Linkage between genes for leaf colour, plant pubescence, number of leaflets and plant height in lentil (Lens culinaris Medik.)
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1 Euphytica (2005) 145: DOI: /s z C Springer 2005 Linkage between genes for leaf colour, plant pubescence, number of leaflets and plant height in lentil (Lens culinaris Medik.) Yogesh Kumar 1, S.K. Mishra 1, M.C. Tyagi 1, S.P. Singh 2 &B.Sharma 1,3, 1 Division of Genetics, Indian Agricultural Research Institute, New Delhi , India; 2 Department of Genetics and Plant Breeding, CCS University, Meerut , India; 3 16/10 East Patel Nagar, New Delhi , India ( author for correspondence: drbrsh@yahoo.co.in) Received 12 January 2005; accepted 22 June 2005 Key words: gene mapping, inheritance, leaf colour, leaflet number, lentil, plant height, plant pubescence Summary Monogenic inheritance and linkage were established on the basis of F 1 observations and analysis of 13,498 plants in 42 crosses for leaf colour, 7046 plants in 27 crosses for plant pubescence, 1926 plants in 8 crosses for number of leaflets per leaf, and 3182 plants in 12 crosses for plant height under field conditions. Normal green colour of foliage was found to be dominant over light green, pubescent plant over glabrous, high number of leaflets per leaf over low number of leaflets, and tall plant over dwarf. Linkage was estimated from joint segregation analysis, taking two characters at a time in all possible combinations as significant χ 2 values were recorded for these genes. Gene symbols Gl, Pub, Ph, and Hl are proposed for these four traits, respectively. The genes are arranged in the order of Ph-Gl-Pub-Hl with the map distances of 21.1, 28.9, and 17.5 cm between them. This short sequence of four linked genes spanning over 37.2 cm has been called Linkage Group 2 of lentil. Introduction Lentil (Lens culinaris Medik.), although an important grain legume, has remained a neglected crop in genetic studies. For a well-designed breeding programme, it is important to know the inheritance pattern and linkage associations between various traits, especially those of economic value. Knowledge about linkage of economic attributes with easily scorable breeding-neutral traits can be used to improve breeding efficiency. Only a few genes for specific traits have been reported so far. The lentil chromosomes are not yet identified with genes for visible traits even though the seven chromosomes have been distinguished with molecular markers (Eujayl et al., 1998). In the absence of linkage established between molecular markers and visible morphological, physiological or biochemical traits, molecular mapping alone cannot be used fruitfully. Information has been reported on the inheritance of plant height (Ph)(Tahir et al., 1994), cotyledon colour (Y, B, Dg) (Emami & Sharma, 1996a,c; Sharma & Emami, 2002), pubescence development on the pod (Glp)(Vandenberg & Slinkard, 1989), peduncle (Pdp) (Emami, 1996), and whole plant (Pep, Pub) (Sarker et al., 1999; Hoque et al., 2002), pigmentation of stem (Gs) (Ladizinsky, 1979), pod (Grp, Pdp, Rdp) (Vandenberg & Slinkard, 1989; Havey & Muehlbauer, 1989; Emami, 1996b), and leaf (Bl) (Emami & Sharma, 1996), pod dehiscence (Pi) (Ladizinsky, 1979b), tendril formation (Tnl)(Vandenberg & Slinkard, 1989), flower colour (V, P) (Lal & Srivastava, 1975), flower number per peduncle (Fn) (Gill & Malhotra, 1980), flowering time (Sn) (Sarker et al., 1999), seed coat colour (Ggc, Tgc)(Vandenberg & Slinkard, 1990), seed coat pattern (Scp, Mot, Spt)(Vandenberg & Slinkard, 1990; Emami, 1996), black testa (Blsc, Blt)(Vaillancourt & Slinkard, 1992; Emami & Sharma, 2000), and biochemical markers (Tahir & Muehlbauer, 1994). Short sequences of
