Wheat streak mosaic virus

RESEARCH

Wheat–Thinopyrum Intermedium Recombinants Resistant to Wheat Streak Mosaic Virus and Triticum Mosaic Virus B. Friebe,* L. L. Qi, D. L. Wilson, Z. J. Chang, D. L. Seifers, T. J. Martin, A. K. Fritz, and B. S. Gill

ABSTRACT To date, only one gene conferring resistance to Wheat streak mosaic virus (WSMV) designated as Wsm1 was transferred from Thinopyrum intermedium (Host) Barkworth and Dewey to wheat (Triticum aestivum L.) in the form of a compensating Robertsonian translocation T4DL·4JsS. Wsm1 confers high levels of resistance to WSMV under field conditions; however, in certain genetic backgrounds and environments, the presence of the T4DL·4JsS translocation reduces agronomic performance. The objective of this study was to shorten the Th. intermedium segment in the T4DL·4JsS translocation. We recovered one proximal (rec36) and four distal (rec45, rec64, rec87, rec213) primary recombinants. Genomic in situ hybridization and molecular marker analyses determined the size of the Th. intermedium segments in the distal recombinants to be about 20% of the 4DS-4JsS arm. All primary recombinant stocks, together with appropriate controls, were evaluated for their resistance to WSMV and Triticum mosaic virus (TriMV) in greenhouse tests. Whereas the distal recombinants rec45, rec64, rec87, and rec213 were resistant to both WSMV and TriMV at low temperatures of 18°C, the proximal recombinant rec36 reacted susceptible, which mapped the Wsm1 gene to the distal 20% of the 4DS-4JsS arm. We successfully shortened the Th. intermedium segment while still retaining the Wsm1 gene. The T4DL·4DS4JsS recombinant chromosome of the rec213 stock was transferred to adapted Kansas hard red winter wheat cultivars.

B. Friebe, L.L. Qi, D.L. Wilson, and B.S. Gill, Wheat Genetic and Genomic Resources Center and Dep. of Plant Pathology, Throckmorton Plant Sciences Center, Kansas State Univ., Manhattan, KS, 66506-5502; Z.J. Chang, Institute of Crop Genetics, Shanxi Academy of Agricultural Sciences, Taiyuan 030031, Shanxi, P.R. China; D.L. Seifers and T.J. Martin, Kansas State Univ., Agricultural Research Center–Hays, 1232 240th Ave., Hays, KS 67601-9228; A.K. Fritz, Dep. of Agronomy, Throckmorton Plant Sciences Center, Kansas State Univ., Manhattan, KS, 66506-5502. Received 1 Sept. 2008. *Corresponding author ([email protected]). Abbreviations: DPI, days post-inoculation; ELISA, enzyme-linked immunosorbent assay; GISH, genomic in situ hybridization; PBS, phosphate buffered saline; SSC, saline sodium citrate; TriMV, Triticum mosaic virus; WSMV, Wheat streak mosaic virus.

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heat streak mosaic caused by Wheat streak mosaic virus (WSMV) and transmitted by the wheat curl mite (Aceria tosichella Kiefer), is a devastating virus disease of common wheat (Triticum aestivum L., 2n = 6x = 42, ABD) in the Great Plains of the United States and Canada and in most spring and winter wheat-producing areas worldwide. Yield losses of wheat infected with WSMV averaged 2.5% (Sim et al., 1988; Christian and Willis, 1993; Bockus et al., 2001), but severe infection can result in complete crop loss (McNeil et al., 1996). High levels of resistance to WSMV are not present in closely related species belonging to the primary and secondary gene pool of wheat. Only some perennial species, including Thinopyrum intermedium (Host) Barkworth and Dewey (2n = 6x = 42, JJsS) and Th. ponticum (Podp.) Barkworth and Dewey (2n = 10x = 70, JJJJsJs), have been reported to have resistance to either WSMV or its vector (McKinney and Sando, 1951; Martin et al., 1976; Stoddard et al., 1987a,b; Friebe et Published in Crop Sci. 49:1221–1226 (2009). doi: 10.2135/cropsci2008.09.0513 © Crop Science Society of America 677 S. Segoe Rd., Madison, WI 53711 USA All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Permission for printing and for reprinting the material contained herein has been obtained by the publisher.

