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Department of Botany and Plant Sciences, University of California, Riverside, CA 92521
* Corresponding author (giles.waines{at}ucr.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONReproductive Biology of Bread...APPENDIX 1REFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONReproductive Biology of Bread...APPENDIX 1REFERENCES |
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Introgression thus refers to "the infiltration of germplasm from one species into another through repeated backcrossing of the hybrids to the parental species" (Anderson and Hubricht, 1938; Arnold 1997). With each successive backcross the hybrid-derived plants progressively accumulate the traits of the backcrossing parent(s). The formation of fertile hybrids and backcross individuals is necessary for a successful introgression between any two taxa. Accordingly, genetic relatedness, ploidy level, and direction of hybridization between hybridizing taxa play a crucial role during the process of introgression (Rieseberg and Wendel, 1993).
A number of angiosperm taxa are believed to be derived from hybridization or introgression between closely related taxa (Clausen et al., 1945; Grant, 1981; Soltis and Soltis, 1993; Rieseberg and Carney, 1998), and even in the extant floras, the occurrence of hybridization or introgression is reported to be widespread (Knobloch, 1972; Stace, 1987; Rieseberg and Wendel, 1993; Peterson et al., 2002). For example, Knobloch (1972) identified thousands of interspecific and intergeneric natural hybridization events between species of angiosperms. Similarly, 7% of the 1264 introduced plant species to the British Isles are known to be involved in hybridization with either native species or other alien species (Stace, 1991; Abbott, 1992). A permanent transfer of genes between hybridizing taxa has been documented in 65 of 165 suggested instances of introgression (Rieseberg and Wendel, 1993). The majority of the 165 documented instances of introgression were reported for angiosperm species including dicots, monocots, and nearly all growth forms, pollination syndromes, and mating systems.
Introgression has played a role in structuring the genetic diversity of species (Wendel et al., 1989; Rieseberg, 1997), in the origin of new adaptations (Rieseberg, 1991), in the transfer of adaptations between species (Heiser, 1973; Rieseberg et al., 2003), in the formation of new ecotypes (Levin, 1967; Abbott, 1992; Rieseberg, 1997) or species (Arnold et al., 1991; Soltis and Soltis, 1999), and in the evolution of invasiveness (Anttila et al., 1998; Ellstrand and Schierenbeck, 2000).
Plant breeders artificially introgress traits from wild relatives into crop plants to develop new cultivars. Earlier, such artificial introgressions were mainly restricted to gene transfer between species that were cross compatible (Maan, 1987), as cross incompatibility problems prevented production of viable seeds among hybrids between unrelated species. However, modern biotechnology techniques, which do not depend on the sexual transfer that occurs in nature, overcome this sexual barrier by making gene transfer possible between unrelated species (Bajaj, 1990; Lörz et al., 1997). By uncoupling the process of gene exchange between species from that of sexual transfer, modern biotechniques have become the preferred method of transferring useful genes into crop cultivars from other taxa irrespective of the taxonomic relationship between donor organisms and crop plants. Although these techniques provide benefits, potential gene flow between crop plants and their wild or weedy relatives (Zohary and Feldman, 1962; Linder et al., 1998) have raised concerns regarding the negative consequences of alien genes in wild populations (Rieseberg and Wendel, 1993; Ellstrand, 2003).
In this review, we focus on three important issues concerning introgression between bread wheat and its wild relatives, especially those wild relatives with a known history of colonizing behavior in North America. First, we discuss reproductive biology and ecology of bread wheat and its wild relatives, as the potential for introgression from bread wheat to a wild relative primarily depends on the effectiveness of wheat pollen as a pollen donor (Joppa et al., 1968; Waines and Hegde, 2003). Second, since the success of wheat pollen in fertilizing a wild species depends on the degree of genetic relatedness between the two hybridizing taxa (Kimber and Feldman, 1987), we talk about the genetic mechanisms controlling intra- and intergenomic compatibility of bread wheat that influence meiosis and fertility of wheat plants and wheat hybrids. Third, we present the documented instances of introgression between bread wheat and its weedy wild relatives occurring in North America.