2 42 few linked genes have also been published (Tahir et al., 1993; Tahir & Muehlbauer, 1994; Emami & Sharma, 1999). It is, therefore, important to discover genes in large numbers and work out their linkage relationship in composite mapping with molecular markers. In a detailed survey of world germplasm maintained in the Division of Genetics, Indian Agricultural Research Institute (IARI), Delhi, about three dozen visible traits could be identified that are suitable for genetic analysis. Acceptably, this is too small a number of discrete traits and genes for a meaningful programme of genetic mapping. Many more genes need to be discovered through mutation induction. Nevertheless, an attempt was made to investigate the mode of inheritance of the identified traits and establish linkage relationships between their genes. The present study reports a short sequence of four linked genes. Materials and methods The experiments were conducted at the Research Farm of the Division of Genetics, IARI, Delhi, during A total of 35, 30, 13, and 19 genotypes were involved in crossing programme to study the inheritance of leaf colour, plant pubescence, number of leaflets per leaf, and plant height, respectively. All the crosses were made at the Wheat Summer Nursery, Dalang Maidan, Lahaul Spiti, Himachal Pradesh. The F 1 seeds were sown in Delhi. The F 2 populations along with the parent strains and F 1 plants were raised in spaced out rows to ensure easy single plant observation. Observations on leaf colour, number of leaflets per leaf, and plant height were recorded at pod filling stage to physiological maturity of pods, i.e days after sowing. Presence or absence of pubescence was recorded days after sowing. To study the inheritance of each trait, χ 2 was estimated by the standard formula. Linkage was detected from joint segregation analysis (Mather, 1951) and map distance as suggested by Kosambi (1944). Results and discussion Green leaf colour Two distinct genotypes were identified within the range of green colour of foliage usually found in natural germplasm. Based on intensity of coloration they were called as normal green and light green. In contrast with the usual chlorophyll mutations of various kind, the genotypes with light green foliage do not seem to be handicapped in terms of viability, fertility, or productivity. Inheritance of colour intensity was studied in 42 crosses (Table 1). The F 1 plants of all the crosses produced normal green foliage. The F 2 populations segregated into plants with normal green and light green foliage with a good fit to 3:1 ratio with nonsignificant χ 2 values (χ 2 = ; P = ). The ratio was confirmed from the analysis of the pooled population of 13,498 F 2 plants (χ 2 = 0.22; P = 0.65) with nonsignificant heterogeneity among the crosses (χhet. 2 = at 41 df; P = 0.93). The intensity of colour within the normal range is thus controlled by a single gene. The gene symbol Dgl was proposed earlier for this trait (Hoque et al., 2002). However, the dark green leaf colour of the dominant allele in this case falls in the normal range. Few accessions in the germplasm have much darker green foliage than the normal green leaf in the present case (wild type) which is due to pleiotropic effect of a gene which in recessive condition produces dark green cotyledons (Sharma & Emami, 2002). Therefore, the darker green colour of foliage within the normal range must be distinguished from other dark green phenotypes. This will also avoid the confusion if more mutations with much darker green foliage beyond the normal range are discovered subsequently. We consider it appropriate to call the two phenotypes investigated in the present study as normal green and light green leaf. Consequently, the gene symbol is revised to Gl (green leaf), with