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al., 1991, 1996a,b; Jiang et al., 1993; Chen et al., 1998a,b, 1999, 2003; Li et al., 2004). To date, Wsm1 is the only named gene conferring resistance to WSMV (Friebe et al., 1991) and being used in cultivar improvement (Baley et al., 2001; Sharp et al., 2002; Divis et al., 2006). Wsm1 was transferred from Th. intermedium to wheat by Wells and coworkers, who released several WSMV-resistant, wheat–Th. intermedium chromosome addition, substitution, and putative translocation lines (Lay et al., 1971; Wells et al., 1973, 1982). C-banding and genomic in situ hybridization (GISH) analyses showed that Wsm1 is located on the short arm of a group-4 Th. intermedium chromosome (designated as 4Ai#2) and further identified one compensating Robertsonian translocation where the short arm of 4D of wheat was replaced by the short arm of the Th. intermedium chromosome 4Ai#2, resulting in the translocation chromosome T4DL·4Ai#2S. Wsm1 was shown to belong to the Js genome of Th. intermedium (Chen et al., 1998b) and was transferred to the Kansas winter wheat cultivar Karl, and a germplasm was released as KS93WGRC27 (Gill et al., 1995). Wsm1 is temperature sensitive and confers immunity to WSMV at low temperatures around 18°C, whereas at higher temperatures around 24°C, the resistance is ineffective (Seifers et al., 1995). Two more Th. intermedium–derived sources of WSMV resistance have been reported; the first was mapped on a Th. intermedium telosome initially believed to belong to group-4 long arms but later shown to be homeologous to group-7 long arms (Friebe et al., 1996a; Qi et al., unpublished), and the second mapped to a Js–genome chromosome present in the Zhong series of wheat–Th. intermedium amphiploids and designated as Js2 (Chen et al., 1999, 2003). None of these sources are being used presently in wheat improvement because of lack of compensating translocations. In addition to Th. intermedium–derived sources for resistance, the germplasm CO960293-2 (Haley et al., 2002; Seifers et al., 2006) and the derived winter wheat cultivar RonL (Martin et al., 2007) as well as the wheat line KS03HW12 (Seifers et al., 2007) were shown to have temperature-sensitive resistance to WSMV. However, the source of these resistances and their chromosomal location is presently unknown. Although Wsm1 confers a high level of resistance to WSMV under field conditions, the presence of the T4DL·4Ai#2S translocation had detrimental effects on bread-making quality and other agronomic parameters (Seifers et al., 1995). Baley et al. (2001) and Sharp et al. (2002) analyzed the effect of the T4DL·4Ai#2S translocation under inoculated and noninoculated conditions in Montana spring wheats. Wsm1 provided a high level of resistance in the presence of the virus but, under noninoculated conditions, the presence of the T4DL·4Ai#2S translocation caused an 11 to 28% decrease in grain yield. However, no detrimental effect of T4DL·4Ai#2S was observed on quality parameters. In a recent study, Divis et 1222

al. (2006) studied the effect of the T4DL·4Ai#2S translocation on grain yield and quality parameters under natural field infection and in the absence of the virus in Nebraskaadapted winter wheat. Their data showed that Wsm1 provided a good protection against WSMV and had no detrimental effect on grain yield and quality parameters. Although Wsm1 in certain genetic backgrounds and environments may not have detrimental effects on grain yield and quality, we initiated further directed chromosome engineering to shorten the Th. intermedium segment in T4DL·4Ai#2S, which will broaden its use in wheat improvement. Recently, we reported an efficient and integrated strategy for producing wheat-alien recombinants using induced homeologous recombination, molecular resources, and cytology involving the Th. intermedium chromosome arm 4Ai#2S and wheat chromosome arm 4DS (Qi et al., 2007). Five primary recombinants were obtained, and in the present study, these were characterized for their resistance to WSMV and Triticum mosaic virus (TriMV), a new virus isolated from wheat in Kansas (Seifers et al., 2008).

