The Journal of Heredity 2001:92(1)
© 2001 The American Genetic Association 92:86-89
Brief Communication |
Parental Effects in the Inheritance of Nonnodulation in Peanut
From the Agronomy Department, P.O. Box 110300, University of Florida, Gainesville, FL 32611-0300 (Gallo- Meagher), IITA, PMB 5320, Ibadan, Nigeria (Dashiell), and Agricultural Research and Education Center, University of Florida, Marianna, FL 32446 (Gorbet).
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Abstract |
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A nonnodulating line (M4-2) and three normal nodulating lines (UF 487A, PI 262090, and Florunner) of peanut (Arachis hypogaea L.) were crossed in full diallel to investigate the inheritance of nodulation. Data from F1, F2, F3, F1BC1, and F2BC1 generations indicated that three genes control nodulation at three independent loci, with nodulation being a product of two genes and inhibited by a third gene when it is dominant and the others are homozygous recessive. A genetic model has been proposed that describes the nonnodulated genotypes as n1n1n2n2N3N3 or n1n1n2n2N3n3 and all other genotypes as normally nodulated except n1n1N2n2N3-, which has reduced nodulation when the n1n2N3 male gamete unites with the n1N2_ female gamete or when the n1n2n3 male gamete unites with the n1N2N3 female gamete.
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionReferences |
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Most legumes, when infected by the appropriate Rhizobium strains, form root nodules that are capable of N2 fixation. However, nonnodulation mutants derived either spontaneously or through mutagenesis have been reported from eight species that normally nodulate. A single recessive gene, rj1, controls nonnodulation in a spontaneously derived soybean (Glycine max L. Merr.) mutant (Williams and Lynch 1954) and two ethyl methanesulphonate (EMS)-induced soybean mutants (Mathews et al. 1989). However, a third EMS-derived soybean mutant is controlled by another single recessive gene different from rj1 (Mathews et al. 1989). In wild pea (Pisum spp.), a homozygous recessive sym-2 gene controls nonnodulation (Holl 1975), and in an EMS-induced pea mutant nonnodulation is conditioned by sym-5 (Kneen and LaRue 1984). In common bean (Phaseolus vulgaris L.), a single recessive gene, nnd-2, controlled nonnodulation in an EMS-derived mutant (Park and Buttery 1994). In nonnodulating mutants of sweetclover (Melilotus alba Desr.), a single recessive gene is responsible for the trait; however, allelism tests demonstrated that at least five different genes, sym-1, sym-2, sym-3, sym-4, and sym-5, are involved in nodulation (Miller et al. 1991). In three chickpea (Cicer spp) mutants derived by ;gg radiation, nonnodulation is controlled by different single recessive genes, rn1, rn2, and rn3 (Davis et al. 1986). Later, spontaneous nonnodulating chickpea mutants were identified that also were controlled by different single recessive genes (Singh et al. 1992; Singh and Ruplea 1998). Nonnodulation in red clover (Trifolium pratense L.) is controlled by a recessive gene, r, which is affected by a cytoplasmic factor and the presence of zygotic and postzygotic lethals (Nutman 1949). In a spontaneous mutant of alfalfa (Medicago sativa L.), nonnodulation is controlled by two tetrasomically inherited recessive genes, nn1 and nn2 (Peterson and Barnes 1981).
Gorbet and Burton (1979) were the first to describe a nonnodulating peanut (Arachis hypogaea L.), which originally was identified in the F3 generation from the hybridization of UF 487A, a University of Florida breeding line, with PI 262090. Nigam et al. (1980) also identified nonnodulating peanut plants from the cross PI 259747 with NC 17 and NC Ac 2731. They reported that two independent duplicate genes control nodulation, with nonnodulated plants reported as homozygous recessive at both loci (n1n1n2n2) (Nigam et al. 1982). However, Dutta and Reddy (1988) proposed a three-gene model where two genes produce nodulation and a third gene inhibits nodulation when it is dominant and the other genes are homozygous recessive (n1n1n2n2N3-). In addition, Essomba et al. (1991), in studies of the inheritance of stem color and nonnodulation in peanut, also reported that nonnodulation may be inherited by three independent genes. However, in that study the three genes showed additive effects, and nonnodulation was conditioned by any two of the three genes being in a homozygous recessive state. In their model, plants with an n1n1n2n2n3n3 genotype would be nonnodulating, whereas in the Dutta and Reddy (1988) model that genotype would be nodulated. Therefore the inheritance of nonnodulation in peanut remains unclear.
