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Published online 20 May 2008
Published in Crop Sci 48:1117-1123 (2008)
© 2008 Crop Science Society of America
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Possible Transmission Route for Common Wheat to the Far East in Asia

H. Nakamura*

National Institute of Crop Science (NICS), Tsukuba, Ibaraki 305-8518, Japan

* Corresponding author (hiro{at}affrc.go.jp).


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
High molecular weight (HMW) glutenin alleles, such as Glu-D1, have an important effect on the quality of Japanese noodles (udon). The Glu-D1f allele is of particular significance to common wheat (Triticum aestivum L.). The frequency of the Glu-D1f allele differs among geographical areas, and it has been identified in wheat from northern and southern Japan, from Xinjiang, Nanjing, Zhejiang, and Beijing in China, the Korean Peninsula, and Afghanistan. However, a particularly high frequency of the Glu-D1f allele has been found in wheat from southern Japan. On the basis of the distribution of an adaptively neutral character, two specific routes of transmission of common wheat to the Far East have been suggested. In the first scenario, common wheat was introduced from Afghanistan, transported to Xinjiang in northwest China, then to Shaanxi, Nanjing, and Zhejiang in southeast China, and finally to southern Japan along the so-called Silk Road. In the second scenario, common wheat was introduced from Afghanistan, transported to Xinjiang in northwest China, then to Shaanxi and Beijing in northeast China, then to the Korean Peninsula, and finally to southern Japan. In a previous study, only the Chinese Route was revealed. Through the course of its transmission and its adaptation to diverse local environments, Japanese common wheat has developed a unique composition of glutenin Glu-D1 alleles, including Glu-D1f.

Abbreviations: HMW, high molecular weight • udon, Japanese noodles


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
HIGH MOLECULAR WEIGHT (HMW) glutenin subunits make up a group of seed endosperm proteins of common wheat (Triticum aestivum L.). These endosperm proteins are characterized by having molecular weights of between 80,000 and 145,000, and a complex biochemical structure that involves disulphide bonds (Payne et al., 1979; Shewry and Tatham, 1990; Nakamura et al., 1990). This group has been extensively explored during the past 25 years and its members have an important effect on the quality of bread and noodles made from wheat. HMW glutenin alleles, such as Glu-D1, are of particular significance for Japanese bread and udon products (Nakamura and Fujimaki, 2002a). The Glu-D1f allele has a major influence on Japanese common wheat. It is thus important to understand the genetic diversity of this allele in noodle-culture zones such as Asia compared with bread-culture zones such as Europe, Canada, and the U.S. (Nakamura, 2001a; Nakamura and Fujimaki, 2001b).

HMW subunits controlled by alleles at the Glu-A1, Glu-B1, and Glu-D1 loci are located on the long arms of chromosomes 1A, 1B, and 1D, respectively (Payne et al., 1987). Common wheat (2n = 42, AABBDD) is thought to have originated about 7000 years ago in the Middle and Near East. It was subsequently transported to Europe, Africa, southern Asia, and China (Tsunewaki, 1966; Nishikawa et al., 1980). The cultivation of wheat can be traced back 3000 years to China (Zhang, 1983), where it was a major crop at the time (Sun et al., 2000). Some common wheat varieties were transported along the so-called Silk Road through China to the Far East, the Korean Peninsula, and finally Japan. Little is known, however, about the precise route of transmission of common wheat to Japan.

Previous studies have concentrated on the variation in the HMW glutenin Glu-D1 allele, and the factors that have affected its distribution in different parts of the world (Nakamura et al., 1999; Nakamura, 1999; 2000a; 2000b; 2000c; 2001a; Nakamura and Fujimaki, 2001b; 2002a). Recently, a specific route of transmission for common wheat to eastern China and Japan was suggested (the Chinese transmission route in Fig. 1 ) (Nakamura, 2002b). Variation in the frequency of the Glu-D1f allele in different wheat varieties suggested a possible transmission route for common wheat to the Far East and Japan (Nakamura, 2002b).