MATERIALS AND METHODS Plant Material The material analyzed consisted of wheat cultivars Karl 92 (PI 564254, TA2923), Overley (PVP200400205, TA9107), Triumph 64 (TA2921, CItr13679), RonL (KS03HW158), the disomic wheat–Th. intermedium chromosome addition line (TA3513), the wheat–Th. intermedium T4DL·4Ai#2S Robertsonian translocation line (TA5040 and KS96HW10-3), and five derived wheat– Th. intermedium primary recombinants designated as rec36, rec45, rec64, rec87, and rec213 produced previously (Qi et al., 2007). All stocks are maintained at the Wheat Genetic and Genomic Resources Center at Kansas State University.

Cytological Procedures Root tips were pretreated with ice water for 24 h and fixed in ethanol (100%)–glacial acetic acid (3:1). Squash preparations were made in 45% acetic acid, cover slips were removed after freezing on dry ice, and the preparations were then dehydrated in ethanol for 5 min. C-banding and chromosome identification was according to Gill et al. (1991). Genomic in situ hybridization was according to Zhang et al. (2001) with the following modifications. Thinopyrum intermedium and Pseudoroegneria spicata (Pursh) Löve (2n = 2x = 14, J) genomic DNA was isolated using DNeasy Plant Mini Kit following the manufacturer’s instructions (Qiagen Inc., Valencia, CA). One microgram of genomic DNA was labeled with fluorescein-12-dUTP (FITC detected by yellow-green fluorescence) (Enzo, Life Sciences, New York, NY) using nick translation. The hybridization mixture contained 50% deionized formamide, 2X saline sodium citrate (SSC), 10% dextran sulfate, 0.3 mg mL–1 of sheared salmon testes DNA, and about 1 μg mL–1 of labeled genomic DNA plus a 1:100 to 1:120 excess amount of unlabeled genomic wheat DNA and was denatured by boiling for 7 min. The probe-to-blocker ratio was between 1:100 and 1:120. Thirty microliters of denatured hybridization mixture was applied to each slide and allowed to hybridize overnight in a humid chamber

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at 37°C. Posthybridization washes were in 2X SSC at 42°C for 10 min, 50% formamide in 2X SSC at 42°C for 10 min (which is equivalent to 82% stringency), 2X SSC at 42°C for 10 min, and 1X phosphate buffered saline (PBS) at room temperature. Chromosomes were counterstained with propidium iodide and fluoresce red. Slides were analyzed with an epifluorescence Zeiss Axioplan 2 microscope and images were captured with a Spot CCD (chargecoupled device) camera operated with Spot 2 software (Diagnostic Instruments, Inc., Sterling Heights, MI) and processed with Photoshop v5.5 (Adobe Systems, San Jose, CA) software.

Antiserum Sources and Indirect Enzyme-Linked Immunosorbent Assay The TriMV and WSMV antisera were prepared as described previously (Seifers, 1992; Seifers et al., 2008). Working dilutions were made from stocks adjusted to 1 mg protein mL–1: TriMV (1:4000 vol:vol) and WSMV (1:1000 vol:vol). Leaf tissue analyzed by enzyme-linked immunosorbent assay (ELISA) was ground in a 1.5 mL microcentrifuge tube using a wooden applicator stick (Fisher Scientific, Cat. # 19-086333, Denver, CO) at a 1:30 (wt:vol) ratio in 0.05 M carbonate buffer, pH 9.6 (Clark and Adams, 1977). The 200 μL extracts were placed in wells of ELISA plates (Immulon 1, Fisher Scientific, Cat. # 1424578) for 1 h at 37°C. Following rinsing, the wells were incubated for 1 h at 37°C with the appropriate antivirus antibody in a blocking buffer (5% nonfat dry milk, 0.01% antifoam A, 0.02% sodium azide, in PBS, pH 7.4). The plates were rinsed and incubated for 1 h at 37°C followed by the addition to each well of 200 μL of anti-rabbit antibody–alkaline phosphatase conjugate (Southern Biotechnology Associates, Birmingham, AL) in blocking buffer (1:3000 vol:vol). The plates were held at 37°C for 1 h, rinsed, and 200 μL of 0.714 mg mL–1 p-nitrophenyl phosphate substrate in substrate buffer (Clark and Adams, 1977) was added to each well. The plates were then held on a lab bench at 20 to 22°C for 30 min. Absorbance was measured at 405 nm using a Titertek Multiscan plate reader (Flow Laboratories, Inc., McLean, VA). Absorbance values were arbitrarily considered positive if they were twice those of the equivalent mock-inoculated control.

