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CROP PHYSIOLOGY & METABOLISM

Genetic Variation in Component Traits of Heading Date in Hordeum vulgare subsp. spontaneum Accessions Characterized in Controlled Environments

I. Karsai^a, P. M. Hayes^b,*, J. Kling^b, I. A. Matus^c, K. Mészáros^a, L. Láng^a, Z. Bed^a and K. Sato^d

^a Agricultural Research Institute of the Hungarian Academy of Sciences, Martonvásár, H-2462, Hungary
^b Dep. of Crop and Soil Science, Oregon State Univ., Corvallis, OR 97331
^c Instituto de Investigaciones Agropecuarias, INIA, CRI– Quilamapu, Casilla 426, Chillan, Chile
^d Research Institute for Bioresources, Okayama Univ., Kurashiki 710, Japan

^* Corresponding author (Patrick.M.Hayes{at}oregonstate.edu).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Ancestral germplasm may be a useful source of genetic variation for crop improvement. Genetic variation in developmental traits that contribute to heading date may be useful in developing varieties that are uniquely tailored to specific stress environments. Hordeum vulgare subsp. spontaneum (K. Koch) A. & Gr. is the ancestor of cultivated barley and useful developmental trait alleles may have been lost in the domestication process. Accordingly, we surveyed a sample of 16 subsp. spontaneum accessions for vernalization requirement, photoperiod sensitivity, photoperiod response, and relative earliness. We compared the subsp. spontaneum accessions to four H. vulgare L. subsp. vulgare accessions representing spring, facultative, and winter growth habit. Thirteen subsp. spontaneum accessions originating from the Fertile Crescent and the one subsp. spontaneum accession from the Caucasus region required vernalization; they were responsive to long photoperiods and most were very early. Two subsp. spontaneum accessions from the Himalayan region had no vernalization requirement but were extremely sensitive to short photoperiods. We used a clustering procedure to define two groups of subsp. spontaneum accessions, a group of subsp. spontaneum that included the two subsp. vulgare accessions of spring and facultative growth habit, and a fourth group comprised of the two subsp. vulgare winter habit cultivars. These data indicate that subsp. spontaneum may be a source of novel alleles for growth habit.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
IT IS WIDELY RECOGNIZED that there is limited genetic variation for many important traits in the primary gene pools of cultivated crop species (Evans, 1993). It is especially important to develop new varieties that combine resistance to abiotic and biotic stresses with high and stable yield. Ancestral species can be a vital sources of new alleles for such germplasm enhancement. Barley (H. vulgare subsp. vulgare) and its wild progenitor (H. vulgare subsp. spontaneum) provide an excellent and economically important model system for gene discovery and utilization. The two diploid subspecies are fully interfertile and an impressive set of genomics tools, including linkage maps, QTL data sets, ESTs, BAC libraries, and arrays is available for analysis of the H genome, which is homeologous with the A, B, and D genomes of hexaploid wheat (Hayes et al., 2003).

Barley is a crop of worldwide importance and it is grown in environments ranging from the deserts of the Middle East to the high elevations of the Himalayas (Hayes et al., 2003). However, most commercial barley production is concentrated between latitudes 20° and 55°, north and south (http://wbc.agr.state.mt.us/prodfacts/wf/wptbp.html[ verified 15 April 2004). This commercial production is based on a relatively narrow genetic base (Matus and Hayes, 2002), and this narrow base, in turn, can be attributed to the very specific quality demands of the malting and brewing industries. Barley breeders have, accordingly, been interested in broadening the genetic base of the crop without disrupting the genetic architecture essential for quality. Hordeum vulgare subsp. spontaneum, the ancestor of cultivated barleys has been the subject of considerable genetic analysis and "allele mining" for abiotic stress resistance traits (Pakniyat et al., 1997; Ivandic et al., 2000; Gorny, 2001), biotic stress resistance traits (Jahoor and Fischbeck, 1987; Manisterski et al., 1986), quality traits (Ellis et al., 1993; Erkilla et al., 1998), and physiological traits (Snow and Brody, 1984; Kato et al., 1998).