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Reproductive Biology of Bread Wheat |
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TOPABSTRACTINTRODUCTIONReproductive Biology of Bread...APPENDIX 1REFERENCES |
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The extrusion of anthers and the duration of flower opening are significant factors affecting cross-pollination and potential gene flow, and in wheat these two factors are affected by both genetic control and environmental influence. Sage and De Isturiz (1974) indicated that anther extrusion in wheat is under the influence of a few genes, probably two, with additive effect and low heritability. Zukov (1969) found a correlation coefficient (r) of 0.93 in hexaploid wheats between the percentage of open florets and the percentage of extruded anthers. It was shown in 10 Canadian spring wheats that cultivars with high outcrossing rates tended to have a greater degree of floret opening at anthesis (Hucl, 1996). Both genotype and environment appear to influence the number of extruded anthers. In a multiyear investigation involving different genotypes and variable environments, Rajki (1962) observed the percentage of extruded anthers varied from 61 to 93%; in the driest year the fewest anthers were extruded because of limited flower opening. In warm weather and at high atmospheric and soil humidity, anthers dehisce faster (De Vries, 1971). Environmental stress that results in a large proportion of extruded anthers would likely represent an ideal situation for gene flow to nearby wild relatives. Cultivars with a large number of open florets before anther dehiscence and/or with a longer duration of flower opening might be prone to greater gene flow than cultivars with a short anthesis period or with a large proportion of cleistogamous flowers (Waines and Hegde, 2003). Genotype and environmental (e.g., dry weather) interaction for flower opening likely results in a continuum of gene-flow effects among wheat cultivars.
Pollen Production
Within wheat cultivars there is large variation for the number of pollen grains produced per anther ranging from 856 to 3867 (Cahn, 1925; Joppa et al., 1968) depending on the anther size (Beri and Anand, 1971). Although pollen production in predominantly self-pollinating wheat plants is nearly one-tenth (450 000 pollen grains) that of rye (Secale cereale L.) (4 200 000 pollen grains), an outcrossing relative (D'Souza, 1970), potential still exists in wheat for gene flow to occur, as 30 to 80% of the pollen is shed outside the flower (D'Souza, 1970; Beri and Anand, 1971). If environmental conditions are conducive and the isolation distance is not great enough between wheat and a wheat relative, gene flow could occur if pollen from one cultivar could pollinate unfertilized flowers of a receptive plant. Under optimal field conditions (20°C, 60% relative humidity), wheat pollen retains viability for approximately 30 min (D'Souza, 1970; De Vries, 1971), a duration long enough to bring about cross-fertilization with a nearby wild relative.
Pollen Movement
Wheat pollen is relatively heavy compared with other grass pollen and as a consequence wheat pollen grains typically travel short distances (Lelley, 1966). However, long-distance pollen movement was also reported by several researchers: wheat pollen grains were detected from a source population at a distance of 20 to 24 m (Suneson and Cox, 1964; De Vries, 1971), 50-60 m (D'Souza, 1970; Khan et al., 1973), or even at 1000 m (Virmani and Edwards, 1983). For example, during a 3-yr period from 1967 to 1969 at Newton, KS, collection stations were placed at 0, 3, and every 6 m afterward up to a 60-m distant from the pollen source. The average number of pollen grains collected hourly from 0700 to 1700 h on glass rods ranged from 72 to 153 grains at 0 to 3 m distance, and 33 to 43 grains at 48 m. A small number of pollen grains were also detected at 60 m from the pollen source (Khan et al., 1973). A similar study was also performed at Pioneer Hi-Bred International, Inc. (Kansas) where researchers conducted pollen trap studies using glass slides and tested the trapped pollen grains for their viability. This pollen trap study revealed that wheat pollen (viable or nonviable) could travel as far as 1000 m from a very large source population (Virmani and Edwards, 1983). In the majority of these pollen movement studies, more than 90% of pollen grains remained within 3 m of their source, and the amount of pollen collected decreased rapidly with increasing distances from the source plant (Jensen, 1968; Khan et al., 1973; Virmani and Edwards, 1983).
Furthermore, this long-distance pollen movement did not proportionately increase gene flow, as gene flow decreased rapidly after 0.5 to 1.5 m (Khan et al., 1973; Hucl and Matus-Cádiz, 2001). In a recent investigation on gene flow in wheat, Hucl and Matus-Cádiz (2001) examined gene flow rates of four wheat cultivars. Percent gene flow was determined for distances from 30 cm to 33 m from the pollen source. Gene flow rate decreased with greater distance from the pollen source, and was dependent upon wind direction and wheat genotype. Maximum gene flow rates at 30 cm (adjacent rows) were 3.8, 2.6, 0.4, and 0.2% for the four cultivars. At 27 m, gene flow was recorded in only 2 (0.095 and 0.06%) of 32 samples (2 yr x 4 cultivars x 4 directions). This emphasizes that physical movement of pollen does not necessarily result in gene flow.
Wheat Genomes and Genetics in Regards to Hybridization and Introgression
Bread wheat is an allohexaploid with three genomes, B, A, and D [genomic formula according to Waines and Barnhart (1992)]. Each genome originated from a different species: the B genome possibly from an ancestor of Aegilops speltoides Tausch; the A genome from Triticum urartu Tum. ex Gand.; and the D genome from Aegilops tauschii Coss. (Kihara, 1944; McFadden and Sears, 1946). The genus Aegilops contributed two-thirds, being the source of B and D genomes of bread wheat. Studies of variation in isozymes (Jaaska, 1978), nuclear DNA (Dvorak and Zhang, 1990), and organelle DNA (Mori et al., 1988; Wang et al., 1997) strongly support the idea that the B genome was derived from an S-genome species of the section Sitopsis, most likely related to allogamous Ae. speltoides.