Wheat Streak Mosaic Virus and Triticum Mosaic Virus Screening Virus source and maintenance: The 06-123 isolate of TriMV was isolated from wheat at the Kansas Agricultural Research Center– Hays (Seifers et al., 2008). The Sidney 81 isolate of WSMV was collected near Sidney, NE, in 1981 (Seifers et al., 2006). Both viruses were propagated separately by mechanically inoculating the wheat cultivar Tomahawk (PI 478006) at the single-leaf stage using the leaf-rub technique (Seifers et al., 2006), with a 1:10 (wt:vol) ratio of tissue to extract buffer (0.02 M potassium phosphate buffer, pH 7 with 1 g of 600 mesh Crystolon flour B per 100 mL of extract). Following inoculation, the plants were held in a greenhouse (temperature range of 18 to 29°C) and harvested after 14 d. Testing for virus resistance: Two metal flats (21 × 31 cm) were fi lled with Harney clay loam soil (fi ne montmorillonitic, CROP SCIENCE, VOL. 49, JULY– AUGUST 2009

mesic Typic Argiustoll). Experimental wheat sources were planted, five seeds per row for each temperature treatment in each of the two experiments, on consecutive days. The cultivars Overley, Karl92, and Triumph 64 were included as susceptible controls. The WSMV-resistant controls were TA5040, RonL, and KS96HW10-3 (Seifers et al., 1995, 2006). Following inoculation, one flat was moved to a growth chamber set at 18°C with 8 h of illumination (20,330 lux) per day. The second flat was moved to a growth chamber at 24°C with the same lighting conditions. For the 18°C treatment, the plants were rated for symptom expression at 28 days post-inoculation (DPI) and for the 24°C treatment at 21 or 28 DPI.

RESULTS AND DISCUSSION Redesignation and genomic origin of chromosome 4Ai#2: Previously chromosome 4Ai#2 was designated as a homeologous group-4 Th. intermedium chromosome of unknown genomic origin (Friebe et al., 1991). Sequential GISH patterns of the wheat–Th. intermedium chromosome addition line DA4Ai#2 using genomic Ps. spicata and genomic Th. intermedium DNA as probes are shown in Fig. 1a and b, respectively. Thinopyrum intermedium genomic DNA painted chromosome 4Ai#2 uniformly over its entire length, whereas Ps. spicata genomic DNA hybridized to proximal and distal regions in both arms with no hybridization signals in the middle of the arms. The J genome of Th. intermedium (JJsS) is related to the E genome of Th. elongatum (Host) Beauv. (2n = 2x = 14, E) and the J genome of Th. bessarabicum (Savul. and Rayss) A. Löve (2n = 2x = 14, J). The S genome of Th. intermedium is related to the S genomes of Ps. strigosa (M. Bieb.) A. Löve (2n = 2x = 14, S) and Ps. spicata. The Js genome of Th. intermedium is a modified genome with S-genome specific sequences present around the centromeres (Dewey, 1984; Chen et al., 1998a,b, 1999, 2003). The GISH pattern using Ps. strigata total genomic DNA confirmed that 4Ai#2 is a Js–genome chromosome. Therefore, this chromosome is now designated as 4Js and the translocation chromosome as T4DL·4JsS. Characterization of recombinants: GISH patterns of the translocation line T4DL·4JsS and the five primary recombinants rec36, rec45, rec64, rec87, and rec213 are shown in Fig. 1c–h, and detailed C-banding and GISH patterns of the critical chromosomes involved in the Wsm1 transfer are shown in Fig. 2. The recombinant rec36 consists of the long arm of 4D, most of the short arm of 4JsS, and a distal segment derived from 4DS of wheat (T4DL·4JsS-4DS), whereas the recombinants rec45, rec64, rec87, and rec213 consist of the long arm of 4D, most of the short arm of 4D, and a distal segment derived from 4JsS of Th. intermedium (T4DL·4DS-4JsS). Chromosome measurements on 10 recombinants of each line after GISH revealed that the sizes of the Th. intermedium segments in rec45, rec64, rec87, and rec213 correspond to 41 ±7%, 32 ±5%, 35 ±5%, and 39 ±8% of their short arms. The distal 4DS wheat segment in rec36 corresponds to