the recessive allele gl producing light green foliage. Plant pubescence The presence or absence of pubescence on pod was first investigated by Vandenberg and Slinkard (1989) and gene symbol Glp (for glabrous pod) was proposed. Sarker et al. (1999) assigned gene symbol Pep for the same trait in pilosae lentils of South Asia and demonstrated its linkage with the genes for seed coat pattern (Scp) and flowering time (Sn). Emami (1996) proposed gene symbol Pdp for peduncle pubescence, but this gene symbol was also proposed for the gene causing violet stripes on the pod (Havey & Muehlbauer, 1989). Sarker et al. (1999) used gene symbol Pep for pubescence development on the whole plant and peduncle alternatingly in the pilosae lentils of South Asia, i.e. the cultivated lentils of the Indian subcontinent
3 43 Table 1. for leaf colour in lentil Cross Female parent Male parent F 1 phenotype Normal green Light green χ 2 (3:1) P Normal Light green L B-G-8 Normal green L 263 L 435 Normal green L Y-13 Normal green L 4378 P Normal green L B-G-8 Normal green L 4384 Precoz Normal green L 6163 P Normal green L 6163 Dwarf mut. Normal green PL B-G-8 Normal green PL 406 L 3685 Normal green PKVL 1 MC 6 Normal green Pusa 4 P Normal green Sehore74-3 Precoz Normal green L 435 Normal green Precoz Normal green B-2 Precoz Normal green B-21 P Normal green B-21 EC Normal green Light Normal green L 435 L 1304 Normal green L 4602 Fsciated mut. Normal green LC L 4149 Normal green LC B-2 Normal green Precoz L 830 Normal green Precoz L 4076 Normal green P E 153 Normal green P L 6163 Normal green P L 1304 Normal green P L 4378 Normal green Dwarf mut. P Normal green EC L 4378 Normal green EC Pusa 4 Normal green EC B-2 Normal green EC L 1304 Normal green EC PL 406 Normal green EC B-2 Normal green MC Normal green MC 6 L 4387 Normal green MC 6 L 4384 Normal green MC 6 Sehore74-3 Normal green Y-50 L 1304 Normal green Y-26globe Sehore74-3 Normal green Pooled over 42 crosses Normal green Heterogeneity (41 df)
4 44 (sometimes also referred to as Indian lentils ). Our observations on a very large volume of germplasm accessions confirmed beyond doubt that pubescence development is not confined to the inflorescence or pod alone. The whole plant is either pubescent or glabrous. Pubescence, when present, is most conspicuous at the growing apex of the plant and on the inflorescence, especially the peduncles and calyx. To avoid multiplicity of gene symbols for the same trait, we have proposed gene symbol Pub for pubescence formation on the lentil plant (Hoque et al., 2002). It needs to be explored if there are Pub alleles responsible for tissue-specific expression. The inheritance of pubescence development on the plant was studied in 27 crosses (Table 2). The F 1 plants of all the crosses were pubescent. The F 2 populations of all the crosses segregated with a good fit to the ratio of 3 pubescent:1 glabrous (χ 2 = ; P = ). The ratio was confirmed by the analysis of pooled population of 7074 F 2 plants (χ 2 = 1.43; P = 0.24), heterogeneity among the crosses being nonsignificant (χ 2 Het. = at 26 df; P = 0.76). Thus, the presence of pubescence on the lentil plant is dominant over its absence (glabrous plant) and the trait is monogenically inherited. This trait was not described in its full manifestation earlier. Therefore, the gene symbols Table 2. for plant pubescence in lentil Cross Female parent Male parent F 1 phenotype Pubescent Glabrous χ 2 (3:1) P Pubescent Glabrous L B-G-8 Pubescent L Y-13 Pubescent L 6163 P Pubescent LH L 3685 Pubescent PL 406 L 3685 Pubescent PL B-G-8 Pubescent Pusa 4 P Pubescent Dwarf mut. P Pubescent Sehore 74-3 Precoz Pubescent L 435 Pubescent P Pubescent B-2 Precoz Pubescent B-2 L 3685 Pubescent Glabrous Pubescent L 435 L 1304 Pubescent L 4602 Fasciated mut. Pubescent Precoz L 830 Pubescent Precoz L 4076 Pubescent Precoz PKVL 1 Pubescent P L 6163 Pubescent P L1304 Pubescent P PL639 Pubescent MC 6 Sehore 74-3 Pubescent EC B-2 Pubescent EC B-2 Pubescent EC PL 406 Pubescent EC L 1304 Pubescent Y-50 L 1304 Pubescent Pooled over 27 crosses Heterogeneity (26 df)
