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Polyploidy in an Amphimictic Population of Heterodera Glycines

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Polyploidy in an Amphimictic Population of Heterodera Glycines Heterodera canadensis n. sp.: Mulvey 371 the white females and cysts of the genus anhydrous glycerin. Nematologica 4:67-69. Heterodera (subgenus Heterodera), a cyst- 7. STONE, A. R. 1975. Head morphology of forming nematode. Can. J. Zool. 52:77-81. second-stage juveniles of some Heteroderidae 6. SEINHORST, J. W. 1959. A rapid method for (Nematoda:Tylenchoidea) Nematologica 21: transfer of nematodes from fixative to 82-88 + 7 plates. Polyploidy in an Amphimictic Population of Heteroder0 glycines ~ A. C. TRIANTAPHYLLOU and R. D. RIGGS2 Abstract: A tetraploid single-cyst isolate of Heterodera glycines from a field population from Indiana has been propagated in the greenhouse on Lee soybeans since its discovery, in 1973. The tetraploid isolate has n = 18 chromosomes, compared with n = 9 of the diploid H. glycines; it has larger cysts and larvae, but shows the same level of parasitism and host range as the diploid population from which it apparently evolved. Association of chromosomes is irregular at meta- phase I, with quadrivalents, trivalents, and univalents often observed in addition to the bivalents. The second maturation division is usually normal. About 80% of the mature oocytes (just before fertilization) have n = 18, and the other 20% have n = 17 or 19. Reproduction of the tetraploid isolate is exclusively by cross-fertilization. The discovery of such a tetraploid provides an experi- mental tool for the study of polyploidy in nematodes. Many amphimictic plant-parasitic nema- todes are suspected of representing polyploids. Key Words: soybean cyst nematode, cross- fertilization. Polyploidy has played a major role in determination (such as hermaphrodites), or the evolution of higher plants, especially by that reproduce uuiparentally (partheno- facilitating the establishment of allopoly- genesis)." Furthermore, Mayr implies that ploids, i.e., fertile pol),ploids of hybrid if polyploidy exists in amphimictic animals, origin (6, 11). More than one-third of all it may have been established during a species of plants are estimated to have arisen partheuogenetic stage in their evolution, or through polyploidy. In animals, polyploidy it occurs in animals in which sex is deter- is encountered frequently among partheno- miued by a definite sex gene rather than by genetic species, whereas in cross-fertilizing a balance of sex-determining factors. Sim- species it appears to be rare or, according to ilarly, Astaurov supported that polyploidy many authors, does not occur at all. Muller, in bisexual species of animals is rare and in 1925, reasoned that polyploidy in bi- probably has an indirect origin via poly- sexual species of animals upsets their sex ploid parthenogenesis and secondary re- chromosome mechanism and therefore can- versal to bisexuality (1). He also expressed not be successful (4). Although several other the opinion that the sterility of autotetra- explanations have been proposed since then, ploids is probably a more serious obstacle to imbalance in sex determination is still the the establishment of bisexual polyploidy most accepted explanation of the rarity of than the imbalance of the sex-determining polyploidy among animals. According to mechanism. White, in 1973, concluded that Mayr (3), "most alleged cases of polyploidy there may be a few genuine cases of evolu- in animals are based on a misinterpretation tionary polyploidy in bisexual animals, but of cytological evidence ('pseudopolyploidy') the topic is one that deserves further con- or are limited to forms that lack gametic sex sideration with objectivity and critical judg- ment (11). Received for publication 17 April 1979. The present article deals with an ap- XPaper No. 5912 of the Journal Series of the North Caro- lina Agricultural Experiment Station, Raleigh, North Caro- parent case of polyploidy in a plant-parasitic lina. This study was supported in part by National Science nematode which reproduces by cross- Foundation Grant No. DEB. 76-20968 A02. 2 Respectively Department of Genetics, North Carolina State fertilization. In 1973, tile junior author University, Raleigh, North Carolina 27650; and Department observed that larvae hatched from a cyst of of Plant Pathology, University of Arkansas, Fayetteville, Arkansas 72701. Heterodera glycines were distinctly larger 372 Journal of Nematology, Volume 11, No. 4, October 1979 than larvae from other cysts of the same and examined for eggs inside the uterus and field population. About 100 large larvae the state of development of the eggs. The from that special cyst and about 2,000 rest of the females were kept for 3 weeks in regular-size larvae from 10 other cysts of the a moist chamber and periodically examined same population were isolated and propa- for the production of embryonated eggs or gated separately on two soybean plants. for hatched