Brief communication. Preferential male transmission of an alien chromosome in wheat

Journal of Heredity, Jan 1998

A telocentric chromosome 5HtL from Elymus trachycaulus (Link) Gould ex Shinners was transferred into common wheat (Triticum aestivum L.). This chromosome was assigned to the homoeologous group 5 of Triticeae species by restriction fragment length polymorphism (RFLP) analysis. Chromosome 5HtL was transmitted in 20% of the female gametes and 97% of the male gametes in the genetic background of wheat, although the expected transmission frequencies of 5HtL through female and male gametes are 25% and 0-5% respectively. It is likely that a gene located on 5HtL promotes male gamete competition. We suggest that the long arms of homoeologous group 5 chromosomes in Triticeae species carry genes that affect their transmission through male gametes.

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Brief communication. Preferential male transmission of an alien chromosome in wheat

HortScience 0 Preferential Male Transmission of an Alien Chromosome in Wheat - No. No. Expectob- expect- ed served ed ratio Generation (N:R)a (N:R) (N:R) x2 WI 2757 (PA) 44:0 NCG-093 (PB) 0:16 F1 54:0 F2 122:41 BC1A 79:0 BC1B 47:33 44:0 0:16 54:0 122:41 79:0 40:40 1:0 0:1 1:0 3:1 1:0 1:1 a R 5 revolute; N 5 normal cotyledons. P value — — — — — — 0.002 .96 — — 2.45 .11 young ( Figure 1). The size and green color of the mutant cotyledons are the same as the normal cotyledons of WI 2757 (Peterson et al. 1982). The true leaves of the seedlings are also normal, and the cotyledons become difficult to distinguish from normal cotyledons when the plants reach the four true-leaf stage. In order to study the inheritance of the revolute cotyledons mutant, NCG-093 and WI 2757 were increased by self-pollination and checked for uniformity of cotyledon type to develop parental inbred lines. The two inbreds were crossed using hand-pollination in a greenhouse. The F1 progeny were self-pollinated to produce the F2 generation and also backcrossed to each parent to produce the BC1A ( F1 3 WI 2757) and BC1B ( F1 3 NCG-093). Seedlings were grown in flats of vermiculite on benches in the greenhouse (temperature 208C–358C with a 13–14 h photoperiod). Six days after seeding, plants were evaluated for cotyledon phenotype and classified as revolute or normal. The cross of normal cotyledons WI 2757 with revolute cotyledons NCG-093 produced all normal F1 progeny ( Table 1). Segregation in the F2 progeny fit the 3:1 expected ratio (P . .96), assuming the trait was controlled by a single recessive gene. Progeny segregation in the BC1A and BC1B generations verified the inheritance pattern for a single recessive gene observed in the F2 progeny. The BC1A (to NCG-093) segregated in a 1:1 ratio, with an adequate fit to expected values (P . .05). No revolute cotyledons seedlings were observed in BC1B (to WI 2757). We concluded that there was a single recessive gene for revolute cotyledons-2 in NCG-093 for which we propose the symbol rc-2. The mutant of Burpless Hybrid having revolute cotyledons described by Whelan et al. (1975) was lost, so it was impossible to compare the mutants for similarity or to cross them to test for allelism. Seeds of NCG-093 can be obtained from T.C.W. From the Department of Horticultural Science, North Carolina State University, Raleigh, NC 27695-7609 (Wehner), the USDA/ARS, Department of Horticulture, University of Wisconsin, Madison, Wisconsin (Staub), and the Department of Horticulture, Nanjing Agricultural University, Nanjing, China (Liu). The research reported in this publication was funded in part by the North Carolina Agricultural Research Service. The authors gratefully acknowledge the technical assistance of Tammy L. Ellington. Please address reprint requests to Dr. Todd C. Wehner, Department of Horticultural Science, North Carolina State University, Raleigh, NC 27695-7609. A telocentric chromosome 5HtL from Elymus trachycaulus (Link) Gould ex Shinners was transferred into common wheat (Triticum aestivum L.). This chromosome was assigned to the homoeologous group 5 of Triticeae species by restriction fragment length polymorphism (RFLP) analysis. Chromosome 5HtL was transmitted in 20% of the female gametes and 97% of the male gametes in the genetic background of wheat, although the expected transmission frequencies of 5HtL through female and male gametes are 25% and 0– 5%, respectively. It is likely that a gene located on 5HtL promotes male gamete