An essential component of gene discovery and utilization studies—be they based on analysis of segregating cross progeny or on association analysis—is a solid base of phenotypic data. This is particularly important in the case of growth habit, as the ancestral forms of the Triticeae are of "winter habit" (Kato et al., 1997; Takahashi and Yasuda, 1970; Yan et al., 2003). Winter habit is a general term describing the growth habit of a winter annual species and in the case of the Triticeae this characteristic is broadly defined as an extended period of vegetative growth before the onset of reproductive growth. The transition from vegetative to reproductive growth in winter habit cultivars can be triggered by completion of a vernalization requirement and/or growth under a photoperiod of sufficient length. In a previous study of a diverse array of barley germplasm, we found that when unvernalized, all genotypes surveyed would eventually flower. However, the heading date of some genotypes was so delayed when unvernalized as compared with vernalized (e.g., up to 141 d) that these genotypes can be said to have a vernalization requirement (Karsai et al., 2001). These genotypes would fall into Classes 4 through 6, descriptors for vernalization requirement used by the Okayama University Barley Germplasm database (http://www.shigen.nig.ac.jp/barley/Barley.html; verified 15 April 2004). There was also variation in the response of genotypes to vernalization—vernalization treatments could delay flowering, have no effect on flowering, or accelerate flowering. In this same experiment, two different responses to photoperiod duration were observed. Under short photoperiods (usually <10 h light/24 h), some genotypes would not flower, or their flowering date was significantly delayed. We use the term photoperiod sensitive to describe this phenotype. Other genotypes showed an accelerated rate of growth in response to long photoperiods (usually 12 h/24 h), and we use the term photoperiod responsive to describe this phenotype. The genetic bases of these physiological processes in barley were first studied in depth by Takahashi and Yasuda (1970), using Mendelian analysis tools, and more recently these traits have been the subject of intensive analysis with molecular tools (Pan et al., 1994; Laurie et al., 1994; Laurie et al., 1995; Karsai et al., 1997; Yan et al., 2003). A third component of growth habit has been termed earliness per se. This phenotype is defined as the difference in flowering time between varieties when vernalization and photoperiod requirements are satisfied (Laurie et al., 1995). Early flowering recessive mutants have been described (Gallagher et al., 1991, Börner et al., 2002), but their allelic relationships with vernalization, photoperiod sensitivity and response, and earliness per se genes are not known.

In the case of exploiting subsp. spontaneum, the issue of growth habit is particularly important since most of the world's production is of "spring" habit varieties where a vernalization requirement is not necessary; photoperiod sensitivity and/or response may or may not be relevant; and earliness per se genes will be key determinants of yield potential. Photoperiod sensitivity and response genes are of particular importance because in many important barley-growing regions, the winters are very mild and spring habit varieties are produced to capitalize on more favorable temperatures and precipitation patterns. Therefore, when introgressing alleles from subsp. spontaneum, information about the number and location of genes determining growth habit would be very useful to avoid undesirable changes in the recipient germplasm. Winter habit varieties have great potential in some barley growing areas and information on genes relating to winter habit could be useful in the improvement of such varieties. Finally, it could be relevant to develop facultative varieties, or varieties with novel growth habit characteristics.

