2 mM Na₂S₂O₅. Proteins were extracted with 0.2 M CaCl₂ to obtain soluble HRGPs, while the remaining cell wall pellet was considered the insoluble HRGP fraction. The extracts and the pellets were hydrolyzed in 6 M HCl for 24 h at 110°C. Hydroxyproline content was determined according to the method of Woessner (1961). Grain produced in the 2000 season was used for quantification of nitrogen, tryptophan, lysine, quality index, and total sugars were performed at CIMMYT's protein quality laboratory on whole grain samples according to methods described by Villegas et al. (1984).

Determination of Grain Hardness and Physical Parameters
Mechanical hardness of the grain was determined in both seasons with a force displacement meter model 921A (Tricor Systems Inc, Elgin, IL) equipped with an electronic force transducer of 20 kg and a 0.8-mm probe. The operation of the force meter was controlled with DFR software (DFR Operation for Windows, version 4.25, Tricor Systems Inc., Elgin, IL). Kernels were equilibrated for 4 wk at 27 ± 1°C and 70 ± 5% RH before hardness measurement. Sixty kernels were tested for peak force (in Newtons, N) for each genotype. The kernel was placed on a metal plate with the embryo facing down. The probe traveled at a rate of 1 cm min^–1 until the kernel cracked and the maximum force applied was recorded (Bergvinson, unpublished data, 2003).

Kernel density was determined according to the method of Korunic et al. (1998). Kernel weight was obtained with a 30-g sample and dividing the weight by the number of kernels. Pericarp/kernel (P/K) ratio was determined by peeling the pericarp from 20 kernels and drying at 25°C, 45% RH for 24 h. This ratio was determined by dividing the weight of pericarp by the whole kernel weight (Hood et al., 1991). Pericarp thickness was measured from pericarp covering the embryo and the site opposite the embryo with a Spin micrometer (Model 10-891-0, Mitutoyo, Japan).

Statistical Analysis
Since genotypes were selected on the basis of previous screening results to obtain a wide range in MW susceptibility, a fixed ANOVA model was used. Susceptibility, biochemical, and physical data were subjected to analysis of variance with the statistical software Statistix v.7 (Analytical Software, Tallahassee, FL) and differences among means were compared by Tukey test at P < 0.05. Orthogonal comparison of means were analyzed from two contrast groups: resistance vs. susceptible (Sokal and Rohlf, 1981, p. 232–242). Differences between the cross P84 x P47 and its reciprocal cross were analyzed by paired t test. Statistix also calculated Pearson correlations and multiple regressions. Multiple regressions were calculated by stepwise regressions for linear models. Only parameters with P < 0.1 were considered in the model. Traits that maximized the r² value were selected on the basis of step-wise regressions for each susceptibility parameters. A fixed model was generated on the basis of the major biochemical and biophysical parameters correlated with susceptibility.

	RESULTS

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Susceptibility Data
Considerable variation in susceptibility parameters was observed among the nine maize genotypes (Table 1). Although genotype x environment interactions were observed for damage, progeny, and Dobie index, estimates of variance components showed that environment contributed less than 10% of the phenotypic variation (data not shown). Analysis of variance indicated that damage, grain weight loss, flour production, progeny, Dobie Index, and MDT showed variation (P < 0.001) among genotypes. All susceptibility parameters were highly correlated (r > 0.9, P < 0.001) to each other. P84 and Sinaloa 35 were the most resistant genotypes, while CML290 and CML244 x CML349 were the most susceptible. On the basis of Dobie Index, three major groups were determined: (i) resistant (P84, P84 x P47, Sinaloa 35, Yucatan 7, P47 x P84), (ii) moderately resistant (P80 and Muneng-8128 C0 HC1-18-2-1-1), and (iii) highly susceptible (CML290 and CML244 x CML349). Orthogonal comparisons of susceptibility parameters show a significant difference between resistance and susceptible groups (P < 0.001).

Cell Wall Phenolic Acids, Biochemical, and Biophysical Parameters
Three major simple phenolic acids (p-CA, cis-FA and trans-FA) and four isomers of DiFA (5,5'-DiFA, 8,5'-DiFA, 8-O-4'-DiFA, 8,5'-DiFAb) were quantified by HPLC. Except for cis-FA, which was produced by photoisomerization of trans-FA, all phenolics showed significant variation among genotypes (P < 0.01, Table 2). trans-Feluric acid represented more than 70% of total phenolic acids, while p-CA and total DiFA represented 16 and 8%, respectively. The most abundant phenolic dimers were 5,5' and 8-O-4'. There was a significant difference between susceptible and resistant genotypes on the basis of orthogonal comparisons in the levels of p-CA, trans-FA, 5,5'-DiFA, 8-O-4'-DiFA, 8,5'-DiFAb, and total DiFAs (Table 2). In all cases, resistant genotypes had a higher phenolic acid content.