Figure 1
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  		Figure 1. Geographical distribution of Glu-D1f allele in common wheat in Asia; a, origin of common wheat; b, Afghanistan; c, Xinjiang; d, Shaanxi; e, Nanjing; f, Zhejiang; g, South Japan; h, North Japan; i, Beijing; j, the Korean Peninsula.

 
Distribution of the Glu-D1 alleles throughout Asia, including the Korean Peninsula, was examined to estimate the route by which common wheat reached the most geographically remote regions of its production in the Far East.


   MATERIALS AND METHODS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The allelic composition of the HMW glutenin subunit investigated was among 1058 wheat genotypes in 131 Japanese improved cultivars, 174 Japanese landraces, 72 Korean landraces, 353 Chinese landraces, 150 Turkish landraces, three Syrian landraces, six Israeli landraces, four Iranian landraces, one Iraqi landrace, 23 Indian landraces, 15 Pakistani landraces, seven Bhutanese landraces, 66 Nepalese landraces, one Myanmar landrace, one Filipino landrace, two Thai landraces, three Indonesian landraces, and 46 Taiwanese landraces of common wheat. The 72 Korean Peninsula wheat varieties were from North Korea and South Korea. The 353 Chinese wheat varieties were from Heilongjiang, Jilin, Liaoning, Hebei, Beijing, Shandong, Shaanxi, Shanxi, Hangzhou, Zhejiang, Henan, Jiangsu, Ningxia, Gansu, Xinjiang, Sichuan, Anhui, and Jiangxi.

The seed storage proteins were investigated by sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE), according to the procedure described by Payne et al. (1979). The gels comprised 10% (w/v) acrylamide and 0.2% (w/v) bis-acrylamide containing 1.5 M Tris-HCl (pH 8.8) and 0.27% SDS. The stacking gel contained 0.25 M Tris-HCl (pH 6.8). A wheat flour sample (10 mg) was suspended in 300 µL of 0.25 M Tris-HCl buffer (pH 6.8) containing 2% (w/v) SDS, 10% (v/v) glycerol, and 5% (v/v) mercaptoethanol, and then shaken for 2 h at room temperature. The suspension was heated at 95°C for 3 min. The top portion of the supernatant was collected after centrifugation for 3 min at 12,000 rpm, and 30 µL of the extract was loaded into each of the gel slots. The electrode buffer was 0.025 M Tris-glycine (pH 8.3) containing 0.1% (w/v) SDS. Electrophoresis was conducted at a constant current of 30 mA for 4 h until the bromophenol blue dye ran to the end of the gel. The HMW glutenin 2.2 subunit is controlled by the Glu-D1f allele on chromosome 1D. To determine the electrophoretic mobility of each HMW glutenin band (allele) by SDS-PAGE, the following standards were included, Bezostaya, Champlein, Chinese Spring, Danchi, Dunav, Federation, Gabo, Hobbit, Hope, Norin 61, Lancota, Sappo, and Serbian (Payne and Lawrence, 1983; Nakamura et al., 1999).

The Japanese, Korean, Chinese, and other Asian hexaploid wheat materials were provided by the National Institute of Agrobiological Resources (NIAR), Tsukuba, Japan. Data were available on the worldwide distribution of Glu-1 alleles for 1380 cultivars from 21 countries, and on the frequencies of the HMW glutenin alleles for the Japanese and Korean Peninsula wheat varieties (Graybosch et al., 1990; Khan et al., 1989; Lawrence, 1986; Lukow et al., 1989; Ng and Bushuk, 1989; Payne et al., 1987; Morgunov et al., 1990; 1993; Pogna et al., 1989; Rogers et al., 1989; Uhlen, 1990). These data sets were compared with the results for 1179 common wheat varieties from Asia, including the Korean Peninsula, determined in the current study.