5 45 Table 3. for number of leaflets per leaf in lentil Cross Female parent Male parent F 1 phenotype High Low χ 2 (3:1) P High Low leaflet no. L B-G-8 High L B-G-8 High PL B-G-8 High EC B-G-8 High Low High leaflet no. L 4602 Fasciated mutant High LC L 6163 High Precoz High Y-50 L 1304 High Pooled over 8 crosses Heterogeneity (7 df) Table 4. for plant height in lentil Cross Female parent Male parent F 1 phenotype Tall Dwarf χ 2 (3:1) P Tall Dwarf L B-G-8 Tall L Y-13 Tall L 3685 Precoz Tall LH Dwarf mut. Tall B-21 P Tall Dwarf Tall L 830 globe L 6163 Tall L 4602 Fasciated mut. Tall P L 6163 Tall P L 1304 Tall Dwarf mut. P Tall EC L 1304 Tall EC PL 406 Tall Pooled over 12 crosses Heterogeneity (11 df) Glp (Vandenberg & Slinkard, 1989) and Pdp (Emami, 1996) are held invalid. Number of leaflets per leaf The leaves in macrosperma lentils are usually longer with conspicuously larger number of leaflet pairs than the microsperma types, although the longer leaf trait has now been transferred to several microsperma genotypes. The inheritance of this trait has not been studied earlier. The inheritance of leaflet number was studied in eight crosses taking parental strains with distinctly different number of leaflets per leaf (Table 3). The number of leaflets per leaf was in the range of 6 8 pairs in the long-leaf genotypes and 4 5 pairs in the strains with shorter leaves. The F 1 plants in all the crosses had high number of leaflets per leaf. The F 2 populations always segregated into 3 high:1 low-leaflet plants (χ 2 = ; P = ). The pooled analysis of 1926 F 2 plants over all the crosses confirmed 3:1 ratio (χ 2 = 1.28; P = 0.26) with nonsignificant
6 46 Table 5. Joint segregation and linkage intensity of the gene Gl (green leaf) with Pub (plant pubescence), Ph (plant height), and Hl (number of leaflets per leaf) in lentil χ 2 Loc. Loc. Joint P R.F. Map Gene pair (X)-(Y) Cross XX Xy xy xy X (3:1) Y (3:1) segregation (Linkage) (%) distance (cm) Gl-Pub (Coupling) Pusa 4 P L B-G P L PL B-G < L Y < P L < EC B < L 435 L < MC 6 Sehore < EC Pusa < Precoz L < L.4602 Fasciated mut < EC B < B-2 Precoz < Dwarf mut. P < Pooled analysis < Heterogeneity (14 df) <0.01 Gl-Ph (Coupling) L B-G < B-21 P < EC PL < P L < L Y < P L < L 4602 Fasciated mut < Pooled analysis < Heterogeneity (6 df) Gl-Hl (Coupling) L B-G < PL B-G < L 4602 Fasciated mut < Precoz < Pooled analysis < Heterogeneity (3 df) heterogeneity among them (χhet. 2 = 4.91 at 7 df; P = 0.67). These results confirm that high number of leaflets is monogenically dominant over the low-number phenotype. The gene symbol Hl is proposed to denote high number of leaflets per leaf. The plant produces fewer leaflets per leaf in homozygous recessive (hl hl) condition. Plant height The inheritance of plant height (tall and dwarf) was studied in 12 crosses which involved 9 tall and 10 dwarf genotypes in different combinations (Table 4). The F 1 plants were tall in all the crosses. In F 2,a3 tall:1 dwarf ratio (χ 2 = ; P = ) was obtained in all the crosses analyzed individually. This pattern was confirmed when the data of 3182 F 2 plants in the 12 crosses were subjected to pooled analysis (χ 2 = 3.03; P = 0.09), heterogeneity among them being nonsignificant (χhet. 2 = 4.68 at 11 df; P = 0.94). Thus, plant height is also a monogenic trait with tallness dominant over dwarfness. The gene symbol Ph is already proposed for this trait (Tahir et al., 1994).