In this paper, we address phenotypic diversity for vernalization requirement, photoperiod sensitivity and response, and earliness in a sample of subsp. spontaneum germplasm compared with cultivated barley accessions representing a range of growth habit. This phenotypic characterization will lay the groundwork for an ongoing extensive and detailed genetic analysis of these traits.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The vernalization requirement, photoperiod sensitivity and response, and relative earliness of 16 H. vulgare subsp. spontaneum accessions (Table 1, henceforth referred to as spontaneum) and four representative H. vulgare subsp. vulgare (henceforth referred to as cultivars) were determined in a controlled environment experiment. Thirteen of the spontaneum accessions originated from the Fertile Crescent (11 from Israel and two from Iran), two originated from the Himalayan region (one from Nepal and one from Tibet), and one was collected in the Caucasus region of the former USSR. Complete information on these accessions is posted at http://www.barleyworld.org/NABGMP/Germplasm/IvanSSR/SSRdivmain.htm; verified 15 April 2004. The criterion we have used for definition of spontaneum is that of von Bothmer et al. (1995). The two key defining attributes are a two-row inflorescence and the brittleness of the rachis. Four cultivars were used as reference standards. Strider and Kold are winter-hardy six-row feed cultivars released by the Oregon Agricultural Experiment Station (USA). In previous controlled experiments, we determined that both require vernalization and that Kold is sensitive to short photoperiod, while Strider is responsive to long photoperiods. 88Ab536 is a winter-hardy experimental line with malting quality developed by the USDA–ARS at Aberdeen, ID (USA). We previously determined that this selection does not require vernalization and that it is not sensitive to photoperiod. We have developed mapping populations from the crosses of Kold and Strider with 88Ab536, hence, the interest in thoroughly characterizing these varieties in this experiment. Harrington is a spring habit two-row malting barley released by the University of Saskatchewan (Canada). It has no vernalization requirement, it is photoperiod insensitive, and it lacks frost tolerance (Karsai et al., 2001).

Data Collection and Analysis
For each plant, we recorded the number of days to heading (developmental phase 49 on the Zadock's scale; Tottman and Makepeace, 1979). This is referred to as Dev49 in the remainder of this report. Some genotypes in some treatment combinations did not flower after 250 d of growth, at which point the experiment was terminated. These genotypes were assigned a Dev49 value of 250 d. The number of days to appearance of the first main stem node (developmental phase 31 on the Zadock's scale and referred to as Dev31 in the remainder of this report) was recorded only for vernalized plants because in the unvernalized treatments plant development was usually prolonged and accompanied by heavy tillering, which made it difficult to establish the first node appearance. The genotypic coefficient of photoperiod sensitivity at the two developmental phases was determined using the model of Roberts et al. (1988), as described by Karsai et al. (1997). Vernalization response was measured as the difference in heading date of unvernalized and vernalized plants for each photoperiod regime. Because of our interest in identifying the earliest heading genotypes at each photoperiod regime, we report relative earliness within this sample of genotypes rather than earliness per se, since this latter term refers specifically to earliness when both vernalization and photoperiod requirement of a given genotype are satisfied. The relative earliness of each genotype was calculated as the difference in heading date between each genotype and the earliest heading genotype within each photoperiod treatment. These seven values were then averaged to calculate relative earliness under all (8–24 h) daylengths (RE-all). We also calculated the relative earliness under long photoperiods (RE-long) by averaging values for the 14- to 24-h photoperiods.

Data were analyzed by MSTAT-C version 1.42 (Michigan State University; http://www.msu.edu/~freed/mstatc.htm; verified 15 April 2004), Microsoft Excel 2000 (Microsoft, Redmond, WA, USA), and SPSS11.0 for Windows (SPSS Inc., Chicago, IL, USA). We performed a cluster analysis using the developmental stage phenotypic data matrix of 20 genotypes x 21 characters (Dev31-v x seven photoperiods and Dev49-v and Dev49-uv x seven photoperiods). After a Z-score standardization of the data, we used the Ward grouping method (Everitt, 1980), as implemented in SPSS for Windows. Distances are shown on a 0-to-25 scale, where 0 represents the smallest distance and 25 represents the largest distance in the range of genotypes examined.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The ANOVAs for first node appearance (Dev31), heading date (Dev49), and relative earliness (RE) (Table 2) revealed highly significant main effects and interactions, although there is probably bias in estimation of the photoperiod main effects and interactions involving photoperiod, since photoperiod treatments were not replicated. For Dev31, the photoperiod term accounted for 76% of the total sums of squares, underscoring the importance of photoperiod duration for this phenotype. As described in the Materials and Methods section, Dev31 was measured only on vernalized plants, because of the difficulty of scoring this phenotype on genotypes that had vernalization requirements. The genotype main effect and the photoperiod x genotype term were also highly significant for Dev31, but they accounted for 13 and 11% of the total sums of squares, respectively. Dev49 and RE were measured on vernalized and unvernalized plants. For both traits, all sources of variation were highly significant. There were, however, large differences in the magnitudes of the sums of squares accounted for by main effects and interactions. For Dev49, photoperiod accounted for the greatest percentage of the sums of squares, followed by vernalization, genotype, and the photoperiod x genotype interaction. For RE, the genotype term accounted for the greatest percentage of the total sums of squares, followed by the photoperiod x genotype and vernalization x genotype interaction terms.