Each one of the three genomes (B, A, and D) of bread wheat is composed of 7 chromosomes, which are labeled 1B, 1A, 1D through 7B, 7A, 7D, respectively. Thus, it is possible to place the 21 different chromosomes into seven groups of three. The chromosomes of each group are termed homeologous (= similar) and they are considered to have a common evolutionary origin (Kimber and Feldman, 1987). The term homologous refers to a pair of chromosomes within a genome that have alleles for the same genes. Although the homeologous chromosomes of the B, A, and D genomes of hexaploid wheat share several structurally identical genes, pairing between these chromosomes is prevented by a gene called Ph1 or Pairing homeologous 1 (Riley and Chapman, 1958; Sears, 1976). The Ph1 locus is mapped to the chromosome 5B linkage group (Riley and Chapman, 1958; Sears and Okamoto, 1958), and Ph1 acts as a dominant gene suppressing the pairing of homeologous chromosomes while allowing regular pairing between homologous chromosomes. Consequently, only bivalents are formed at meiosis; therefore, common wheat behaves as a typical allopolyploid showing disomic inheritance. Furthermore, the Ph1 locus was also found to prevent homeologous chromosome pairing between wheat and several other related genomes in hybrids (Riley et al., 1959; Jauhar and Chibbar, 1999).
The Ph1 locus largely operates premeiotically to guarantee the association and alignment of homologous chromosomes (Feldman, 1966; Martinez et al., 2001), thus restricting synapsis and recombination to homologs rather than between homeologues. In the absence of Ph1, premeiotic alignment is presumably not restricted to homologs and can also occur between homeologues (Sears, 1977; Benavente et al., 1996), leading to the formation of one to several multivalent chromosomes (Riley, 1960; Sears, 1976) at a relatively high frequency (Riley, 1966; Benavente et al., 1998). The removal of Ph1 is necessary before homeologous chromosomes can pair; but this does not guarantee synapsis and recombination. In fact, the degree of recombination achieved between homeologous chromosomes appears more related to their evolutionary divergence—for example, recombination is less likely to occur between unrelated but paired homeologous chromosomes (Feldman, 1993).
The effect of the Ph1 gene is suppressed under a variety of genetic backgrounds, as in the case of hybrids between bread wheat and some diploid Aegilops species. Some genes from Aegilops species are found to suppress the effect of the Ph1 locus and thereby allow homeologous chromosome pairing. This suppression was first observed in hybrids of bread wheat with Ae. speltoides (Feldman and Mello-Sampayo, 1967; Dover and Riley, 1972), but has since been observed in hybrids with certain genotypes of Ae. caudata L., Ae. sharonensis Eig, Ae. longissima Schweinf. & Muschl. and perhaps all diploid Aegilops and Triticum species (van Slageren, 1994). Another distant genus, Amblyopyrum muticum (Jaub. & Spach) Eig (synonym: Ae. mutica Boiss.), also effects suppression of the Ph1 locus (Dover and Riley, 1972).
A multi-allelic series is also known for differential suppression of the Ph1 locus in most species (Dover and Riley, 1972). But, so far, it is not clearly known if genes in polyploid Aegilops relatives are also able to suppress the Ph1 locus and thereby promote homeologous chromosome pairing and introgression. However, a few recent reports (Zemetra et al., 1998; Wang et al., 2001; Lin, 2001; Morrison et al., 2002b) indicated that, probably, Ph1 suppression also occurs at the polyploid level. Lin (2001) made artificial crosses between Ae. cylindrica (as female parent; genomes CCDD) and bread wheat (genomes BBAADD) and obtained 16 to 21% hybrid seeds. Subsequently these hybrids were backcrossed (BC1) to Ae. cylindrica (as male parent) producing 2 to 2.5% BC1 seeds. The author contended that formation of a few fertile F1s in his experiments was probably because of the pairing between shared D genomes of jointed goatgrass and wheat. If such interspecific hybrids between wheat and other polyploid Aegilops can also take place in nature, this may allow recombination of wheat transgenes into weedy Aegilops species.
In addition to the Ph1 genetic system, another genetic system called Kr is involved in controlling the ability of bread wheat to cross with rye and other genera. The ability of common wheat to cross with rye is controlled by four loci located on four chromosomes; loci kr1and kr2 (Lein, 1943) located on 5B (Riley and Chapman, 1967; Falk and Kasha, 1981) and 5A (Sitch et al., 1985) respectively; locus kr3 on 5D (Krolow, 1970); and kr4 (Luo et al., 1989) on 1A (Zheng et al., 1992). These four loci do not equally contribute to the ability to cross, as their strength decreases from kr1, kr4, kr2, and kr3 in that order; in other words, the alleles providing the greatest crossing ability are shown to occur on chromosomes 5B, 1A, and 5A (Luo et al., 1989; Zheng et al., 1992).
