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Department of Agronomy, Iowa State University, Ames, IA 50011 USA
brummer{at}iastate.edu
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ABSTRACT |
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, the genetic relationship between the traits has been poorly documented. This study was conducted to rigorously characterize this relationship in a segregating population. We developed an F1 population of 200 plants derived from crossing an elite subsp. sativa clone, ABI408, and a semi-improved subsp. falcata clone, WISFAL-6. We clonally propagated the parents and progeny and planted replicated trials at Ames and Nashua, IA in 1998. Plant height, a measure of fall dormancy, was measured in October 1998 at both locations. Winter injury was rated in April 1999. Transgressive segregation in both directions was noted in all cases, except for plant height at Ames, where no F1 genotype was shorter than WISFAL-6. The heritability of fall growth was estimated at 0.69 ± 0.044 on an entry mean basis and 0.29 ± 0.035 on a plot basis, and of winter injury at 0.73 ± 0.039 and 0.39 ± 0.040, respectively. Phenotypic correlations between the traits based on entry means were not evident (P < 0.05) but were weakly negative based on plot data (-0.11 at both Ames and Nashua, P < 0.01). The genetic correlation between fall height and winter injury was -0.16 ± 0.048. A weak association exists in this population—taller plants in the fall have less winter injury. These results provide compelling evidence that considerable improvement in both fall growth and winter hardiness can be achieved simultaneously. We suggest that the varied pathways controlling winter hardiness provide ample opportunity for selection of agronomically desirable genotypes.
Abbreviations: SCA, specific combining ability • TNC, total nonstructural carbohydrates
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INTRODUCTION |
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TOPNOTESABSTRACTINTRODUCTIONMaterials and methodsResults and discussionREFERENCES |
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Whether or not acclimation for the onset of winter could be accomplished without reducing growth is unclear. Recent results in Arabidopsis suggest that plants can possess constitutive cold tolerance, allowing them to survive low temperatures without any prior acclimation (Xin and Browse, 1998). The literature on cold tolerance among a variety of crop plants suggests that the avenues to cold or winter hardiness are many and highly diverse (Guy, 1990; Warren, 1998). This complexity suggests that modifying the fall dormancy response in alfalfa may be achievable without simultaneous losses of winter hardiness.
Phenotypic correlations reported between autumn growth and winter injury or survival suggest that concurrent selection for substantial autumn growth and limited winter injury will be unsuccessful. High positive phenotypic correlations (r > 0.90) between autumn growth and winter injury have been found in studies that compare germplasm differing in autumn growth potential (Blinn, 1911; Peltier and Tysdal, 1931; Smith, 1961; Larson and Smith, 1963; Stout and Hall, 1989; Schwab et al., 1996). Moderate phenotypic correlations
have been found among segregating progeny from parents differing widely in autumn growth and cold and winter hardiness (Daday and Greenham, 1960; Kohel and Davis, 1960; Daday, 1964; Perry et al., 1987).
Different results have been found when examining crosses between parents differing moderately in autumn growth and winter hardiness. Among F2 progeny from crosses of `Vernal' (dormant) x `DuPuits' (moderately dormant), Busbice and Wilsie (1965) found either no association or positive correlations of autumn growth with spring recovery and total yield—that is, more autumn growth correlated with better spring recovery and higher total yield in the succeeding year. Similarly, Daday (1964) crossed DuPuits to either `African' or `Hairy Peruvian' (both nondormant) and found no phenotypic correlation of autumn dry matter yield with cold hardiness in the F1 or F2 progeny
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Genetic correlations have been computed in only three cases. Perry et al. (1987) estimated genetic correlations of 0.91 to 1.20 between specific conductance and autumn plant height based on progeny derived from parents ranging from very dormant to very nondormant. In a dormant x nondormant cross, Daday and Greenham (1960) found similar results for autumn dry matter yield and cold tolerance. However, in a more restricted set of germplasm, Daday (1964) found no genetic correlation of yield and cold tolerance.
Two experiments in which plants were divergently selected based solely on autumn height have been conducted (Smith, 1961; Cunningham et al., 1998). In Vernal (Smith, 1961) and CUF101 (Cunningham et al., 1998), winter hardiness declined in the taller populations and improved in the shorter populations. Selection in the moderately dormant cultivar Lahontan was effective at changing height but did not affect winter hardiness (Cunningham et al., 1998).
Our objectives were to study the relationship between plant height measured in the autumn and winter injury and to attempt to reconcile existing data on winter hardiness and fall dormancy.
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Materials and methods |
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TOPNOTESABSTRACTINTRODUCTIONMaterials and methodsResults and discussionREFERENCES |
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15 h and 9 h, respectively. For key dates in this study, the photoperiod was 13 h on 19 August, 12 h on 16 Sept., and 11 h on 16 Oct.