7 Table 6. Joint segregation and linkage intensity of the gene Pub (plant pubescence) with Ph (plant height), and Hl (number of leaflets per leaf) in lentil χ 2 Joint P Map Gene pair (X)-(Y) Cross XY Xy xy xy Loc. X Loc. Y segregation (Linkage) R.F. (%) distance (cm) Pub-Ph (Coupling) EC L EC PL P L < L Y P L < L 4602 Fasciated mut < Pooled analysis < Heterogeneity (5 df) Pub-Hl (Coupling) L B-G < PL B-G < Y-50 L < L 4602 Fasciated mut < Pooled analysis < Heterogeneity (3 df) < Table 7. Joint segregation and linkage intensity between the genes Ph (plant height) and Hl (number of leaflets per leaf) in lentil χ 2 Joint Map Gene pair (X)-(Y) Cross XY Xy xy xy Loc. X (3:1) Loc. Y (3:1) segregation P (Linkage) R.F. (%) distance (cm) Ph-Hl (Coupling) L B-G < Detection of linkage Fifteen crosses were analyzed to detect linkage between the genes Gl and Pub (Table 5). Joint segregation analysis in the F 2 of each cross as well as in the pooled data of 3858 F 2 plants revealed highly significant linkage χ 2 for the Gl-Pub gene pair, ranging from 9.3 to 649.8; P = 0.01 or less. The recombination percentage was in the range of in different crosses in coupling phase. The recombination value in pooled data was 26.1%. The map distance varied from 12.6 to 45.8 cm in different crosses, with the average of 28.9 cm (Table 5). The joint segregation of the gene Gl with Ph was studied in seven crosses (Table 5). The linkage χ 2 values were highly significant in each cross individually as well as in the pooled data of 1680 F 2 plants, indicating Gl-Ph linkage (χl 2 = ; P < 0.01). The coupling phase recombination value ranged from 13.3 to 22.0% in different crosses, and 19.9% in pooled data, which corresponds to the map distance of cm (average 21.1 cm). Linkage between Gl and Hl was revealed in four crosses (Table 5) individually as well as in pooled analysis of 1057 F 2 plants (χl 2 = ; P < 0.01). The recombination rate in coupling phase was % (24.8% averaged over all the crosses). The map distance varied from 20.9 to 39.3 cm, with the mean value of 27.2 cm. Joint segregation in the F 2 of each of the six crosses as well as pooled population of 977 plants (Table 6) confirmed Pub-Ph linkage (χl 2 = ; P < 0.01). The recombination fraction was in the range of % in individual crosses, and 29.7% over all the crosses in coupling phase, which corresponds to the map distance of cm in individual crosses, with the mean of 34.2 cm. The Pep gene showed 38% recombination with Sn in an earlier study (Sarker et al., 1999). The Ph-Pub recombination recorded in this study was 29.7%. This means that Ph is either located close to Sn or at almost similar distance on the opposite side beyond Hl. In the latter event, the genes Scp and Hl should be tightly linked as they recombined with Pep at 18% frequency
8 48 References Figure 1. Linkage group 2 of lentil. Map distances in cm. in the experiment of Sarker et al. (1999) and 16.8% (Pub-Hl) inthe present study (see below). Joint segregation analysis of the gene Pub with Hl (Table 6) had highly significant linkage χ 2 in each cross individually as well as in the pooled data of 1204 F 2 plants, indicating linkage between these genes (χl 2 = ; P < 0.01). The recombination frequency varied from 7.1 to 33.1% in different crosses in coupling phase, and 16.8% in pooled data. The map distance varied from 7.1 to 39.8 cm in different crosses (17.5 cm on pooled basis). Analysis of the F 2 population of 424 plants in the cross L B-G-8 revealed strong linkage between Ph and Hl (χl 2 = 43.6; P < 0.01). The recombination frequency was 31.6% and map distance 37.2 cm in coupling phase (Table 7). Limited information was reported earlier on the inheritance and linkage of three of the four