In hexaploid wheat, the ability to cross with rye is facilitated by recessive alleles or inhibited by dominant alleles at these loci (Snape et al., 1979; Fedak and Jui, 1982). This assertion was also supported by observation that noncrossable hexaploid wheat cultivars contain only dominant Kr alleles (Zheng et al., 1992). In addition to the dominant-recessive nature of the crossing alleles, wheat-rye crossing is also affected by the genotype of wheat cultivars, as there was marked variation in the amount of outcrossing between cultivars of wheat with rye—on average most of the 1400 wheat cultivars tested for crossing with rye exhibited greatly reduced seed set. Among these wheat cultivars, those producing higher seed set in crosses with rye were native to East Asia (Deng-Cai et al., 1999). Incidentally, the most popular bread wheat cultivar in wheat genetics research, Chinese Spring, was chosen for its high ability to cross with rye (Sears and Miller, 1985) and was a descendant of a land race from Sichuan Province, China (Deng-Cai et al., 1999).
Introgression in North America
In the USA, natural hybridization has been documented between Aegilops cylindrica Host. (jointed goatgrass) and bread wheat (Mayfield, 1927; Morrison et al., 2002a,b). Although another Aegilops species, Ae. triuncialis, has significant presence in northern California and also occurs in Pennsylvania, there has been no record of hybrids forming between bread wheat and Ae. triuncialis (Watanabe and Kawahara, 1999). The two Aegilops species have not been reported as occurring in Canada (Canadian Food Inspection Agency, 2003). Rye is a distant relative of wheat and feral rye populations persist in many places in the western wheat growing areas of the USA (Sun and Corke, 1992; Pester et al., 2000). There are reports of successful artificial hybrids created between wheat and rye (Florell, 1931), but natural hybrids between these two species have not been reported in the USA. Although plant breeders and agriculture extension workers observed natural wheat x rye hybrids occurring in Canada, such reports have yet to appear in the peer-reviewed publications. Therefore, in the following section we primarily discuss the biology and ecology of jointed goatgrass as related to the documented instances of introgression in North America.
Biology of Jointed Goatgrass
Jointed goatgrass generally grows 20 to 40 cm tall. As the plant matures, it can produce up to 135 tillers. The inflorescence is a narrow cylindrical spike with six to eight spikelets. Each spikelet can have two to five florets with usually one to two and sometimes three kernels per spikelet. In terms of seed production, a jointed goatgrass plant can produce up to 100 spikes, 1500 spikelets or joints and up to 3000 kernels. However, when growing in a wheat crop, even with adequate moisture, a typical jointed goatgrass plant produces approximately 130 kernels per plant (van Slageren, 1994).
Jointed goatgrass is similar to bread wheat (in particular, the winter types) in growth habit and appearance, but differs substantially in a few morphological traits (Donald and Ogg, 1991). Jointed goatgrass tends to have a more prostrate growth habit, narrower leaves, and a more compact spike than does bread wheat. Jointed goatgrass has hairs on the leaf margins, whereas bread wheat does not. The coleoptile color in jointed goatgrass is red versus green in bread wheat (Snyder et al., 2000). The joints (spikelets) differ from wheat spikelets, looking like small pieces of stick. At maturity, the spike falls intact and the spikelets then separate with a segment of the rachis still attached.
Ecology
Jointed goatgrass is a weed of winter wheat, and it rarely infests spring wheat. Spring wheats grow in regions where the winters are too harsh for the winter varieties. The cold winter temperature, therefore, also prevents the successful establishment of jointed goatgrass. Winter wheats are planted in the fall in regions where the winters are relatively mild and dry. The grain begins to grow before the cold weather approaches and they become dormant during the winter and resume growth in the spring. Winter wheat is harvested in the summer. Physiologically, jointed goatgrass and winter bread wheat are analogous, having similar temperature optimums, maximum photosynthetic rates and growth rates, as well as other similar physiological characteristics. Thus both morphological and physiological similarities of jointed goatgrass to winter wheat make control very difficult once jointed goatgrass is introduced into a wheat field (Donald and Ogg, 1991).
Jointed goatgrass has definite weedy characteristics, which make it particularly troublesome. The kernels ripen before those of winter wheat and spikelets readily shatter from the plant. Studies indicate that jointed goatgrass readily germinates at soil temperatures of 10 to 35°C (Morrow et al., 1982). Further, some germination will occur at temperatures as low as 2°C and as high as 40°C. Jointed goatgrass can emerge from soil at depths as great as 16 cm (Cleary and Peeper, 1980); thus, plowing to bury the spikelets at depths great enough to prevent emergence has not been effective. In addition, jointed goatgrass seeds may remain viable in the soil for 3 to 5 yr after being shed. In terms of seed dormancy, the basal seeds of a spikelet have greater dormancy than the subterminal seeds exhibiting germination-polymorphism among seeds of a spike (Morrow et al., 1982). Seed dormancy has helped the species to persist in the soil and to rapidly colonize new areas.