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Figure 1. Genomic in situ hybridization (GISH) patterns of wheat (Triticum aestivum L.) Thinopyrum intermedium introgression lines using (a) total genomic Pseudoroegneria spicata DNA and (b–h) total genomic Th. intermedium DNA as probes: (a) and (b) disomic addition line DA4Js; (c) Robertsonian translocation line T4DL·4JsS; (d) rec36; (e) rec45; (f) rec64; (g) rec87; and (h) rec213.

Figure 2. C-banding and genomic in situ hybridization (GISH) pattern of the critical chromosomes involved in the Wsm1 transfer. Top row from left to right: C-banding pattern of 4Js, GISH pattern of 4Js using total genomic Thinopyrum intermedium and Pseudoroegneria spicata DNA as probes, C-banding patterns of 4D and T4DL·4SsS, and GISH patterns of T4DL·4JsS using total genomic Th. intermedium and Ps. spicata DNA as probes. Bottom row left to right: GISH pattern of wheat (Triticum aestivum L.)–Th. intermedium recombinants using total genomic Th. intermedium DNA as a probe.

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21 ±6% of its short arm. The sizes of the distal Th. intermedium segments in these recombinants are larger than those estimated from molecular marker analysis. Qi et al. (2007) reported that the breakpoints in all these recombinants are located in the distal deletion bin delineated by the deletion stock del4DS-2 and the telomere, corresponding to the distal 18% of this arm. The recombinants rec64 and rec87 have similar breakpoints and the smallest Th. intermedium segments detected by marker BE403913/HindIII, whereas rec36, rec45, and rec213 have more proximal breakpoints detected by marker BF291316/EcoRV (Qi et al., 2007). Although the size of the distal Th. intermedium segments on the basis of the presented GISH data are larger than those inferred from mapping studies, they also suggest that rec45 and rec213 have larger Th. intermedium segments than rec64 and rec87. Because of the nature of GISH, the fluorescein-labeled Th. intermedium segments fluoresce much brighter than wheat chromatin, which results in an overestimation of the Th. intermedium segments (Lukaszewski et al., 2005). However, the size of the distal wheat segment in rec36 determined by GISH was 21% of the arm, which matches well with the size determined by molecular marker analysis (18%; Qi et al., 2007). Wheat streak mosaic virus resistance evaluations: All recombinants except rec36, together with resistant and susceptible controls, were screened based on phenotypic symptoms and ELISA in Exp. 1, and all materials were evaluated in Exp. 2. The results were consistent in both experiments (Table 1). At 18°C, only the susceptible controls Overley, Karl 92, Triumph 64, and rec36 developed symptoms when inoculated with WSMV (Table 1). Lines TA5040, rec64, rec87, rec213, RonL, and KS96HW10-3 were not infected with WSMV at this temperature. When inoculated with TriMV, Overley, Karl 92,Triumph 64, RonL, and rec36 developed symptoms, whereas rec45, rec64, rec87, rec213, TA5040, and KS96HW10-3 were not infected. At 24°C, some plants in all lines developed symptoms when inoculated with WSMV (Table 1). In the first experiment only one plant was symptomatic in lines rec64 and rec87, whereas in the second experiment 7 out of 10 and 6 out of 8 plants were symptomatic. In addition, two KS96HW10-3 plants were symptomatic. These three wheat lines also had the fewest symptomatic plants when inoculated with TriMV when held at 24°C. When analyzed by ELISA, only symptomatic plants inoculated with TriMV or WSMV were positive to their respective antiserum. The only recombinant that was susceptible to systemic infection with WSMV and TriMV at 18°C was rec36, which is the only recombinant that has 21% of the distal segment of 4JsS missing, being replaced with 4DS, indicating that the resistance to WSMV is located within the distal 21% of the 4DS-4JsS short arm. The lack of systemic infection in RonL and KS96HW10-3 observed at 18°C in both tests was expected