traits covered in this study, i.e. green leaf colour (Gl), plant pubescence (Pub), and plant height (Ph). One more trait (leaflet number) has been added to this linkage group. The monogenic trait of pubescence development was identified differently in earlier studies as peduncle pubescence (Emami, 1996), pod pubescence (Vandenberg & Slinkard, 1989), and whole plant pubescence in pilosae lentils (Sarker et al., 1999) with three gene symbols (Pdp, Glp and Pep, respectively). The present study seeks to correct this anomaly by treating pubescence development on the plant as a single trait with gene symbol Pub for all types of cultivated, semiwild, and wild lentils. The inheritance of plant height with the gene symbol Ph was investigated earlier (Tahir et al., 1994) without determining its affinity to any linkage group. The arrangement of genes derived from different crosses is presented in Figure 1. The order of genes after putting all the segments together is Ph-Gl-Pub- Hl. The map positions of Dgl (now called Gl) and Pub are shown on the basis of an earlier report on their linkage (Hoque et al., 2002). Emami, M.K., Genetic mapping in lentil (Lens culinaris Medik.) (Ph.D. Thesis). Indian Agricultural Research Institute, New Delhi, India. Emami, M.K. & B. Sharma, 1996a. Digenic control of cotyledon colour in lentil (Lens culinaris). Indian J Genet 56(3): Emami, M.K. & B. Sharma, 1996b. Inheritance of brown leaf pigmentation in lentil. Indian J Genet 56(3): Emami, M.K. & B. Sharma, 1996c. Confirmation of digenic inheritance of cotyledon colour in lentil (Lens culinaris). Indian J Genet 56(4): Emami, M.K. & B. Sharma, Linkage between three morphological markers in lentil (Lens culinaris Medik.). Plant Breed 118: Emami, M.K. & B. Sharma, Inheritance of black testa colour in lentil (Lens culinaris Medik.). Euphytica 115: Eujayl, I., M. Baum, W. Powell, W. Erskine & E. Pehu, A genetic linkage map of lentil (Lens sp.) based on RAPD and AFLP markers using recombinant inbred lines. Theor Appl Genet 97: Gill, A.S. & R.S. Malhotra, Inheritance of flower colour and flower number per inflorescence in lentils. LENS 7: Hoque, M.E., S.K. Mishra, Y. Kumar, R. Kumar, S.M.S. Tomar & B. Sharma, Inheritance and linkage of leaf colour and plant pubescence in lentil (Lens culinaris Medik.). Indian J Genet 62(2): Kosambi, D.D., The estimation of map units from recombination values. Ann Eugen Lond 12: Ladizinsky, G., The genetics of several morphological traits in lentil. J Hered 70: Lal, S. & R.S. Srivastava, Inheritance of flower colour in lentils. Indian J Genet 35(1): Mather, K., The Measurement of Linkage in Heredity. Wiley, New York. Sarker, A., W. Erskine, B. Sharma & M.C. Tygi, Inheritance and linkage relationship of days to flowering and morphological loci in lentil (Lens culinaris Medikus subsp. culinaris). J Hered 90(2): Sharma, B. and M.K. Emami, Discovery of new gene causing dark green cotyledons and pathway of pigment synthesis in lentil (Lens culinaris Medik.). Euphytica 124: Tahir, M. & F.J. Muehlbauer, Gene mapping in lentil with recombinant inbred lines. J Hered 85(4): Tahir, M., F.J. Muehlbauer & S.C. Spaeth, Association of isozyme markers with quantitative trait loci in random single seed descent lines of lentil (Lens culinaris Medik.). Euphytica 75: Tahir, M., C.J. Simon & F.J. Muehlbauer, Gene map of lentil Areview. Lens Newsl 20(2): Vaillancourt, R.E. & A.E. Slinkard, Inheritance of new genetic markers in lentil (Lens Miller). Euphytica 64: Vandenberg, A. & A.E. Slinkard, Inheritance of four new quantitative genes in lentil. J Hered 80: Vandenberg, A. & A.E. Slinkard, Genetics of seed coat colour and pattern in lentil. J Hered 81:
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