The objective of this study was to examine the inheritance of nonnodulation in peanut using the nonnodulating peanut line, M4-2, selected from the original nonnodulating germplasm described earlier (Gorbet and Burton 1979). Our results support the three locus model of Dutta and Reddy (1988). However, crosses with n1N2_ female gametes fertilized by n1n2N3 pollen or n1N2N3 female gametes fertilized by n1n2n3 pollen resulted in reduced or nonnodulation, whereas the reciprocal crosses produced normal nodulation.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionReferences |
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Three normal nodulating lines, UF 487A (University of Florida line), PI 262090 (Robore, Bolivia), and Florunner (cultivar unrelated to the above peanuts), and a nonnodulating line, M4-2, derived from the cross UF 487A x PI 262090, were used as parents in a diallel cross. F1 plants were backcrossed to M4-2 or PI 262090. The F1, F2, F3, F1BC1, and F2BC1 generations were field grown at the University of Florida Agricultural Research and Education Center at Marianna, Florida. Recommended agronomic practices were utilized, including inoculation of seed at planting with cowpea-type Rhizobium sp.
Leaf color ratings of individual plants were taken from a representative leaf from each plant just prior to digging. Each plant was tagged so that foliage color could be compared with nodule characteristics. Plants were dug using a conventional peanut digger-inverter, cutting roots 20–25 cm below the soil surface. Immediately after digging, nodulation of roots of individual plants were rated according to size and number as nodulated (equivalent to the number and size of nodules found in Florunner), few (less than 50 nodules whose diameters were almost twice the size of Florunner nodules), and nonnodulated. Pods were hand picked from individual plants that were to be progeny tested. In classifying the nodulation trait in crosses subsequent to the F1 generation, the few class was considered as nodulated. This classification scheme is consistent with those used by others examining nodulation in peanut (e.g., Dutta and Reddy 1988). Data were analyzed by chi-square tests for goodness-of-fit to the two-locus (Nigam et al. 1982) and three-locus models for nodulation (Dutta and Reddy 1988; Essomba et al. 1991).
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Results and Discussion |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionReferences |
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Field observation indicated three nodule categories: nonnodulated, few nodules, and normally nodulated. Leaf colors were yellow-green or dark green. Yellow-green plants either had few or no nodules, and dark green plants had normal nodulation. Most plants with few nodules also had larger nodules than a normally nodulated plant. Peanut plants with few, very large nodules also were observed by Nambiar and Dart (1980) in populations that were segregating for nodulating and nonnodulating plants.
Reciprocal crosses in the F1 involving the nonnodulating mutant, M4-2, showed differences in nodulation (Table 1). The three crosses with M4-2 as the female parent resulted in all progeny being normally nodulated. However, the three crosses with M4-2 as the male parent exhibited reduced nodulation in the F1. This effect was particularly pronounced in F1 plants generated from PI 262090 x M4-2. Of the 33 F1 plants rated, 8 were nonnodulated, 24 had few, and only 1 was normally nodulated.
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F2 data were analyzed by chi-square tests for goodness-of-fit to the expected ratios for the two-locus (Nigam et al. 1982) and three-locus models for nodulation (Dutta and Reddy 1988; Essomba et al. 1991). Only the three-locus model proposed by Dutta and Reddy (1988) fit the observed F2 data (Table 2). The results indicate that three gene loci are operating in these crosses. The genotypes proposed for the parents are n1n1n2n2N3N3 for M4-2, n1n1N2N2n3n3 for PI 262090, N1N1n2n2N3N3 for UF 487A, and N1N1N2N2n3n3 for Florunner (Table 1). The cross UF 487A (N1N1n2n2N3N3) x M4-2 (n1n1n2n2N3N3) and the reciprocal cross segregated 3 nodulated:1 nonnodulated. This indicates that the N1 allele is completely dominant to n1 and results in nodulation. The cross PI 262090 (n1n1N2N2n3n3) x M4-2 (n1n1n2n2N3N3) segregated 10 nodulated: 6 nonnodulated because half of the plants that were heterozygous at the N2 locus (n1n1N2n2N3-) were formed as a result of either the union of an n1N2N3 female gamete and an n1n2_ male gamete or an n1N2n3 female gamete and an n1n2N3 male gamete which would produce plants that were nonnodulated as a result of the parental effect described earlier.