Distribution in North America
Jointed goatgrass is a native of western Asia and eastern Europe and was introduced into the USA at the end of the 19th century (Carleton, 1915; Hitchcock, 1951). Currently it has colonized many states, from the east to west coasts, although most abundantly in the western and northwestern states and the plains of the Midwest (Donald and Ogg, 1991). At the time of last survey conducted in 1993 to document the distribution of jointed goatgrass, the infestation in U.S. winter wheat production areas was over 2 million hectares and was spreading unchecked at a rate of 20000 ha per year (National Jointed Goatgrass Research Program, 2003). It is most commonly found in winter wheat fields or other cereal grain fields, fencerows, roadsides, and waste areas. It also infests rangelands surrounding wheat growing areas and land in the conservation reserve program throughout the western USA (Westra and Davis, 1987). It disperses through spikelets (joints) and has been introduced to some areas by custom combines (Fenster and Wicks, 1976) and to others by planting contaminated wheat grain as seed (Swan, 1984).
Introgression (Bread Wheat x Jointed Goatgrass)
Jointed goatgrass is an allotetraploid (DDCC; genome formula according to Kimber and Tsunewaki, 1988) with 28 chromosomes. Each chromosome set contains 7 chromosomes and originates from two species designated by CC and DD (Kihara, 1937; Kimber and Sears 1987). One reason jointed goatgrass and wheat are so similar is that the two species share a common ancestor, Ae. tauschii, the donor of the D genome. Hexaploid wheat also contains genomes B and A from two other species. The D genomes in jointed goatgrass and bread wheat are so similar that in the hybrid the D genomes from the two species complement each other acting as a homologous pair (Kimber and Sears, 1987; Zemetra et al., 1998) while producing a few viable hybrids (Mallory-Smith et al., 1996; Morrison et al., 2002b). In an ideal situation, the pentaploid hybrids can be expected to possess 7 pairs of D genome chromosomes, and a haploid set of A (7 chromosomes), B (7 chromosomes), and C (7 chromosomes) genomes with a hybrid genome of 2n = 5x = 35, DDCAB or BADDC (depending on whether jointed goatgrass or bread wheat is the female parent). Nevertheless, in nature there may be breakdown of strict homologous chromosome pairing, and the wheat and jointed goatgrass hybrids may exhibit an array of chromosome numbers (Zemetra et al., 1998) depending on the number of promoter or suppressor genes for homeologous chromosome pairing.
A majority of plants of both species are primarily self-pollinating, but the discovery of a few natural hybrids between bread wheat and jointed goatgrass indicates that a small amount of outcrossing does occur under natural conditions both in the USA and other world areas where both the parental species co-occur (Zohary and Feldman, 1962; Hammer and Matzk, 1993; van Slageren, 1994; Mallory-Smith et al., 1996). When formed, bread wheat x jointed goatgrass hybrids are expected to be sterile because they are pentaploid (2n = 5x = 35) and hybrids lack chromosome pairing during meiosis except for the chromosomes of the D genomes. Because of the lack of meiotic pairing and subsequent unbalanced chromosome numbers in the gametes, most (>99%) of the F1 hybrids were completely sterile (Zemetra et al., 1998).
Nevertheless, a few fertile hybrid seeds were observed in the U.S. wheat fields (Mallory-Smith et al., 1996; Snyder et al., 2000; Morrison et al., 2002b) and glasshouse experiments (Zemetra et al., 1998; Wang et al., 2001). Furthermore, even seeds were obtained on subsequent backcross generations (Zemetra et al., 1998; Wang et al., 2002). For example, a backcrossing program was initiated in the glasshouse between wheat x jointed goatgrass F1 hybrids (Zemetra et al., 1998) and either jointed goatgrass or wheat was used to determine the potential for seed set and the restoration of self-fertility. Seed set occurred on the wheat x jointed goatgrass hybrids with either wheat or jointed goatgrass as the pollen parent and the frequency of seed-set (2.0 and 2.2%) was similar between the two pollen sources. Furthermore, these glasshouse seed-set data were similar to the overall frequency of seed set (2.2%) on natural hybrids observed in the field, indicating that the seed set observed in the glasshouse was not an artifact of controlled emasculation–pollination. Backcross individuals with either species as the recurrent parent exhibited a similar level of seed set (4.6– 5.1%). The level of seed set on BC2 plants differed between the two recurrent parents, with jointed goatgrass BC2 plants having three times the level of partial female fertility (37.4%) compared with wheat BC2 plants (13.7%). Although the relative female fertility level increased from 2% in the F1 hybrids to 37% in the backcross generations in glasshouse conditions, some of the techniques used in the glasshouse to achieve a higher hybrid seed production and to rescue BC1 seeds are too artificial to relate the results to the same set of plants growing under natural conditions. For example, in the glasshouse a partially emerged head of wheat, jointed goatgrass, or backcross plant was emasculated and pollinated only with one of the selected parents; however, in nature, pollen grains from different sources such as self- and cross-pollen compete to fertilize the ovules. In the glasshouse, a 5% seed set was accomplished on BC1 plants after BC1 seeds were rescued through an embryo rescue technique.