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 | (1) |
2g, 2gl, and 2e represent variance components due to genotype, genotype x location, and experimental error, respectively; l is the number of locations
; and r is the number of replications per location
. For heritabilities on a plot basis, 2gl and 2e were not divided by the number of locations or replications by locations, respectively. Standard errors of the heritability estimates were calculated using the delta method (Holland and Cervantes-Martinez, 1999, unpublished data). To estimate the genetic correlation between autumn growth and winter injury, the complete data set was analyzed, considering entries as fixed effects, to generate least square means for genotypes at each location. The means for autumn height and winter injury of the 200 F1 progeny were used to compute the variances and covariances using the MANOVA statement in PROC GLM (SAS Institute, 1990). The genetic correlation and its standard error were computed based on formulae in Falconer and Mackay (1996). The significance of all results was considered to be at the 0.05 level.
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Results and discussion |
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TOPNOTESABSTRACTINTRODUCTIONMaterials and methodsResults and discussionREFERENCES |
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Our results with this population are broadly congruent with those of Busbice and Wilsie (1965) and Daday (1964), both of whom identified genotypes that combined autumn growth with winter survival or cold tolerance. Busbice and Wilsie (1965) could not calculate a genetic correlation, but their phenotypic associations were similar to ours and their observation that taller plants in the autumn tended to have less winter damage is reflected by our genetic correlation. On an entry mean basis, Daday (1964) calculated the heritability of cold injury as 0.78 to 0.80, and as 0.38 to 0.51 on a plot basis (plots of 10 plants). In the F1 generations he analyzed, phenotypic correlations were -0.069 to -0.190 and genetic correlations -0.032 to -0.084; his correlations in the F2 generation were similar. Even though Daday's (1964) results were confounded by genotype x environment interaction—he only tested one environment—and were assessed in a moderately dormant x nondormant population, his results are strikingly similar to ours (Table 2). Daday (1964) reasoned that not only would response to selection for cold tolerance and growth under cool temperatures be rapid, but that selection for both characters simultaneously would be possible. Our data concur with his assessment.
In previous studies, late summer and autumn growth was shown to be predominantly under additive genetic control (Kohel and Davis, 1960; Daday, 1964; Knipe and Stockton, 1977; Perry et al., 1987), although partial dominance was suggested by one cross (Knipe and Stockton, 1977). Our F1 population mean was similar to WISFAL-6 at Nashua, but similar to ABI408 at Ames. The differential reaction could be due to environmental effects or to phenological effects since a longer interval between cutting and the height measurement occurred at Ames than at Nashua. Cold susceptibility was partially dominant to winter hardiness, as measured by electrical conductivity (Kohel and Davis, 1960; Perry et al., 1987). Daday and Greenham (1960) found cold tolerance to be under additive genetic control. Our data suggest additivity as well, because the F1 population mean did not differ from either parent and significant transgressive segregation was seen both above the high parent and below the low parent at both locations. Estimates of combining ability for autumn growth or winter hardiness have shown general combining ability to be more important than specific combining ability (SCA) in all cases (Daday and Greenham, 1960; Theurer and Elling, 1963; Perry et al., 1987), although SCA effects were significant for cold susceptibility (Perry et al., 1987) and winter hardiness (Theurer and Elling, 1963). Based on the putative genetic control of these traits, our broad-sense heritability estimates may be quite close to narrow-sense values, although more research is needed.
Two phenomena may have interfered with accurate results in our study. First, the late summer harvest at Ames was made on 19 Aug. 1998. This date was earlier than desirable for autumn growth determination according to the alfalfa standard test (Barnes et al., 1995), but because the Ames and Nashua height data were highly correlated
, we do not feel the early harvest produced spurious results. Similarly, the data on winter injury were measured 2 wk weeks apart at the two locations, but the correlation between Ames and Nashua was 0.57 (P < 0.0001). Thus, we are confident that our data represent the true autumn growth and winter injury capacities of these genotypes.
Second, we conducted this test on spaced-planted, rooted vegetative cuttings. Brouwer et al. (1998) showed that cuttings and seedlings gave similar results for winter survival ratings, and Theurer and Elling (1963) found that spaced plantings gave winter survival rankings similar to drilled plots. Viands and Teuber (1985) reported that direct seeding or transplanting produced similar results for fall dormancy. Though rooted clonal cuttings are not identical to transplants derived from seed, both produce a different root system than direct seedings, characterized by more, larger lateral roots and a less dominant taproot. Our results should be broadly applicable to most breeding applications as well as to commercial production environments.