A chi-square test for independence was calculated to test for frequency differences among the Glu-D1f alleles by using the JMP6 Japanese version of SAS (SAS Institute Japan Co., Ltd.). The frequencies of the Japanese improved cultivars, Japanese landraces, and those from other Asian areas (Turkey, Syria, Israel, Iran, Iraq, India, Pakistan, Bhutan, Nepal, Myanmar, The Philippines, Thailand, Indonesia, and Taiwan, Afghanistan, and the Korean Peninsula) were analyzed relative to those of China using independent pair-wise comparisons. Chi-square values were obtained by treating the Japanese variety frequencies as expected values, and using the observed frequencies of the cultivars from other areas in Asia.


   RESULTS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The present study showed that carriers of the Glu-D1f allele were distributed across a limited region of Asia, comprising southern and northern Japan, Xinjiang in northwest China, Nanjing and Zhejiang in southeastern China, Beijing in northeast China, the Korean Peninsula, and Afghanistan. However, the allele was relatively rare in wheat varieties from north Japan, the Korean Peninsula, China, and Afghanistan (Table 1 and Fig. 1). The frequencies of Glu-A1, Glu-B1, and Glu-D1 alleles in common wheat varieties are known to differ between Japan and other countries (Morgunov et al., 1993; Nakamura et al., 1999; Nakamura, 1999). The HMW glutenin 2.2 subunit controlled by the Glu-D1f allele was frequently found among Japanese improved cultivars, as well as in Japanese landraces. However, only a few of the Korean, Chinese, and Afghani wheat varieties possessed this allele (Table 1).


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  		Table 1. Frequency of Glu-D1f allele among wheat genotypes from different geographical regions.

 
Glu-D1f was reported to be rare in previous studies of the worldwide distribution of Glu-1 alleles (Morgunov et al., 1993; Nakamura and Fujimaki, 2002a). Moreover, this allele was found to be more common in wheat seed storage proteins from Japan than in those from bread-culture zones (Morgunov et al., 1993; Nakamura, 2000a; 2000b; 2001a). The present study showed that the Glu-D1f allele was more common in Japan than elsewhere in Asia, including the Korean Peninsula (Table 1). The frequency of this allele was shown to be in excess of 35% among improved Japanese cultivars and 25.3% among Japanese landraces, while it was found in only 1.4% of Chinese varieties, 6.9% of Korean varieties, and 9.5% of Afghani varieties (Table 1 and Fig. 1). This allele was identified in five Chinese varieties [two in Xinjiang (labeled as "c" in Fig. 1), one in Jiangsu (labeled as "e" in Fig. 1), one in Zhejiang (labeled as "f" in Fig. 1), and one in Beijing (labeled as "i" in Fig. 1)], in five varieties from the Korean Peninsula (labeled as "j" in Fig. 1), and in two Afghani varieties (labeled as "b" in Fig. 1; Table 1). These results suggest that there are no other wheat cultivars possessing the Glu-D1f allele in any other region of Asia.

In this study, the Far East implies only the Korean peninsula and Japan, not including eastern China. The Far East is remote from most other wheat growing areas. In the course of its long journey and its adaptation to diverse local environments, Japanese common wheat appears to have depleted its genetic diversity. The frequency of the Glu-D1f allele differed between the Japanese and other Asian common wheat varieties, including those from the Korean peninsula. Therefore, it is possible that all Japanese wheat varieties have a common heritage. This hypothesis explains the similarities in Glu-1 patterns among Japanese wheat varieties.

The distribution of an adaptively neutral character revealed by this study suggests two specific routes of transmission for common wheat to the Far East—either to eastern China and Japan, or to eastern China, the Korean Peninsula, and Japan. In the first scenario, wheat was introduced from Afghanistan, transported to Xinjiang in northwest China, to Shaanxi, Nanjing, and Zhejiang in southeast China, and then to southern Japan along the Silk Road. In the second scenario, wheat was introduced from Afghanistan, transported to Xinjiang in northwest China, to Shaanxi and Beijing in northeast China, to the Korean Peninsula, and then to southern Japan. During the course of its transmission and its adaptation to diverse local environments, Japanese common wheat has developed a unique set of glutenin alleles including the worldwide rare Glu-D1f allele, which is correlated with the quality of Japanese udon products.