To further explore the role of photoperiod on Dev49, we performed separate ANOVAs on short (8–12 h) and long (14–24 h) photoperiod treatments (Table 3). The choice of 12- and 14-h treatment as the dividing line between short and long was based on the previous results with other barley genotypes (Karsai et al., 1997) and on inspection of data from the current experiment (e.g., Fig. 1) . These two ANOVAs provided an interesting and revealing perspective on the role of photoperiod duration. Under long photoperiods, where all photoperiod requirements are satisfied, vernalization requirements had to be met in order for genotypes to flower, and the vernalization term accounted for 63% of the total variation. All of the main effects and interactions were highly significant, but of much smaller magnitude. In comparison, under short photoperiods, where some genotypes do not flower or are significantly delayed in flowering, vernalization and photoperiod duration had much less effect (9 and 16%, respectively) than genotype (41.7%).

View larger version (48K): [in this window] [in a new window]   Fig. 1. a–e. Responses of the four groups of H. vulgare genotypes shown in Fig. 2 to photoperiod duration in terms of the days to first node appearance (a) heading date (b and c), and relative earliness (d and e). The number of days to first node appearance (Dev31) was measured only for vernalized treatments. The number of days to heading (Dev49) and relative earliness were measured with and without vernalization. Group means followed by the same letter are not significantly different at the 0.05 probability level.

View larger version (17K): [in this window] [in a new window]   Fig. 2. Cluster analysis based on data for three phenotypes—number of days to first node appearance (with vernalization), number of days to heading (with vernalization), and number of days to heading (without vernalization)—measured at seven photoperiod regimes (8, 10, 12, 14, 16, 18, and 14 h light/24-h period) for the 16 H. vulgare subsp. spontaneum accessions and four H. vulgare subsp. vulgare cultivars described in Table 1.

As shown in Fig. 2 , the cluster analysis identified four groups of genotypes. The groups reflect geographic origin and/or degree of domestication and therefore provide a convenient tool for identifying principal attributes of the germplasm array. There are some interesting unique characteristics of members of each group, and these will be highlighted later in this Results section and in the Discussion. The spontaneum accessions from Israel, Iran, and the Caucasus formed two groups. On average, the Group 1 and Group 2 accessions were both responsive to long days and responded to vernalization. However, the Group 2 accessions were earlier when vernalization and photoperiod requirements were met. Group 3 consists of a spring habit cultivar variety (Harrington), a facultative habit experimental germplasm (88Ab536) and the two spontaneum accessions from the Himalayan region. None of the genotypes in this group had vernalization requirements. The two cultivated forms showed little response to photoperiod duration, whereas the two spontaneum accessions were sensitive to short photoperiods. The two winter habit cultivars were quite divergent from the other germplasm. Both had vernalization requirements and were sensitive to short photoperiods.