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In accordance with this model of inheritance, the crosses Florunner[lb (N1N1N2N2n3n3) x M4-2 (n1n1n2n2N3N3), UF 487A (N1N1n2n2N3N3) x PI 262090 (n1n1N2N2n3n3), and reciprocals produced the same F2 segregation ratios since they had the same F1genotypes (N1n1N2n2N3n3, with an expected ratio of 58 nodulated:6 nonnodulated. All N1_ _ _ _ _ and _ _N2N2_ _ genotypes were normally nodulated. Half of the plants that were n1n1N2n2N3N3 and n1n1N2n2N3n3 would be phenotypically classified as nonnodulated and the other half as normally nodulated, for the same reason mentioned in the previous cross.
The crosses Florunner (N1N1N2N2n3n3) x PI 262090 (n1n1N2N2n3n3), Florunner (N1N1N2N2n3n3) x UF 487A (N1N1n2n2N3N3), and their reciprocals produced all normally nodulated plants since both parents were homozygous dominant at the N1 and/or N2 locus. All but one of 2920 segregates were nodulated. This one easily could have been nonnodulated due to a number of factors including environmental conditions or mutations. The chi-square values for all F2 data had probabilities above the 10% level, strongly supporting the three-locus model (Table 2).
The number of F2 families (classified F3 plants) derived from nodulated F2 plants was determined by calculating the ratio of each expected F2 genotype that had normal nodulation and then determining the expected segregation ratio of the progeny for each genotype, and the results supported the three-locus model of nodulation. For example, from the cross UF 487A x M4-2 and the reciprocal, one would expect one-third of the nodulated plants to produce only nodulated progeny and two- thirds to segregate 3 nodulated:1 nonnodulated. These expected ratios were observed (P = .49 and .54).
The F1BC1 data also provided strong evidence to support the proposed model (Table 3). For example, in the last two entries involving PI 262090 and M4-2 (Table 3) the genotypes of the parents are n1n1N2N2n3n3 and n1n1N2n2N3n3, when the female gamete was n1N2n3 and the male gamete was n1n2N3, the resulting F1BC1 plant was nonnodulated with a genotype of n1n1N2n2N3n3. However, when the female gamete was n1n2N3,, and the male was n1N2n3, the F1BC1 plant was nodulated and had the same genotype as the previous example, n1n1N2n2N3<n3. So, the genotypes are the same, but their nodulation differs relative to inheritance from the maternal or paternal parent. Similar results were also obtained for F2BC1 data.
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Our proposed model for inheritance of nonnodulation in peanut suggests that the phenotype of peanut plants can be different even though the genotypes are the same because of a parental effect. Mouli and Patil (1975) reported a similar mode of inheritance for an X-ray-induced foliaceous stipule mutant in peanut. They found that F1 plants showed normal stipules when the mutant was used as the female parent, but when the mutant was used as the pollen parent all F1 plants had foliaceous stipules. Similar to our results, parental influence on expression also was evident in their F1BC1. A parental effect in peanut has also been described in a spontaneously derived shriveled seed mutant (Jakkula et al. 1997b). Jakkula et al. (1997a) found that when the shriveled seed mutant was the male parent, the progeny segregated in the expected Mendelian fashion, 3 normal:1 shriveled in the F2 derived from a cross with a wild-type peanut. However, when the mutant was used as the female parent, only normal seed was produced in F1, F2, and F3 seed progenies.
In this study, results of our F2 and backcross data make it appear unlikely that extranuclear inheritance plays a role in nonnodulation. One possible interpretation of our results may be that the inheritance of nodulation in peanut is controlled by parental or gametic imprinting (for a review see Matzke and Matzke 1993). In such genomic imprinting, either the maternally or paternally derived allele is actively expressed, while the other is silent. Imprinting involves an epigenetic mechanism such as DNA methylation. In the mammalian genome, it has been shown that there are allele-specific regions of differential methylation in imprinted genes, and a trend for imprinted genes to be clustered (for a review see Constância et al. 1998). In our study, it is possible that imprinting of the N2 locus results in reduced expression when inherited through the egg. However, when inherited through the male gamete, imprinting of the N2 locus is erased and this allele becomes fully active. Since a parental effect has been detected for several different characters in peanut, it supports the hypothesis that peanut may regulate expression of a number of genes through some form of genomic imprinting.
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Acknowledgments |
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The authors thank Drs. D. S. Wofford and R. L. Smith for critical review of the manuscript. This work was approved for publication as journal series no. R-07333 by the Florida Agricultural Experiment Station.
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Footnotes |
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Corresponding Editor: Halina T. Knap
Received January 24, 2000
Accepted August 31, 2000
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References |
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