larvae. Later, preliminary examination of larvae For the morphometric study, 50 yellow and females revealed that: a) larval size was females (cysts) were obtained from stock stable and characteristic of each isolate; b) cultures of each isolate, and the length and both isolates reproduced by cross-fertiliza- width of each were measured. The cysts tion; c) females of the isolate with large were then broken to release the eggs and larvae had about twice as many chromo- larvae. Four larvae were picked at random somes as those of the isolate with larvae of from each of 25 cysts from each isolate, regular size. These observations suggested mounted on slides in water, and heated the existence of polyploidy in a cross- gently to relax the larvae for easier measure- fertilizing nematode, a unique case that de- ment. Females were measured at 25×, larval served further consideration. The present length at 100×, and other morphometrics comparative study of the cytogenetic, mor- (Table 1) at 1,000×. phometric, and host-range characteristics of The host-range study was conducted in a the two isolates confirms the polyploid greenhouse at 25-30 C. The source of amphimictic nature of the isolate with the inoculum was cultures maintained in an large larvae. Further investigations are actively reproducing condition. Females and under way concerning the implications of cysts were obtained by the roiling and siev- polyploidy combined with amphimixis in ing method and placed in a Waring blender this nematode. to release the eggs and larvae. The suspen- sion of eggs and larvae was injected into the MATERIALS AND METHODS soil in each pot with an automatic pipette which delivered a uniform amount (about Tile population of H. glycines used was 2,000 eggs and larvae) to each pot. Some obtained in 1973 from a soybean field in plants were germinated in tile testing Vanderburgh County, Indiana. About 100 medium, whereas others were transplanted large-size larvae hatched from one cyst were from a stock source. Five weeks after inocu- used to inoculate a two-week-old soybean lation the females and cysts were recovered seedling (Glycine max Merr. cv Lee). An- separately from each plant by the roiling other 2,000 regular-size larvae obtained from and sieving method, and counts were made 10 cysts of the same population were used to using a stereomicroscope. The counts were inoculate a second soybean seedling. The converted to an index figure (index of para- two isolates thus established were propa- sitism) by dividing the number recovered gated separately on Lee soybeans for the from each plant by the average number re- following 5 years. covered from the Lee soybean cultivar and For the cytological study, egg-laying fe- multiplying by 100. males were processed and stained with propionic orcein as described for other OBSERVAT2ONS Heterodera species (8). To test for the capacity of females to Cytology and mode of reproduction: reproduce in the absence of males, single- Tile cytological behavior of the isolate with larva inoculations were made of soybean regular-size larvae (diploid isolate) was seedlings germinated in sand in plastic petri identical to that described for Heterodera dishes. Four days after inoculation, the glycines (9). Nine bivalent chromosomes seedlings were transplanted in 10-cm-diam were observed in metaphase 2 (Fig. 1), and pots filled with a I:I mixture of sand and nine univalents in telophase 2, polar body soil. Forty-five days after transplanting, the I, and metaphase 12 figures (Fig. 3). roots were examined for females, with or The general pattern of maturation of without egg masses. Some of the females oocytes of the isolate with large larvae found were stained with propionic orcein (tetraploid isolate) was also similar to that Polyploidy in Heterodera glycines: Triantaphyllou, Riggs 373 TABLE 1. Egg counts and morphometrics of a diploid and a tetraploid isolate of Heterodera glycines. Diploid Tetraploid Character isolate isolate 1) Larval body length (100)* 400 gm ± 12.9 b 642 #m --+ 21.5 2) Larval body width (100) 20.8 #m ± 0.6 23.2 #m ± 1.1 3) Larval stylet length (100) 22.6#m ± 0.3 27.8#m ± 0.7 4) Larval tail, clear portion (100) 25.3#m ± 1.3 36.4#m± 2.2 5) Larval DGO ~ (100) 4.6#m± 0.3 8.4gm± 0.7 6) Cyst length (25) 761 #m ± 20.0 891 #m ± 20.1 7) Cyst width (25) 521 #m ± 13.9 527 #m -- 13.9 8) No. of eggs in body (25) 112 __+ 6.4 126 ± 4.3 9) No. of eggs in egg mass (25) 7 ± 2.1 5 ± 3.3 *Number of observations. bMean ± standard error of the mean. *Distance of dorsal esophageal gland orifice from styler. described for H. glycines (9). However, the tetraploid isolate, especially during the sec- chromosome number in metaphase I figures ond maturation division of the oocytes, was difficult to determine because of ir- when the sperm nucleus chromosomes regular association of the chromosomes. In tended to become more discrete. some metaphase I figures, 18 bivalent After the second maturation division, chromosomes could be counted (Fig.
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