Relationship between Susceptibility and Resistance Factors
Table 5 shows the correlations between susceptibility, and biochemical, and biophysical parameters. Pericarp cell wall phenolic acids were negatively correlated with susceptibility parameters. The phenolic dimers, total phenolic acid, and insoluble HRGPs were inversely correlated with damage, flour production, progeny, and the Dobie Index. The soluble fraction of HRGPs did not relate to susceptibility. Whole kernel nitrogen was negatively correlated with susceptibility parameters while sugar content only showed a low positive correlation with Dobie index.

No significant correlation was observed among susceptibility parameters and tryptophan, lysine, index of quality, and grain weight. Index quality was correlated with p-CA (r = –0.56, P < 0.01), HRGPs (r = –0.61, P < 0.01), pericarp/whole kernel ratio (r = –0.44, P < 0.05), and total phenolics (r = –0.44, P < 0.05).

Step-wise multiple regressions to predict susceptibility parameters are reported in Table 6. On the basis of step-wise regression, the susceptibility parameters were best predicted by HRGPs, grain hardness, 5,5'-DiFA, and p-CA (r² = 0.80 to 0.92). On the basis of the major biochemical components in a fixed regression model, variability in susceptibility parameters was also explained by HRGPs, grain hardness, pericarp fiber, 8-O-4'-DiFA, and trans-FA (r² = 0.77–0.91).

	DISCUSSION

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To understand the importance of diferulates, a detailed analysis of DiFAs was conducted. The analysis revealed the presence of four isomers, which were recently reported in maize grain pericarp (Bily et al., 2003). The most prominent were 5,5'DiFA and 8-O-4'-DiFA follow by 8,5'-DiFAb. On the basis of step-wise regression models, 5,5'-DiFA, 8-O-4'-DiFA, p-CA, and trans-FA were the most important phenolic acids in explaining phenotypic variance in MW resistance. These results are consistent with previous reports on the role of diferulates as important maize resistance factors to corn borers (Bergvinson et al., 1997) and ear rot (Bily et al., 2003).

Insoluble HRGPs were identified as a new MW resistance factor. This fraction of HRGPs has been previously reported in cell walls of maize pericarp and has been related to pericarp thickness and toughness (Hood et al., 1991; Fritz et al., 1991) but not with insect resistance. Extensins have been shown to accumulate in the pericarp during kernel development (Fritz et al., 1991), and according to some reports may act as a physical barrier to biotic stresses (Mazau et al., 1987). Our research provides the first evidence that cell wall bound HRGPs in the pericarp are correlated with MW resistance in maize.

The simple phenolic acids, diferulic acids, and HRGPs were correlated with increased mechanical strength of the kernel and resistance to MW. trans-Feluric acid ester-linked to heteroxylans in the cell wall can be cross-linked by the action of cell wall peroxidases in the presence of hydrogen peroxide to form diferulates (Fry et al., 2000). In this study, DiFA dimers accounted for 8% of the total phenolic acid content, with resistant genotypes having a three-fold higher level than susceptible genotypes. Extensins are linked together by isodityrosine bridges (Fry, 1986) that in turn are linked with feruloylated heteroxylans, thus forming an insoluble network within the cell wall (Saulnier and Thibault, 1999). This cross-linking process of DiFA and extensin has been established as a normal function to afford protection in mature cells (Fritz et al., 1991; Cassab, 1998; Fry et al., 2000).

In this study we define the relationship between kernel hardness and MW resistance, both of which are highly correlated with extensin and DiFA linkages within the pericarp cell wall of maize. Such cross-linkages provide a biochemical mechanism for controlling the mechanical properties of the cell wall (Waldron et al., 1996) and they limit the biodegradation of cell wall polysaccharides (Ishii, 1997). This complex likely contributes to insect resistance by fortifying the pericarp cell wall, thereby increasing the physical strength of this structure as well as overall kernel hardness. Other cell wall factors could be contributing to resistance such as cellulose and xylan content; however, fiber, as an indirect measure of these components, was negatively correlated with susceptibility parameters (Table 5). The current findings confirm the importance of the pericarp in MW resistance, its maternal effects (Tipping et al., 1988; Serratos et al., 1993; Derera et al., 2001; Dhliwayo and Pixley, 2003) and further our understanding of the underlying biochemical and biophysical factors involved in MW resistance.

Lack of correlation among insect performance and grain quality and lysine and tryptophan content is similar to that observed for quality protein maize (Arnason et al., 1993). It is not clear whether grain quality could be adversely affected by extensive cell wall cross-linking; however, other studies have established the health benefits of hydroxycinnamates in maize bran (Kroon and Williamson, 1999).

In summary, cell wall components in the maize pericarp play a significant role in weevil resistance. Structural resistance mechanisms against storage pests should be as an important trait in maize improvement programs for regions where storage pests are a threat to food security.

	ACKNOWLEDGMENTS

 
We gratefully acknowledge the support of the Canadian International Development Agency (CIDA) for the project titled "Reducing Postharvest Losses in Maize" and a Ph.D. scholarship to S. García-Lara by CONACyT, Mexico (95352). Editorial and technical reviews of the manuscript by K. Pixley, D. Beck, S. Pandey, and D.W. Krogmann are gratefully acknowledged.

Received for publication October 24, 2003.

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