competition. We suggest that the long arms of homoeologous group 5 chromosomes in Triticeae species carry genes that affect their transmission through male gametes. Jiang et al. 1994a). Production of wheatalien chromosome addition lines is usually the first step to do such transfers. One common character for most of the wheatalien monosomic addition lines (42 wheat chromosomes plus one alien chromosome) is the low transmission of the alien chromosome through pollen, often less than 5%. Thus pollen with the additional alien chromosome can hardly compete with normal ones in fertilization. During the past few years we have isolated several wheat-Elymus trachycaulus (2n 5 4x 5 28, genomically StStHtHt) chromosome addition lines (Jiang et al. 1994b; Morris et al. 1990) . In the selfed progenies of a monotelosomic 5HtL addition line, the telocentric chromosome 5HtL was detected almost exclusively in all the plants analyzed. This article reports on this rare case of preferential male transmission of 5HtL in the genetic background of wheat. Materials and Methods Wheat-E. trachycaulus monosomic addition line 5Ht (designated as MA 5Ht, chromosome constitution is 210 1 5Ht9), monotelosomic addition line 5HtL (MTA 5HtL, 210 1 5HtL9; 5HtL represents a telocentric chromosome derived from the long arm of 5Ht) and monoisosomic addition line 5HtL·5HtL (MIA 5HtL·5HtL, 210 1 5HtL·5HtL9; 5HtL·5HtL represents an isochromosome derived from the long arm of 5Ht) were isolated from the backcrossed progenies of an E. trachycaulus 3 Chinese Spring (CS) wheat hybrid. These lines were used for male and female transmission studies in crosses with CS wheat. Chromosomes 5HtL and 5HtL·5HtL were identified by Nbanding analysis ( Endo and Gill 1984) . For RFLP analysis, genomic DNA was isolated from young leaf tissue of wheat and the monosomic addition lines. DNA samples were digested with restriction enzyme HindIII and blotted to MSI membrane. Prehybridization and hybridization were done at 658C in 53 SSC, 100 mM NaPO4 (pH 6.5), 20 mM EDTA, 0.5% SDS, and 0.2 mg/ml denatured salmon sperm DNA. The membranes were washed at 508C in 0.13 SSC and 0.1% SDS, and exposed to X-ray film. The two group 5-specific RFLP markers, PSR118 and PSR128 (Sharp et al. 1989), were kindly provided by Dr. M. D. Gale, John Innes Center, Norwich, England. Results Genes from a number of wild species have been successfully transferred into cultivated wheat ( Islam and Shepherd 1992 ; Designation of Chromosome 5Ht Chromosome 5Ht has two characteristic Nbands near the centromere on the long Brief Communications 87 arm ( Figure 1). Therefore chromosomes 5Ht, 5HtL, and 5HtL·5HtL can be distinguished from all the wheat chromosomes. RFLP analysis with wheat homoeologous group 5-specific probes indicated that 5Ht belongs to group 5. The RFLP marker, PSR118, assigned to the short arms of group 5 chromosomes, hybridized to a specific DNA fragment derived from the short arm of 5Ht ( Figure 2a). Similarly the group 5 long arm marker, PSR128, hybridized to a DNA fragment from the long arm of 5Ht ( Figure 2b). Chromosome Transmission The telocentric chromosome 5HtL from a monotelosomic addition line showed male and female transmission frequencies of 0.97 (29/30) and 0.20 (2/10), respectively ( Table 1). Based on the previous estimates of transmission of alien chromosomes in the genetic background of wheat ( Hyde 1953; Riley 1960) , the expected transmission frequencies of 5HtL through male and female gamete are 0.00–0.05 and 0.25, respectively. The present data indicate a preferential transmission of 5HtL through the male gametes. Preferential male transmission was also observed in progeny of selfed MTA 5HtL. Assuming 0.20 female and 0.97 male transmission of 5HtL, we expected five ditelosomic addition (210 1 5HtL0) and 21 monotelosomic addition plants from a total of 27. This is close to the 6 and 21 plants observed for the respective classes ( Table 1). We also analyzed 20 seeds from a selfed population of a double monosomic 5B and 5Ht (200 1 5B9 1 5Ht9). Nineteen plants had at least one copy of 5Ht. This result indicated that the complete chromosome 5Ht has a similar male transmission behavior as its long arm 5HtL. A population of selfed MIA 5HtL·5HtL was analyzed for the transmission of the isochromosome 5HtL·5HtL. If an alien chromosome has no preferential transmission in the wheat genetic background, 25% monosomic additions and 75% euploid plants will be expected from selfed progenies of a monosomic