Two possible transmission routes for common wheat through the Far East were detected in this study, a Chinese Route that was previously reported (Nakamura, 2002b), and a new Korean peninsula route.


   DISCUSSION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
The current analysis of HMW glutenin alleles is expected to show the post-factum status of the loci, as, until recently, common wheat breeders in Japan had not manipulated Glu-1 alleles intentionally. The findings of this study might therefore reflect indirect changes in the genetic constitution of common wheat caused by selection for related or linked traits in Japanese wheat breeding programs. Japanese common wheat is characterized by high frequencies of alleles such as Glu-D1f at the Glu-D1 locus (Nakamura, 2000a; 2000b; 2000c; 2001a; Nakamura and Fujimaki, 2002a). Both natural and artificial selection are thought to have narrowed the genetic basis of Japanese common wheat, and the relatively frequent occurrence of the Glu-D1f allele supports this inference.

The unique composition of the Glu-1 glutenin alleles of Japanese common wheat is of considerable interest to both wheat breeders and cereal chemists. The objectives of common wheat breeding in Japan are largely based on the quality of salted white noodles (udon) (Nakamura, 2000c; Nakamura and Fujimaki, 2002a). In contrast, in areas where bread is more commonly consumed, similarities in the Glu-1 allele composition profile between countries seem to be based on bread making quality (Graybosch et al., 1990; Khan et al., 1989; Lawrence, 1986; Lukow et al., 1989; Ng and Bushuk, 1989; Payne et al., 1987; Morgunov et al., 1990; 1993; Pogna et al., 1989; Rogers et al., 1989; Uhlen, 1990). The current study has shown that the Glu-1 allele frequencies differ between noodle-culture zones such as Asia and bread-culture zones such as Europe, Canada, and the U.S. Glu-1 alleles directly affect wheat-gluten quality (Bushuk, 1996; Shepherd, 1996; Nakamura and Fujimaki, 2002a). It is thus likely that specific differences in Glu-1 patterns in Japan occur due to the intensity of selection pressure toward udon-noodle making quality, as opposed to selection for good bread-making quality (Nakamura and Fujimaki, 2001b; 2002a).

Four routes have been suggested by which people moved across Asia in ancient times. The first of these routes is the so-called Silk Road, which is divided into the Chinese route, or the route via the Korean Peninsula to Japan. This route ran from Afghanistan either through Xinjiang in northwest China, then Gansu, Ningxia, Xian (the capital city Shaanxi is located at the eastern end of the Silk Road), Nanjing, and Zhejiang in southeast China, or through Xinjiang in northwest China, then through Gansu, Ningxia, Xian (Shaanxi), and Beijing (Hebei), to the Far East, the Korean peninsula, and eventually Japan. The second route ran through Pakistan, India, and Myanmar, and then to Yunnan in China. The third route ran through Nepal or Pamir and Tibet, and then into Sichuan in southwest China or Shaanxi in northeast China. The fourth and final route ran directly into southern China by boat from India (Tsunewaki, 1966; Nishikawa et al., 1980; Tsujimoto and Tsunewaki, 1985; Tsujimoto et al., 1998).

