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Variation and Geographical Distribution of Perisperm Starch in Grain Amaranths (Amaranthus Spp.), and the Origin of Waxy Perisperm Type

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Variation and Geographical Distribution of Perisperm Starch in Grain Amaranths (Amaranthus Spp.), and the Origin of Waxy Perisperm Type Trop. Agr. Develop. 60（3）：172 － 178，2016 Variation and Geographical Distribution of Perisperm Starch in Grain Amaranths (Amaranthus spp.), and the Origin of Waxy Perisperm Type Kazuhiro NEMOTO1, *, Mineo MINAMI1, and Tsukasa NAGAMINE2 1 Graduate School of Agriculture, Shinshu University, 8304 Minamiminowa, Nagano 399-4598, Japan 2 National Institute of Agrobiological Sciences, 2-1-2 Kannondai, Tsukuba, Ibaraki 305-8602, Japan Abstract Excluding cereals, grain amaranths are known as the only crop with non-waxy and waxy starch types in seeds. We examined the amylose content stored in the perisperm and starch types; non-waxy, waxy and low-amylose types in 266 accessions of three grain amaranth species i.e. Amaranthus hypochondriacus L., A. cruentus L. and A. caudatus L. from around the world. In the accessions from the New World where these species were domesticated, a wide range of amylose contents and all the starch types were detected. Conversely, very limited variation of this trait was observed in the accessions from Asia and Africa. We concluded that the waxy type originated in the New World before being disseminated into Asia and Africa. However, the selection pressure for the waxy type in the perisperm of grain amaranths in the New World was considered to differ from that acting on cereal crops because of differences in the use and people’s preference for sticky food. Key words: Amaranthus spp., Amylose content, Geographical distribution, Grain amaranth, Waxy type In previous reports, the waxy starch type of a grain Introduction amaranth, which stained reddish brown with iodine The starch-rich seeds of grain amaranths (Amaran- solution, had been observed in A. leucosperma S. Wats. thus spp.), which belong to the family Amaranthaceae in (= A. hypochondriacus) (Wolf et al., 1950) and A. cruentus the Eudicots, are used as cereals, as well as quinoa and (MacMasters et al., 1955). Since then, intraspecific dif- buckwheat grain. The seed storage starch of grain ama- ferentiation of the types, non-waxy and waxy in A. hy- ranths is located in the diploid perisperm (2n), which is pochondriacus (Sakamoto, 1982), low-amylose type in A. a modified nucellus of the embryo sac, while in the grass caudatus (Tomita et al., 1980) and non-waxy, waxy and family (Poaceae), starch stored in cereal grains is depos- low-amylose types in A. cruentus (Inouchi et al., 1999) ited in the triploid endosperm (3n). They consist of three has been reported. Inheritance of the waxy perisperm cultivated species i.e. A. hypochondriacus L., A. cruentus trait is controlled by a single major structural gene with L. and A. caudatus L., all of which were domesticated the waxy allele, which is recessive to the Waxy allele in from early time in the New World (Sauer, 1976). A. hypochondriacus (Okuno and Sakaguchi, 1982). Starch is a complex polysaccharide composed of After the discovery of the New World by Columbus, amylose and amylopectin molecules. Non-waxy (non- the cultivation of grain amaranths was disseminated glutinous) starch contains both amylose and amylopec- throughout Asia and Africa far away from their area of tin, while waxy starch (glutinous) is composed of only origin. Especially, the southern foot of the Himalayas in amylopectin, or amylopectin with a very little amylose. the Indian subcontinent is considered to be the second- In grain amaranths, the perisperm starch has the waxy ary center of genetic diversity (Sauer, 1976), which con- type, which was differentiated from the non-waxy type trasts markedly with the decline of amaranth cultivation by spontaneous mutation (Sakamoto, 1997). This prop- in the New World. erty of the grain amaranths is unique in the Eudicots, The waxy/non-waxy trait which is correlated to the in other words, except for cereals such as rice, foxtail amylose content of the starch granules in grains, is an millet, common millet, Job’s tears, sorghum, barley and important characteristic for the breeding of cereal crops, maize. particularly in rice, because differences in the amylose content affect the texture of the processed grains. Communicated by K. Irie However, research on this aspect in grain amaranths is Received Oct. 13, 2015 limited. In addition, variations of the amylose content of Accepted Jan. 8, 2016 these grain amaranths and the geographical distribution * Corresponding author [email protected] have not been revealed yet. In the present study, we Nemoto et al.: Variation of perisperm starch in grain amaranths 173 described the variations of the amylose content and the A. hypochondriacus, 99 of A. caudatus, and 70 of A. cruen- geographical distribution