Model for Dormancy x Winter Hardiness Interactions
Despite the importance of both late-season forage production and winter survival, surprisingly little research has been conducted on the genetics of the traits. Synthesizing the extant research results into a consistent hypothesis regarding the genetic regulation of these traits in alfalfa poses several problems. First, few studies have been conducted in more than a single environment, limiting the inferences that can be drawn from them. None of the studies reporting genetic correlations between the traits was conducted in multiple environments. Second, most studies have examined populations, with little attempt to evaluate the performance of single genotypes. To our knowledge, no examination of these traits on a clonally replicated population has been conducted previously. Third, different germplasm has been evaluated in each experiment. Fourth, a diverse array of parameters relating to autumn growth and fall dormancy and winter hardiness have been measured. Below we develop a tentative hypothesis to explain both our results and those of previous studies, interpreted in light of the extensive molecular genetic information that has become available recently.
Fall dormancy reflects the acclimation response of alfalfa to both shortening photoperiods and falling temperatures (McKenzie et al., 1988). Acclimation of plant tissues prior to exposure to freezing conditions greatly improves survival (Guy, 1990). Even constitutively freezing-tolerant Arabidopsis mutants are better able to survive temperatures below -8°C if acclimated prior to exposure (Xin and Browse, 1998). Acclimation for winter is likely to occur in the following temporal sequence: (i) perception of environmental cues signaling the impending arrival of cold temperatures; (ii) signal transduction into a biochemical response; (iii) induction of appropriate genes; and (iv) development of freezing tolerance (Dhindsa et al., 1998).
Winter hardiness is controlled by diverse biochemical pathways (Guy, 1990; Castonguay et al., 1998; Thomashow, 1998; Warren, 1998; Xin and Browse, 1998). Genes (or their products) that are preferentially expressed during exposure to cold temperatures (2–6°C) have been isolated in a variety of species, including alfalfa, wheat (Triticum spp.), barley (Hordeum spp.), spinach (Spinacea spp.), Brassica, and Arabidopsis (Thomashow, 1998). The gene products fall into several classes: (i) proteins that are also induced by drought stress or abscisic acid, including the Cold Regulated (COR) family (Thomashow, 1998) and the Late Embryogenesis Abundant (LEA)/dehydrin family (Campbell and Close, 1997); (ii) proteins whose expression is regulated solely, or primarily, by cold temperature (Houde et al., 1992; Nordin et al., 1993); (iii) signal-transduction and regulatory proteins (Jonak et al., 1996; Ishitani et al., 1998); (iv) cryoprotecting proteins (Sieg et al., 1996); and (v) antifreeze proteins (Griffith et al., 1997; Worrall et al., 1998). Additionally, mutants that constitutively accumulate the osmoticum proline have been identified, although the genes and proteins have not been isolated (Xin and Browse, 1998). The variety of proteins identified suggests that they are involved with different components of winter hardiness (e.g., dehydrins with dessication tolerance and cryoprotecting proteins with tolerance to freeze–thaw cycles) (Thomashow, 1998).
In the past, several possible reasons for the association of winter hardiness and fall dormancy have been proposed: pleiotropy, genetic linkage, and natural selection-induced gametic phase disequilibrium among populations (Daday, 1964). The question appears not to be whether the acclimation process (i.e., fall dormancy) is distinct from winter hardiness, but rather to what extent the acclimation process can be altered without diminishing winter hardiness. We contend the discussion needs to be refocused to the different mechanisms of acclimation, on such questions as the relationship between photoperiod and temperature induction of dormancy and the particular pathways induced at specific times. The key questions regarding the manipulation of alfalfa winter hardiness are: How early in the autumn does acclimation need to begin, and how fast can it occur once initiated, to still provide adequate winter survival? How is the slowing and, ultimately, the cessation of shoot and leaf growth related to acclimation for winter?
We suggest that two types of genes are operative: (i) major genes that determine whether or not a significant acclimation response will be activated, and (ii) minor genes that modulate the level of winter hardiness by altering the timing and mechanisms of acclimation. Under this model, nondormant plants would have alleles at the major loci preventing the triggering of the various pathways leading to winter hardiness. By contrast, very dormant plants would initiate all pathways involved in winter hardiness and begin their development well before autumn. Natural selection would have resulted in extreme contrasts in alleles between northern and southern alfalfa populations (Daday, 1964). We suggest allelic rather than genic differences among genotypes because the genome organization and copy number of the cold-acclimation genes studied thus far in cereals do not appear to be related to genotypic differences in cold hardiness (Houde et al., 1992; Chauvin et al., 1993; Ouellet et al., 1993).