The distribution of the Glu-D1 alleles is of great interest with respect to these routes across Asia. The Glu-D1a and Glu-D1f alleles were found to be widespread in Japanese common wheat. The Glu-D1a allele was commonly found in wheat varieties from all over Japan; whereas the Glu-D1f allele was present predominantly in those from the south (Nakamura et al., 1999; Nakamura, 1999; 2000a; 2000b; 2000c; 2001a; 2002b; Nakamura and Fujimaki, 2002a). According to this scenario, common wheat carrying Glu-D1a or Glu-D1f initially arrived and spread across southern Japan. The wheat was then transmitted northwards through Japan. As a consequence, the northern Japanese common wheat varieties predominantly carry the Glu-D1a allele (Nakamura, 2002b). Therefore, this allele may be linked to a gene that makes the wheat suitable for cultivation in the colder winters of northern Japan in contrast to the Glu-D1f allele, which is not linked to such a trait. Wheat varieties with the stronger winter habit (IV–VI) intensity of northern Japan do not possess the Glu-D1f allele (Nakamura and Fujimaki, 2002a). The high frequency of the Glu-D1f allele in southern Japan might be due to a selective advantage conferred either by the allele itself or by the action of another gene linked to udon-noodle making quality.

The Glu-D1f allele was found more frequently among improved varieties than in landraces in Japan (Table 1). This allele was present in improved cultivars prevalent in southern Japan (Nakamura and Fujimaki, 2002a). A noticeable geographical decline has been reported in the frequency of the Glu-D1f allele in Japan (Nakamura et al., 1999; Nakamura, 1999; 2000c; 2002b). To elucidate the factors involved in the establishment of this decline, a previous study also investigated the association of the glutenin Glu-D1f gene with winter growth habit and flour hardness (Nakamura and Fujimaki, 2001b; 2002a). As the Japanese islands extend a considerable distance from north to south, they present a diverse range of environments within which wheat is cultivated. Improved Japanese cultivars and locally grown landraces show diverse winter growth habits, reflecting the differences in the temperature during winter cultivation (Nakamura and Fujimaki, 2001b:2002a). The winter growth habit is the most important factor for Japanese common wheat production in the field; generally, less winter-hardy varieties are grown in southern Japan, and more winter-hardy varieties are grown in the north. The weaker winter habit (I–III) is found in southern Japan, and the stronger winter habit (IV–VII) intensity is in northern Japan. In fact, these genealogical examinations revealed that the Glu-D1f allele was present in the varieties in the Kyushu district (southern Japan), and frequently appeared in its pedigree. However, it was absent in the cultivars found in Hokkaido district (northern Japan), and was carried only by a few of its remote ancestors (Nakamura and Fujimaki, 2002a).

A strong correlation was previously observed between the winter-hardiness and the occurrence of the Glu-D1f allele (Nakamura and Fujimaki, 2001b: 2002a). Improved cultivars with weaker winter-growth habits tended to carry the Glu-D1f allele more frequently than those with stronger winter-growth habits, while the allele was absent from most winter-hardy cultivars cultivated in the northern part of Japan (Nakamura and Fujimaki, 2001b; 2002a). It was previously reported that Glu-1 alleles are not associated with ecogeographical parameters in a worldwide context (Morgunov et al., 1993). However, the results from the current study suggest that the Glu-D1f allele is associated with ecogeographical parameters in Japan (Nakamura and Fujimaki, 2001b: 2002a). Spring and facultative cultivars are sown in autumn and spring, respectively, in Afghanistan, Xinjiang in northwest China, Nanjing and Zhejiang in southeast China, and southern Japan. This style of cultivation is specific to these regions. Genotypes that are suitable for this type of common wheat cultivation in China might have been selected during the process of transmission to Japan. All of the varieties (both spring and facultative types) processing the Glu-D1f allele in northern Japan are sown in the autumn (Nakamura and Fujimaki, 2001b; 2002a).