All genotypes, when vernalized, showed a decrease in the number of days to Dev31 with increasing daylength (Fig. 1a). This decrease was most notable from photoperiods of 8 to 16 h. Beyond 16 h, the responses leveled off. At each photoperiod, there were significant differences between groups. Group 3 (consisting of the spring habit variety, the facultative variety, and the two East Asian spontaneum) was the first to reach Dev31 at 8 and 10 h photoperiods. Groups 1 and 2 (consisting of spontaneum accessions from Iran, Israel, and the Caucasus) showed very similar patterns of response. The two winter cultivars were always the last to reach this growth stage, and the differences were significant at 14-, 16-, and 24-h daylengths. The data shown in Fig. 1b and 1c may explain the shift in the importance of effects when ANOVAs for Dev49 were performed for long and short photoperiods (Table 3), as opposed to all photoperiod regimes. In both vernalized and unvernalized treatments, there was an overall pattern of accelerated growth with increasing photoperiod duration, reflecting the pattern observed for Dev31. In both vernalized and unvernalized treatments, responses leveled off after 16 h. With vernalization, there were greater responses to lengthening photoperiod, particularly in the 8- to 14-h range and there were relatively small differences between groups. On average, the spontaneum accessions in Group 2 were significantly earlier to head than any other group at all photoperiods except 8 and 10 h. The Group 4 genotypes were usually the latest to head, but the differences small and not always significant. There was an interesting effect at 8-h photoperiods: although there were large differences between Groups 3 and 4 vs. Groups 1 and 2, these differences were not significant. As shown subsequently in the section on vernalization, this is due to the very different responses to vernalization of some genotypes within Groups 2, 3, and 4 at the 8-h photoperiod.

Without vernalization, there was less of a response to photoperiod duration than with vernalization. The winter habit cultivars in Group 4, which have a vernalization requirement, were earlier to flower under long photoperiods than short photoperiods, but they were always later to head than other groups. They showed the greatest response between 8- and 16-h photoperiods and were significantly later to head than all other groups from 8 to 12 h. At 14 to 24 h, they were not significantly later than the Group 1 spontaneum, which showed little response to photoperiod duration. As in the case of Dev. 31, the Group 3 genotypes were usually first to flower, and differences were significant at photoperiods greater than 14 h. Responses at 8 h were more consistent with vernalization than without vernalization: winter cultivars were significantly later than all other types, whereas Groups 1, 2, and 3 were quite similar.

As shown in Fig. 1d and 1e, the relative earliness (RE) of the four groups was very different in vernalized and unvernalized treatments. When vernalized, the RE responses were quite similar to the Dev49 responses. The Group 2 spontaneum were earliest and the Group 4 winter cultivars were the latest. As in the case of heading date, despite large differences between group means at 8 h photoperiod, these differences were not significant. Again this is due to the variable responses to vernalization of genotypes within Groups 2, 3, and 4. When unvernalized, the RE of groups in response to photoperiod duration was similar to that for heading date without vernalization, but the lack of response of Groups 1, 2, and 3 to photoperiods >10 h was particular notable. In contrast, the two winter cultivars in Group 4 had lower RE values from photoperiods of 8 to 16 h.

Group and individual genotype coefficients of photoperiod sensitivity for Dev31 and Dev49 are shown in Fig. 3a and 3b . The higher the coefficient of photoperiod sensitivity, the more a genotype shows accelerated growth at longer photoperiods. Considering Dev31, the Group 2 spontaneum were, on average, significantly more responsive to increasing photoperiod than any of the other groups (Fig. 3a). This difference is in large part attributable to Hvs1, Hvs 5, and Hvs 6 since within the Group 1 spontaneum there were accessions as responsive as some in Group 2. Within Group 3 there was considerable variation, with the two East Asian spontaneum more responsive than the cultivars. The two winter varieties were quite different, with Strider much more responsive than Kold. Considering the coefficient of photoperiod sensitivity as it relates to Dev49 (Fig. 3b), two factors are readily apparent. First, for vernalized treatments, genotypes were uniformly more responsive to lengthening photoperiod for the period up to Dev31 than Dev31 and Dev49. Second, with the exception of the Group 3 genotypes, when this sample of germplasm was not vernalized, it was much less responsive to increasing daylength than when it was vernalized.

View larger version (73K): [in this window] [in a new window]   Fig. 3. a and b. Genotypic coefficients of photoperiod sensitivity for the 16 H. vulgare subsp. spontaneum accessions and four H. vulgare subsp. vulgare cultivars described in Table 1. The group designations correspond to those in Fig. 2. Panel a shows the genotypic coefficients of photoperiod sensitivity for days to first node appearance (Dev31) and panel b shows the genotypic coefficients of photoperiod sensitivity for heading date (Dev49). Group means followed by the same letter are not significantly different at the 0.05 probability level.