in three grain species using tus, collected from Central and South America, Asia, and amaranth genetic resources collected from around the Africa, were used in the present study (Table 1). Among world. We also analyze of the origin of the waxy peri- them, 219 strains were provided from the USDA-ARS sperm type in grain amaranths. National Plant Germplasm Amaranth Collection and 47 accessions of A. hypochondriacus and A. caudatus from Materials and Methods around Asia were collected by Shinshu University. Some Plant materials accessions consisted of mixtures of seeds with different A total of 266 accessions of grain amaranths, 97 of seed coat color and/or appearance of the perisperm. In Table 1. Geographical distribution of perisperm starch types identified by I2KI staining in three grain amaranth species. No. of Perisperm starch type Origin strains Non-waxy Low-amylose Waxy A. cruentus Central and South America Mexico 33 1 2 30 Guatemala 15 14 - 1 United States 6 1 - 5 Peru 3 3 - - Asia India 4 4 - - Africa Nigeria 2 2 - - Ghana 3 3 - - Zambia 3 3 - - Zaire 1 1 - - Total 70 32 2 36 A. caudatus South America Peru 37 9 3 25 Bolivia 29 1 6 22 Argentina 7 6 1 - Ecuador 1 1 - - Asia Nepal 18 - 18 - India 5 - 5 - Pakistan 1 - 1 - Bhutan 1 - 1 - Total 99 17 35 47 A. hypochondriacus Central and South America Mexico 46 35 - 11 United States 2 - - 2 Guatemala 1 1 - - Puerto Rico 1 1 - - Brasil 1 - - 1 Chile 1 - - 1 Asia Nepal 22 2 - 20 Pakistan 6 - - 6 India 5 - - 5 China 5 - - 5 Bhutan 2 - - 2 Afganistan 1 - - 1 Africa Nigeria 2 1 - 1 Uganda 1 - - 1 Zambia 1 - - 1 Total 97 40 - 57 Grand total 266 89 37 140 174 Trop. Agr. Develop. 60（3）2016 that case, seeds were separated and analyzed as a differ- distribution of the amylose content in A. cruentus and A. ent accession. hypochondriacus showed two clear peaks. In A. caudatus, the number of accessions tended to decrease when the Measurement of amylose content amylose content increased. The amylose content of perisperm starch was mea- I2KI staining and seed appearance of A. cruentus sured colorimetrically using a TECHNICON SOLID- and A. caudatus revealed the existence of three types PREPTM II autoanalyzer (Instruments Co., NY). Given of perisperm starch (waxy, low-amylose and non-waxy) the large number of samples that had to be measured, in these species (Table 1). On the other hand, the ac- whole grain powder instead of purified starch granules cessions of A. hypochondriacus only contained two types from the grains was used for the analysis. Twenty milli- (waxy and non-waxy). The three types, waxy, low-amy- grams of grain powder passed through a 50-mesh screen lose and non-waxy ranged from 0 to 2.9%, 1.8 to 2.7% and was gelatinized in a mixture of 0.5N NaOH for more than 4.4 to 12.0% in A. cruentus, 0 to 1.9%, 0.9 to 5.9% and 8.0 to two hours at room temperature, and then applied to the 17.7% in A. caudatus, respectively. In A. hypochondriacus, autoanalyzer. The amylose content was calculated using the two types, waxy and non-waxy ranged from 0 to 2.7% a calibration curve made from using values obtained and 6.8 to 15.9%, respectively. Because the value of the from starch granule from Oryza sativa L. and A. cruentus amylose content is relative, waxy and low-amylose types (Table 2). The measurements of all the accessions were could not be differentiated clearly from each other. The conducted in triplicate. variation range of both types in the two species over- lapped, although both types could easily be identified by Identification of perisperm starch type the appearance of the perisperm (See Fig. 2). Among the Accessions were classified into three groups based three types, the waxy type predominated in all the three on the perisperm starch type, i.e. non-waxy, low-amylose species (Table 1). Whereas only 2 accessions consisted and waxy, which could be clearly distinguished from of the low-amylose type in 70 A. cruentus, 33 low-amylose one another by I2KI staining; grain powder of non-waxy, accessions were found in 99 A. caudatus. low-amylose and waxy types stained blue, purple and reddish brown, respectively (Fig. 1). In addition, these Geographical distribution of amylose content and peri- types could also be distinguished based on the perisperm sperm starch type appearance, when the seed was not covered with the The geographical distribution of the amylose con- seed coat colored dark brown or black. Non-waxy and tent and perisperm types is shown in Fig. 4 and Table low-amylose types of perisperms were translucent, while 1. Wide variation of both traits was observed in Central the waxy type of it was opaque, respectively (Fig. 2). and South America where these species had been do- mesticated, while limited variation was observed in Asia Results and Africa. Variation of amylose content and perisperm starch type In A. cruentus, all the accessions from Asia and Af- The amylose content of the accessions used in the rica belonged to the non-waxy type.
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