The acclimation process in the late summer and autumn undoubtedly diverts fixed C away from shoot and leaf growth and into the various compounds involved in survival. Nondormant genotypes may not survive well because their acclimation response is not activated; they continue autumn growth and do not accumulate sufficient winter hardiness–related compounds in their roots and crown. An analogy to concurrently improving winter hardiness and autumn growth is suggested by research on alfalfa grazing tolerance. Maintenance of root total nonstructural carbohydrates (TNC) is critical for grazing tolerance in alfalfa, and grazing tolerant plants can maintain higher TNC levels during defoliation than grazing intolerant plants (Brummer and Bouton, 1992). Alfalfa cultivars with both grazing tolerance and high yield, `Alfagraze' for example (Bouton et al., 1991), not only maintain high TNC levels under defoliation, but also accumulate higher levels of TNC than low-yielding grazing tolerant cultivars (Brummer and Bouton, 1992). In the case of winter hardiness, some genotypes may be able to partition their fixed C in a more agronomically desirable manner by maintaining an acceptable growth rate while still developing adequate cold protection. Apparently, this is what some constitutively cold tolerant Arabidopsis mutants are doing (Xin and Browse, 1998).
In crosses between dormant and nondormant genotypes, alleles at major genes will be segregating in the progeny, resulting in both nonacclimating plants that can maintain high growth rates and acclimating plants that will necessarily show some growth reduction. This is concordant with the results of Perry et al. (1987) and Daday and Greenham (1960), who showed a strong positive genetic relationship between autumn growth and winter injury. Similarly, cultivar evaluations that have included germplasm covering the full range of fall dormancy have invariably shown high, positive phenotypic and genotypic correlations between autumn growth and winter injury (Schwab et al., 1996).
By contrast, studies in which a truncated set of genotypes were evaluated, that is, dormant through moderately dormant or moderately dormant through nondormant, show a marked difference. In many cases, both phenotypic and genotypic correlations are low or not different from zero (Kohel and Davis, 1960; Daday, 1964; Busbice and Wilsie, 1965). In narrow crosses, such as ours and those of Busbice and Wilsie (1965), all plants will be acclimating, but now variation among genotypes for timing, duration, and level of expression of the response can be evaluated. Thus, different acclimation responses will result in altered winter hardiness profiles, and the relationship between autumn growth and winter hardiness will be more obscure.
Two additional results support a limited relationship between the traits across a restricted range of dormancy groups. First, Schwab et al. (1996) considered 251 alfalfa cultivars in arriving at a phenotypic correlation (r) of 0.95 between autumn growth and winter injury. We restricted their data set to 169 cultivars planted in the north-central USA (i.e., fall dormancy classes 2 to 4) and computed a new correlation. The correlation of the traits in this group is 0.45, still significant (P < 0.01), but only one-half that reported for all cultivars. Second, an alfalfa variety trial that we had planted at the Northeast Research Farm near Nashua, IA in 1995 suffered severe winterkill during the 1996-1997 winter (Brummer and Crim, 1997). We correlated the survival of the 25 entries with the fall dormancy ratings provided by the breeder of each cultivar
. Because most of these cultivars were recent releases, this weak correlation suggests that newer cultivars may break the connection between the traits.
While some individuals in our population possessed both autumn growth and winter survival to the extent possible in this cross, further improvements in autumn growth will require subsequent crosses to more nondormant germplasm. A breeding program to sequentially ratchet these traits to desirable levels may be needed, whereby adequate winter hardiness is integrated in stages with improved autumn growth. The breeding goal is to delay the onset of acclimation until absolutely necessary, perhaps at the time of a first frost, rather than weeks before. To do this, evaluation of individual genotypes must be practiced, and clonal replication or some form of progeny testing may be necessary to avoid environmental noise, as suggested by our heritability estimates. We could not calculate a heritability estimate on a single-plant basis (the way most alfalfa breeding is conducted), but the decrease in heritability from replicated trials at two locations to single plots of five clones strongly intimates further reduction on a single-plant basis, which will result in very weak heritabilities for these traits.
In conclusion, data on the relationship of winter hardiness and fall dormancy need to be interpreted in light of the germplasm evaluated and in terms of the correlations discussed. Studies considering the relationship of the variables in progenies of crosses can provide genetic information that phenotypic correlations do not, particularly when the latter are calculated for a broad range of germplasm that was not selected specifically for dissociation of the traits. Concurrent selection for both winter hardiness and greater autumn biomass production should be possible. Given the weak link between these traits, assigning winter hardiness values to populations on the basis of autumn plant height may produce an inaccurate picture of survivability, especially if they had been selected specifically for taller growth and winter hardiness. Therefore, autumn plant height should not be used to classify cultivars for winter hardiness.
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ACKNOWLEDGMENTS |
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NOTES |
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TOPNOTESABSTRACTINTRODUCTIONMaterials and methodsResults and discussionREFERENCES |
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Received for publication August 4, 1999.
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TOPNOTESABSTRACTINTRODUCTIONMaterials and methodsResults and discussionREFERENCES |
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