In a similar glasshouse study (Wang et al., 2001), the fertility of wheat x jointed goatgrass hybrids and backcross progenies were tested for their seed set as a measure of gene flow from wheat to jointed goatgrass. Although this study did not provide the number of hybrid seeds generated via artificial crossing in the glasshouse, the authors report 100% male sterility and 0.87% female fertility for F1 hybrid plants. When jointed goatgrass was used as the male parent to generate backcross generations, the seed-set percentages on F1, BC1, and BC2 plants were 0.9, 4.4, and 18, respectively. Furthermore, there was a dramatic increase in fertility restoration when the BC2S1 plants (56% seed set) and the subsequent generation (BC2S2; 79% seed set) plants were selfed. Such a high proportion of seed set in the backcross generations indicates that a wheat transgene with either a higher fitness or a neutral effect could spread in a jointed goatgrass population if it escaped. For example, a soft red winter wheat was mutagenized and plants resistant to an imidazolinone-class herbicide were selected from the mutagenized population (White and Morrison, 1998). The herbicide kills both bread wheat and jointed goatgrass deficient for the herbicide-resistant mutant gene. In a 1995-1996 herbicide efficacy study, jointed goatgrass pollen fertilized some imidazolinone-resistant wheat plants near Pullman, WA (Ball et al., 1999). Two herbicide-resistant hybrids were discovered in the next generation. These hybrids produced seven viable seeds in the first backcross generation between the hybrid and wheat plants. The hybrid plants were, on average, 15 cm taller and more robust than the surrounding herbicide-resistant wheat cultivar (Seefeldt et al., 1998). The subsequent glasshouse experiments showed that a few viable seeds were produced via selfing or open pollination (Snyder et al., 2000).
One interesting aspect regarding wheat and jointed goatgrass hybrid derivatives is the genes located on the D genome of wheat have a greater chance of retention in the F1 and backcross generation plants, compared with genes of the A or B genomes. In both F1 and backcross hybrids, normal bivalents are formed between the D genome chromosomes of wheat and jointed goatgrass, while the majority of chromosomes of the A and B genomes of wheat and the C genome of jointed goatgrass form univalents at meiosis-I (Zemetra et al., 1998; Wang et al., 2001, 2002). The results of this study suggest that normal bivalents could also be expected between A and B genomes of wheat and wild relatives possessing these genomes.
This indicates that, at least in theory, some genes could be transferred between wheat and jointed goatgrass, especially if those genes are located on the D genome of bread wheat. However, for genes located on the A or B genomes of bread wheat, the probability of their incorporation in the hybrids and hybrid-derived generations is substantially lower and very stochastic (Lin, 2001; Wang et al., 2002). Lin (2001) tested the transferability of genes present on different genomes (B and D) of wheat into jointed goatgrass (C and D genomes). Accordingly, the author transformed line 31 of ‘Bobwhite’ wheat with the glufosinate (herbicide)-resistant Bar gene in the B genome, and line 71 individuals of Bobwhite wheat with the glufosinate-resistant Bar gene in the D genome. Under glasshouse condition, these transformed wheat lines were used as male parents to pollinate jointed goatgrass as female parents. Three ways of pollination were performed between the parents: natural pollination on unemasculated jointed goatgrass females, natural pollination on emasculated jointed goatgrass females, and artificial pollination on emasculated jointed goatgrass females. Subsequently, the same three-way pollination method was also repeated, using fertile F1 plants as female parents and jointed goatgrass as pollen donor, to generate backcross progenies. The unemasculated and naturally pollinated spikes of jointed goatgrass did not produce any seeds. The emasculated and naturally pollinated jointed goatgrass spikes set 16 and 17% seeds with male parental lines 31 and 71, respectively; and emasculated and artificially pollinated jointed goatgrass spikes set 21 and 18% seeds with male parental lines 31 and 71, respectively. But among BC1 crosses, only the emasculated and artificially pollinated F1 plants produced some seeds. The cross (jointed goatgrass x line 31) x jointed goatgrass set 2% seeds, and the cross (jointed goatgrass x line 71) x jointed goatgrass set 2.5% seeds out of 50 pollinated spikes under each of the two crossing schemes. When the BC1 plants were tested for the presence of the glufosinate-resistant Bar genes, two-thirds of BC1 plants possessed the resistant gene from the cross [(jointed goatgrass x line 71) x jointed goatgrass] where line 71 wheat carried the resistant Bar gene on the D genome, whereas none of the BC1 plants possessed the resistant gene from the cross [(jointed goatgrass x line 31) x jointed goatgrass] where line 31 wheat carried the resistant Bar gene on the B genome. These results suggest that the transfer of transgenic genes located on the A or B genomes of wheat to other related plants is less likely via sexual hybridization.