Vernalization was a significant source of variation in all the ANOVAs, and accounted for 63% of the variation under long (14–24 h) photoperiods. Positive vernalization response values mean the genotype headed earlier when vernalized than when not vernalized, and the larger the value the greater the difference. A negative value means a genotype headed later when vernalized than when not vernalized. Considering group means, as photoperiod increased, vernalization had an increasingly important effect on accelerating heading date. If heading was prevented or significantly delayed, by short photoperiod, the impact of vernalization was negligible. However, once a permissive photoperiod was reached, the vernalization requirement (if extant) needed to be met in order for a genotype to flower. This is apparent in Fig. 4a , where there is an overall trend toward more vernalization response at longer photoperiods, but there are important differences between groups. The Group 3 genotypes were actually delayed by vernalization at photoperiods 12 h, and at photoperiods 14 h, they showed very modest responses to vernalization. At all photoperiods, their vernalization responses were significantly lower than any of the other groups. The Group 1, 2, and 4 genotypes, in contrast, showed a marked increase in vernalization response from 8 to 12 h, and then responses leveled off. Responses among these three groups were quite similar, although the Group 2 spontaneum were significantly different from the group 1 and 4 genotypes at 18- to 24-h photoperiods.

View larger version (48K): [in this window] [in a new window]   Fig. 4. Vernalization responses (the difference in number of days necessary to reach Dev49 between unvernalized and vernalized treatments) for the 16 H. vulgare subsp. spontaneum accessions and four H. vulgare subsp. vulgare cultivars listed in Table 1 and grouped in Fig. 2. Panel a shows the average vernalization response of the four groups at each photoperiod regime. Group means followed by the same letter are not significantly different at the 0.05 probability level. Panel b shows the vernalization responses of each genotype at long (18 h) and short (8 h) photoperiod regimes.

We used relative earliness (RE)—the difference in heading date between each genotype and the earliest heading genotype for each photoperiod treatment—rather than earliness per se (the difference between genotypes when vernalization and photoperiod requirements are met). The higher the RE value, the later the genotype. Considering first the unvernalized treatments and all photoperiods (Fig. 5a) , Groups 2 and 3 were significantly earlier than Groups 1 and 4. However, two of the Group 2 genotypes (Hvs1 and Hvs5) were as late, or later, than any Group 1 accessions. Under long photoperiods, the Group 3 genotypes were significantly earlier than any other group and the Group 4 varieties were significantly later. As shown in Fig. 5b, all genotypes except those in Group 3 were much earlier when vernalized than when unvernalized and the Group 1 and 2 spontaneum accessions were significantly earlier under all and long photoperiods.

View larger version (51K): [in this window] [in a new window]   Fig. 5. Relative earliness values for the 16 H. vulgare subsp. spontaneum accessions and four H. vulgare subsp. vulgare cultivars listed in Table 1 and grouped in Fig. 2. Panel a shows the relative earliness measured without vernalization, panel b with vernalization. Group means followed by the same letter are not significantly different at the 0.05 probability level.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

Although the vernalization response of the accessions in Group 1 was always greater than the response of the accessions in Group 2, the differences were significant only at the 18- and 24-h photoperiods. Photoperiods of such duration never occur in the natural habitats. All of the spontaneum accessions were photoperiod responsive and their developmental rates were accelerated under long photoperiods, especially the time necessary to reach Dev31. This photoperiod responsiveness is of particular interest because shorter photoperiods and modest winter–summer changes in photoperiod duration are characteristics of the Middle Eastern and Himalayan regions where these accessions originated. Between the latitudes of 30 and 35 degrees, the minimum and maximum photoperiods are approximately 9 and 13 h, whereas in the principal barley growing regions of the Northern Hemisphere, the two extremes are approximately between 8 to 16 h. In both wheat (Triticum aestivum L.) and barley, photoperiod reaction genes are located on the group 2 chromosomes (Scarth and Law, 1983; Worland, 1996; Laurie et al., 1994; Karsai et al., 1997). In the case of the vernalization responsive spontaneum accessions and cultivars, photoperiod sensitivity was expressed only when the vernalization requirements were fulfilled. This underscores that photoperiod sensitivity complements, but does not substitute for, vernalization.