The HMW glutenin 2.2 subunit controlled by the Glu-D1f allele is known to be associated with weak gluten strength, and has the most detrimental effect on bread-making quality among all of the subunits (Takata et al., 2000). Therefore, the Glu-D1f allele has an important role in the dough quality of Japanese wheats. Glu-D1f has previously been regarded as a characteristic glutenin allele of Japanese soft wheat cultivars that no hard wheat possesses (Nakamura and Fujimaki, 2002a). However, while many common wheat cultivars in southern Japan possess the Glu-D1f allele most northern Japanese cultivars do not. Furthermore, considerable variation in β-amylase isozymes is present among different varieties, which are split into 11 main phenotype groups (types A–K) (Ainworth et al., 1983). Types A and J are both shown to be common in Japan, with the former found throughout the country and the latter present predominantly in southern regions (Tsujimoto et al., 1998). This distribution of β-amylase isozyme types is similar to that of the Glu-D1f allele in Japanese common wheat. In addition, an analysis of five isozyme types (ADH, DIA, GPI, PER, and PGD) in 324 varieties of Chinese wheat showed the genetic diversity among eastern China to have similar geographical differentiation to that of Korea and Japan (Ghimire et al., 2006). The founder principle can explain many instances of rapid speciation and high local frequencies of alleles that are rare in other areas (Templeton, 1980). Hexaploid wheat brought to Japan probably included a limited subset of the wheat varieties found in China; the founder effect described in evolutionary literature is generally associated with gene frequencies on islands such as Japan (Nakamura and Fujimaki, 2002a). Recently, Xinjiang common wheat was characterized based on the genetic diversity revealed by microsatellite DNA polymorphisms and several agronomic traits. The results of a principal coordinate analyses revealed distinctive differentiation between Xinjiang common wheat landraces and foreign common wheats; the Xinjiang common wheat landraces appeared to be genetically differentiated from foreign common wheats, and were more closely related to those from neighboring countries such as Afghanistan, Pakistan, Turkey, and Russia than those from Japan and other parts of China (Cong et al., 2006). If cultivated hexaploid wheat originated in the Middle and Near East and traveled via the Silk Road through China to the Far East, the Korean Peninsula, and Japan, it could have been exposed to a selective bottleneck induced by the external environment, as well as a founder effect (as all of the populations went through a bottleneck). This selective bottleneck might have been extremely intense, and most ancestral populations might have become extinct in Japan (Nakamura and Fujimaki, 2002a). The theory presented here attempts to explain wheat's model of speciation and, more importantly, has generated testable predictions that can be examined in both natural and artificial selection using current methodologies and systems. This theory of Japanese wheat variety evolution demonstrates how population genetic theory can be applied to the problem of speciation in more extensive and thorough fashion than it has in the past.


   CONCLUSIONS
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
This study used the specific distribution of an adaptively neutral characteristic, the Glu-D1f allele, to suggest a transmission route for common wheat into East China, the Far East, the Korean Peninsula, and Japan. In the first scenario, common wheat was introduced from Afghanistan, transported to Xinjiang in northwest China, then to Shaanxi, Nanjing, and Zhejiang in southeast China, and finally to southern Japan along the so-called Silk Road. In the second scenario, common wheat was introduced from Afghanistan, transported to Xinjiang in northwest China, then to Shaanxi and Beijing in northeast China, then to the Korean Peninsula, and finally to southern Japan. These two pathways are also believed to have been the routes of transmission of noodles to Japan in ancient times (Ishige, 1991). These results indicate that the rare Glu-D1f allele is a powerful and useful analytical tool for investigating the transmission routes of common wheat in Asia.


   ACKNOWLEDGMENTS
 
The author thanks S. Ninomiya and H. Fujimaki for helpful discussions and comments, and T. Ihara, K. Tanaka, and S. Kawakami for assistance with the SDS-gel electrophoresis.


   NOTES
TOP
 NOTES
ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
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.

Received for publication January 10, 2008.


   REFERENCES
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 





This Article
Right arrow Abstract Freely available
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Right arrow Citing Articles via Google Scholar
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Right arrow Articles by Nakamura, H.
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Right arrow Articles by Nakamura, H.
Related Collections
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Right arrow Plant Genetic Resources
Right arrow Crop Genetics

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