Introgression between Bread Wheat and Rye
Natural introgression between bread wheat and rye has rarely been reported in North America (Leighty, 1915) and appears infrequent in other areas of the world (Rimpau, 1891; Dorofeeva, 1966). Nevertheless, several successful artificial crosses were performed between these two genera (Falk and Kasha, 1981). For example, Falk and Kasha (1981) and Tanner and Falk (1981) reported a high correlation between the ability of specific wheat cultivars to cross with S. cereale L.
Genetics of Wheat x Rye Hybrids
The ability of wheat and rye to cross was reported to be controlled by one (Taylor and Quisenberry, 1935) or by two recessive genes, kr1 and kr2 (Lein, 1943) in wheat. In contrast, dominant genes in S. cereale control crossing with wheat (Tanner and Falk, 1981). In addition, suppression of Ph1 locus was found to induce wheat and rye homeologous chromosomes to pair and recombine (Naranjo and Fernández-Rueda, 1996).
Wheat–rye hybrids are easier to obtain than rye–wheat hybrids (Backhouse, 1916; Leighty and Sando, 1928). Most Triticum–Secale hybrids are completely male sterile and highly female fertile. The chromosomes of Triticum species do not pair with chromosomes of Secale species, and meiosis in the F1 was highly irregular (Maan, 1987). Occasionally, fertilization involving unreduced functional gametes results in selfed seed that produces fertile amphiploid progeny (Yakubtsiner, 1952; Sadykov, 1952). Although genes from Ph and Kr loci are directly involved in the regulation of meiosis in wheat–wheat and wheat–alien hybrids they may also indirectly affect seed set in the hybrids. Therefore, it is possible that interactions between the pairing and crossing genes in wheat and rye may reduce or enhance seed set depending on the direction of hybridization.
Fertility of Interspecific and Intergeneric Wheat Hybrids
Triticum and its related genera consist of diploid and polyploid species with various genome combinations. Therefore, the extent of hybrid fertility between species of these genera is a function of ploidy and genomic compatibility between hybridizing taxa. Although many species of Triticum and related genera are cross-compatible, and hybrids between species belonging to the same as well as different genera can be produced (Knobloch, 1968, p 47–52; Maan, 1987; van Slageren, 1994), most interspecific and intergeneric hybrids involving species of Triticum are highly male sterile but partially female fertile (Maan, 1987). This female-only fertile condition may encourage introgression. Therefore, the F1 hybrids sometimes produce backcross progeny from pollination with parental or other related species (Maan, 1987). Polyploid species are more fertile acting as females than as males in crosses between diploid and polyploid species (Maan, 1987). Also, there is substantial intra- and interspecific variability in cross-compatibility among the species of Triticum and related genera. Certain species of Triticum are cross-compatible only as a male or as a female with other species of Triticum and related genera, regardless of the ploidy differences between the parental species (Kihara, 1937; Gill and Waines, 1978).
Implications of Introgression in Consideration of Current and Possible Future Development of Transgenic Wheat
Bread wheat is a major food crop of mankind in terms of the area under cultivation and megagrams of grain harvested (Braun et al., 1998). The crop is cultivated in all the continents and, in several places, bread wheat and wild relatives grow side by side (van Slageren, 1994). The fact that hybrids between wheat and jointed goatgrass are partially fertile raises the question of whether a wheat gene could be transferred to jointed goatgrass if jointed goatgrass were the recurrent parent in the backcross. This is important because one possible control strategy for jointed goatgrass is the use of genetically engineered herbicide resistant wheat. On the basis of our analysis
(see Appendix 1),
we estimated that the probability of recovering BC2 seed with jointed goatgrass as the recurrent parent would be approximately one plant out of 1.54 million plants if a transgene is present on the D genome of wheat. In reality, however, the hybridization rate in BC2 might be very much lower than what was predicted by our analysis. For example, the haploid genomes A, B, and C in the F1, each of which contains seven chromosomes, rarely segregate intact to one of the meiotic poles. Such irregular meiosis tends to produce higher numbers of sterile pollen and eggs than was predicted by our analysis
(Appendix 1).