It is notable, and perhaps of agronomic importance, that over 75% of the spontaneum accessions with vernalization requirements and photoperiod sensitivity had rapid developmental rates, resulting in early flowering over the range of the photoperiods. Four accessions—Hvs6, Hvs7, Hvs8 and Hvs15—were among the earliest to flower at all photoperiods, and this earliness was most pronounced at shorter photoperiods. The genetic basis of this earliness is not known. The spontaneum may have alternative alleles at the earliness per se (eps) loci described by Laurie et al. (1995), at the ea loci, or at un-described loci. In the case of the eps loci, alleles resulting in earlier heading were found both in spring and in winter germplasm (Laurie et al., 1995). Recessive allelic variants at ea loci leading to early heading under short photoperiods have been identified in spring barley (Gallagher et al., 1991; Börner et al., 2002) but there are no reports in winter habit germplasm. Approximately half of the earlier heading spontaneum accessions were early regardless of photoperiod length. All the early flowering types were responsive to vernalization, whereas the two Himalayan accessions had no vernalization requirement and were sensitive to short photoperiods.

Genetic diversity studies using molecular markers have found that winter cultivars are more genetically similar to spontaneum than spring habit cultivars (Matus and Hayes, 2002; Pillen et al., 2000; Dávila et al., 1999). These same spontaneum accessions and cultivars were part of a comprehensive germplasm diversity study using simple sequence repeat (SSR) markers (Matus and Hayes, 2002). There was a high degree of SSR allele diversity among and between these 16 spontaneum accessions and they were all very distinct from cultivated barley. Although the groupings of spontaneum accessions based on SSR allele size usually reflected geographic origin, the accessions from Iran, Tibet, Nepal, and one of the accessions from Israel (Hvs15) were all placed in the same cluster and we have found that these accessions show very different habit. The differences may be a consequence of the relatively limited number of molecular markers used for characterizing genetic diversity and low marker density in regions of the genome where genes determining growth habit are located. These differences, however, could also be due to a high degree of genetic similarity in most of the genome, with only a few, but key, allele differences at growth habit determining loci. In any event, these differences highlight the need to characterize germplasm for phenotypic traits of interest, as well as for diversity at phenotypically neutral molecular marker loci.

In summary, we found significant phenotypic variation for developmental traits—vernalization requirement, photoperiod sensitivity, and relative earliness—in a sample of spontaneum accessions. Variation was observed between accessions from the Fertile Crescent, but much of this variation was observed at photoperiod durations uncharacteristic of the region. The transition from vegetative to reproductive growth is of key importance to a wild winter annual species. It is reasonable to expect that there would be little allelic variation at loci determining this transition, since genotypes that were too early would be subject to unfavorable conditions at anthesis and would thus have reduced reproductive fitness. Likewise, individuals that were late to flower would be subjected to moisture stress and would thus therefore also have reduced reproductive fitness. It is interesting that a "redundant" control mechanism involving both vernalization and photoperiod is operational in the Fertile Crescent germplasm. This system ensures that even if the vernalization requirement is met (e.g., winter temperatures can be quite variable), photoperiod sensitivity will ensure that the genotype does not flower until a specified daylength requirement is met (e.g., daylength is invariable at a given latitude). Other genes determining developmental rates would then ensure the genotype would proceed as quickly as possible from stem elongation to anthesis and seed production. A different set of environmental conditions prevails in the Himalayan region. Domestication, selection, and breeding have led to different combinations of growth habit phenotypes than are found in ancestral germplasm. The power of long distance germplasm exchange to create novel variation is apparent. An understanding of the genetic basis of growth habit differences will allow us to determine if there are novel alleles in spontaneum accessions that are useful to agriculture. Manipulation of vernalization, photoperiod, and earliness per se genes will be necessary and important as we are faced with climate change and production in stress and degraded environments.

Received for publication July 30, 2003.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

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