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†

‡

owing to the resistance to systemic infection with Table 1. Numbers of symptomatic wheat plants of different lines following mechanical inoculation with Wheat streak mosaic virus (WSMV) WSMV at this temperature (Seifers et al., 1995; Seif- or Triticum mosaic virus (TriMV) when held at 18°C for 28 days posters et al., 2006). At 24°C, some or all of the plants in inoculation (DPI) or at 24°C for 21 DPI (Exp. 1) and when held at 18°C or these lines developed systemic mosaic as expected 24°C for 28 DPI (Exp. 2). because of the breakdown of the WSMV resistance 18°C 24°C at this temperature (Seifers et al., 1995, Seifers et al., Entry WSMV TriMV WSMV TriMV 2006). All RonL plants were systemically infected 1 2 1 2 1 2 1 2 by TriMV at 18 and 24°C as expected, because Overley 9/9 19/19 9/9 8/19 8/8 18/18 9/9 17/21 the temperature-sensitive resistance to WSMV in Karl 92 8/8 10/10 8/8 1/5 10/10 8/8 9/9 6/9 RonL is not effective against infection with TriMV Triumph 64 17/17 15/15 17/17 16/18 18/18 20/20 18/18 16/19 (Seifers et al., 2008). These results demonstrate for rec36 N/A 8/8 N/A 9/10 N/A 9/9 N/A 5/9 the first time that the T4DL·4JsS translocation stocks rec45 0/10 1/9 0/10 0/9 10/10 10/10 10/10 5/9 TA5040 and KS96HW10-3, as well as the derived rec64 0/10 0/9 0/10 1/10 1/10 7/10 2/9 6/10 distal recombinants rec45, rec64, rec84, rec213, rec87 0/9 0/6 0/8 1/8 1/6 6/8 5/6 6/6 have temperature-sensitive resistance at 18°C to rec213 0/10 0/10 0/10 1/10 10/10 10/10 10/10 5/10 systemic infection with TriMV, but this resistance TA5040 0/9 0/7 0/9 0/7 8/10 9/9 9/9 4/9 is ineffective at 24°C. KS96HW10-3 0/17 0/18 0/15 0/16 2/19 13/20 5/18 10/20 The presented data show that we successfully RonL 0/17 0/19 16/16 11/18 18/18 15/20 19/19 13/17 shortened the Th. intermedium segment in the distal †The numerator represents the number of symptomatic plants and the denominator the number recombinants rec45, rec64, rec87, and rec213, while of plants inoculated. still retaining the Wsm1 gene. The T4DL·4DS-4JsS ‡All symptomatic plants had mosaic symptoms, some more pronounced than others. The plants held at 18°C were analyzed by enzyme-linked immunosorbent assay, and only the symptomatic recombinant chromosome of the rec213 stock was plants tested positive against the homologous antiserum. transferred to adapted Kansas hard red winter wheat Chen, Q., B. Friebe, R.L. Conner, A. Laroche, J.B. Thomas, and B.S. and a germ plasm was released as KS08WGGRC50 Gill. 1998b. Molecular cytogenetic characterization of Thinopy(Gill et al., 2008). We hope that the reduced size of the Th. rum intermedium-derived wheat germplasm specifying resistance intermedium segment in KS08WGGRC50 will improve to wheat streak mosaic virus. Theor. Appl. Genet. 96:1–7. the agronomic performance and broaden the use of Wsm1 Chen, Q., R.L. Conner, A. Laroche, G. Fedak, and J.B. Thomas. in wheat improvement. Small seed samples of KS08WG1999. Genome origins of Thinopyrum chromosomes specifyGRC50 are freely available on request. ing resistance to wheat streak mosaic virus and its vector, AceAcknowledgments We thank John W. Raupp for critical reading of the manuscript. This research was supported by grants from the Kansas Wheat Commission and a special USDA-CSREES grant to the Wheat Genetic and Genomic Resources Center. Z.J. Chang’s visit at the Wheat Genetic and Genomic Resources Center was supported by a grant from the Shanxi Scholar Committee of China. This paper is contribution number 09-066-J from the Kansas Agricultural Experiment Station, Kansas State University, Manhattan, KS 66506-5502.

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