Moreover, in the field, the frequency of successful backcross seed production could be much lower since our assumptions of 1% seed set of F1 hybrids and 5% seed set in BC1 plants are from experimental data obtained under optimum conditions in the glasshouse (Wang et al., 2001). Furthermore, the extent of backcrossing with jointed goatgrass is very limited in the field because of competition between wheat and jointed goatgrass pollen (Snyder et al., 2000) and also because of a limited number of jointed goatgrass plants in the field, as agronomic practices to control weeds eliminate many of the jointed goatgrass plants. Although partial introgression may occur in approximately one in 1.54 million plants from our probability analysis, there is no empirical evidence linking the invasiveness of species such as jointed goatgrass to their introgression with bread wheat. The recent experimental evidence only suggests that introgression is possible between jointed goatgrass and bread wheat.
One concern associated with genetically modified wheat is that when/if a transgene is introduced into a population of wild relatives, there may be an undesired ecological effect associated with the presence of the transgene, such as increased fitness or competitiveness. The perceived concern is the potential for a greater ecological risk if the transgene involved has a potential to enhance the fitness of hybrids in a weedy wild population, thereby increasing the weed potential of the receiving species. Escaped transgenes for traits like seed color and flavor, per se, may not bring any fitness advantage to the wild populations, while a drought tolerance, or an insect or herbicide resistant transgene has, under certain conditions (e.g., insect or herbicide induced selective pressure) the potential to enhance the fitness of a wild population if it escaped. But bread wheat and its wild relatives have to overcome several internal and external constraints to produce a viable hybrid or introgressed wild population in nature. In the first place, a predominantly self-pollinating bread wheat and its wild relatives coupled with their asynchronous flowering phenologies effectively prevent any large-scale pollen flow between wheat and wild populations. Besides, cross incompatibility between species, and hybrid sterility in the F1 and subsequent backcross generations, further reduce viable hybrids between wheat and wild relatives.
The discussion, so far, points to the process of introgression between bread wheat and wild relatives, in the present scenario, as a two-step process. The first, and also the most important step, is the formation of viable hybrids with a fitness equal or higher than the parents. The available data on hybrid frequency do not suggest the formation of wheat and wild wheat hybrids in any significant frequency either in the USA or in other wheat growing areas of the world when bread wheat and wild relatives occur in sympatry. Even the reported incidence of hybrids are mostly based on morphological traits; therefore, the hybrid frequency data may be an under or overestimation of the actual figure. Many natural hurdles preclude hybrid formation between wheat and wild relatives, namely, asynchronous flowering, gametic or zygotic incompatibility, reduced hybrid fitness, or hybrid sterility. For example, many wild wheats have distinctly different sets of genomes that do not pair with wheat chromosomes during gamete formation in F1 hybrids or may cause developmental instability thus reducing the ability of the hybrids to survive in the parental habitats.
Technological innovations bring their own set of benefits and risks to the environment, and no technology is 100% safe. The same is true for transgenic crop plants that contain novel traits incorporated by the tools of biotechnology and for crop cultivars produced by traditional plant breeding methods (Hegde and Ellstrand, 2002). Therefore, when considering a new product, it is important to consider the risk and benefits of the current cropping system compared with the risks and benefits of the new system. For most of the fitness enhancing traits such as disease, insect, and herbicide resistance, the potential harm to the environment is not very much different. So, some of the modern wheat cultivars with fitness enhancing traits can be used as a model system to evaluate the risk of escape of an introduced gene to wild populations. This kind of investigation will benefit both transgenic risk analysis research and the environment.
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APPENDIX 1 |
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TOPABSTRACTINTRODUCTIONReproductive Biology of Bread...APPENDIX 1REFERENCES |
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(I) Parental Cross
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(II) Backcrossing
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Potentially, all the BC1 individuals can undergo backcrossing with JGG and produce some seeds (Appendix Table A1). However, for the illustration purpose, the BC1 plant with the genome combination DDCC is the best candidate to generate fertile BC2 individuals in the subsequent round of backcrossing with JGG. The frequency of BC1 individuals with DDCC genome combination is (1/7 x 1/1100) 
1/7700. If these individuals have an average 4% female fertility (1/7700 x 4/100 = 4/770 000) with equal survival of BC1 gametes, the results will be as follows:
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If the transgenic trait is placed only on one of the two D genomes of wheat (as is the practice in transgenic corn), then such a chromosomal arrangement creates a hemizygous condition for the transgenic trait. Then there is a one-half probability of the transgene being present among F1 individuals, 1/4 among BC1 individuals, or 1/8 among BC2 individuals. Therefore, the overall probability of getting a transgenic BC2 individual from the cross [BC1 (DDCC) x JGG] is (4/770 000 x 1/8) nearly one in 1.54 million.
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ACKNOWLEDGMENTS |
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Received for publication April 30, 2003.
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TOPABSTRACTINTRODUCTIONReproductive Biology of Bread...APPENDIX 1REFERENCES |
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