addition line. While assuming 5HtL·5HtL has 20% female and 97% male transmission, similar to 5HtL, we expected about 20% diisosomic addition (210 1 5HtL·5HtL0) and 80% monoisosomic addition plants. The observed transmission of 5HtL·5HtL was in the middle of these expectations ( Table 1). Therefore the isochromosome 5HtL·5HtL showed reduced preferential transmission as compared to the telocentric chromosome 5HtL. About 38% (8/21) of the plants in the selfed progenies of MIA 5HtL·5HtL contained a 5HtL telosome. These telocentric chromosomes may have been derived from misdivision of the isochromosome 5HtL·5HtL. The meiosis of MTA 5HtL was studied. No abnormal meiotic behavior except lagging 5HtL was observed at anaphase I and anaphase II. More than 95% of the pollen grains of MTA 5HtL were of normal size, with two visible sperm nuclei and one vegetative nucleus. Discussion In plants, euploid male gametes generally have a distinct competitive advantage over male gametes with extra chromosomes. The frequency of disomic wheatalien chromosome additions among the progenies of monosomic additions is usually very low because of the low transmission of the alien chromosome through male gametes. In this study, the transmission of 5HtL through the female gametes (20%) is within the range (15–45%) of other E. trachycaulus chromosomes in the genetic background of wheat. However, 5HtL was transmitted in 97% of the male gametes, suggesting that the male gametes with 5HtL had a competitive advantage over euploid male gametes. Telocentric chromosome 5HtL was frequently detected in the selfed progenies of MIA 5HtL·5HtL and MA 5Ht ( Table 1). Most of these telocentric chromosomes probably originated in the pollen because they can be preferentially transmitted through male gametes. In contrast to 5HtL, the short arm of 5Ht (5HtS) was rarely recovered in the selfed progenies of MA 5Ht. The frequent recovery of 5HtL from the rare misdivision of 5HtL·5HtL and 5Ht again indicates a strong selective advantage of male gametes with 5HtL. The genetic mechanism of the preferential male transmission of 5HtL is not known, but it seems different from that reported for the gametocidal chromosomes from Aegilops species ( Endo 1990; Endo and Tsunewaki 1975; Maan 1975; Miller et al. 1982) . A gametocidal chromosome will cause abortion of the gametes lacking it, resulting in partial sterility and exclusive transmission of such chromosomes through both male and female gametes ( Endo 1990) . In the present case, more than 95% of the pollen from MTA 5HtL appeared normal, and both MA 5Ht and MTA 5HtL are fully fertile. In addition, no chromosomal structural changes were observed in the progenies derived from MA 5Ht, MTA 5HtL, and MIA 5HtL·5HtL, while chromosomal mutations were frequently detected in the progenies of wheat plants containing gametocidal chromosomes ( Endo 1990) . Another distinct characteristic of 5HtL is its preferential transmission only through male gametes. Gametocidal chromosomes are transmitted preferentially through both male and female gametes ( Endo 1990) . A possible genetic mechanism is that a gene located on 5HtL may be responsible for its preferential male transmission. This gene makes male gametes more competitive than the gametes lacking it. Supporting evidence for this hypothesis is that another homoeologous group 5 chromosome, 5St, from E. trachycaulus may have a similar gene that enhances male gamete transmission. Although this chromosome is not preferentially transmitted through male gametes like 5HtL, it was detected more frequently in the backcrossed derivatives of the E. trachycaulus 3 CS hybrids than the other six St genome chromosomes. The long arms of wheat chromosomes 5A, 5B, and 5D may also carry important genes for transmission of male gametes. Ditelosomic 5AS, 5BS, and 5DS, in which the long arm is absent, are among the few unavailable ditelosomic lines of CS wheat (Sears and Sears 1978). It has been impossible to recover ditelosomic 5AS, 5BS, and 5DS plants from progenies of selfed plants with the chromosome constitution of 200 1 5AS0 1 5AL9, 200 1 5BS0 1 5BL9, and 200 1 5DS0 1 5DL9, respectively. It is most likely that male gametes of 209 1 5AS9, 209 1 5BS9, and 209 1 5DS’ are not functional or they cannot compete with those of 209 1 5AS9 1 5AL9, 209 1 5BS9 1 5BL9, and 209 1 5DS9 1 5DL9, respectively. In the progenies of heterozygous 5A (or 5B or 5D) deletion lines, homozygous deletion plants were never recovered if the deleted 5A (or 5B or 5D) had less than 50% of the long arm ( Endo and Gill 1996) . This result suggests that male gametes with deleted 5A (or 5B or 5D) are not functional or are unable to compete with those having normal 5A (or 5B or 5D). The genes that are critical for male gamete transmission are possibly located on the proximal half of chromosomes 5A, 5B, and 5D. From the Wheat Genetics Resources Center and Department of Plant Pathology, Kansas State University, Manhattan, Kansas. This research was supported by USDA-CRGO grants. Contribution No. 96-161-J from the Kansas Agricultural Experiment Station, Kansas State University, Manhattan, Kansas. The authors thank Dr. T. R. Endo for valuable discussion and suggestions to improve the manuscript. Address correspondence to J. Jiang, Department of Horticulture, University of Wisconsin-Madison, Madison, WI 53706, or e-mail: . Morris KLD, Raupp WJ, and Gill BS, 1990. Isolation of Ht genome additions from polyploid Elymus trachycaulus (StStHtHt) into common wheat (Triticum aestivum). Genome 33:16–22. Riley R, 1960. The meiotic behaviour, fertility and stability of wheat-rye chromosome addition lines. Heredity 14:89–100. Sears ER and Sears LMS, 1978. The telocentric chromosomes of common wheat. In: Proceedings of the Fifth International Wheat Genetics Symposium, New Delhi, India, 23–28 February 1978 (Ramanujam S, ed). New Delhi, India: India Society of Genetics and Plant Breeding, IARI; 389–407. Sharp PJ, Chao S, Desai S, and Gale MD, 1989. The isolation, characterization and application in the Triticeae of a set of wheat RFLP probes identifying each homoeologous chromosome arm. Theor Appl Genet 78:342– 348. Received September 13, 1996 Accepted May 5, 1997 Corresponding Editor: Kendall R. Lamkey Low Allozyme Diversity in Schwalbea americana (Scrophulariaceae), an Endangered Plant Species M. J. W. Godt and J. L. Hamrick Schwalbea americana, a hemiparasitic member of the Scrophulariaceae, is an early successional, fire-dependent species of the eastern coastal plain of North America. We sampled 13 populations across the range of this endangered perennial herb to describe allozyme diversity at 15 presumptive loci. Genetic diversity was low for the species, within populations, and for polymorphic loci (Hes 5 0.006; Hep 5 0.005; HT 5 0.028). Three of the 15 loci (20%) were polymorphic across the species’ range, but frequencies of uncommon alleles were uniformly low (mean P 5 .05). No polymorphism was detected in seven populations. Population extinctions and decreases in population sizes, coupled with habitat fragmentation, may account for the low genetic diversity. The fugitive life-history characteristics of this shade-intolerant species presumably have also contributed to the loss of genetic diversity by predisposing the species to founder effects and population extinctions. Schwalbea americana comprises a monotypic genus in the figwort family, Scrophulariaceae. Like many members of this family, S. americana is a hemiparasite, obBrief Communications 89 Endo TR , 1990 . Gametocidal chromosomes and their induction of chromosome mutations in wheat . Japan J Genet 65 : 135 - 152 . Endo TR and Gill BS , 1984 . Somatic karyotype, heterochromatin distribution, and nature of chromosome differentiation in common wheat , Triticum aestivum L. em Thell. Chromosoma 89 : 361 - 369 . Endo TR and Gill BS , 1996 . The deletion stocks of common wheat . J Hered 87 : 295 - 307 . Endo TR and Tsunewaki K , 1975 . Sterility of common wheat with Aegilops triuncialis cytoplasm . J Hered 66 : 3 - 18 . Hyde BB , 1953 . Addition of individual Hynaldia villosa chromosomes to hexaploid wheat . Am J Botany 40 : 174 - 182 . Islam AKMR and Shepherd KW , 1992 . Alien genetic variation in wheat improvement . In: Chromosome engineering in plants: genetics, breeding, evolution (Gupta PK and Tsuchia T, eds). Amsterdam: Elsevier Science; 291 - 312 . Jiang J , Friebe B , and Gill BS , 1994a . Recent advances in alien gene transfer in wheat . Euphytica 73 : 199 - 212 . Jiang J , Morris KLD , and Gill BS , 1994b . Introgression of Elymus trachycaulus chromatin into common wheat . Chromosome Res 2 : 3 - 13 . Maan SS , 1975 . Exclusive preferential transmission of an alien chromosome in common wheat . Crop Sci 15 : 287 - 292 .


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Jiang, J, Gill, BS. Brief communication. Preferential male transmission of an alien chromosome in wheat, Journal of Heredity, 1998, 87-89, DOI: 10.1093/jhered/89.1.87