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Published in Crop Sci 39:1881-1886 (1999)
© 1999 Crop Science Society of America
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Crop Science 39:1881-1886 (1999)
© 1999 Crop Science Society of America

PLANT GENETIC RESOURCES

Genetic Diversity in Cotton Assessed by Variation in Ribosomal RNA Genes and AFLP Markers

M. Pillaya and G.O. Myersb

a International Institute of Tropical Agriculture, PMB 008, Nchia-Eleme, Port Harcourt, Nigeria
b Dep. of Agronomy, Louisiana Agric. Exp. Stn., Louisiana State Univ. Agric. Center, Baton Rouge, LA 70803 USA

gmyers{at}agctr.lsu.edu


   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 Materials and methods
 Results and discussion
 REFERENCES
 
Variation in the ribosomal RNA genes (rDNA) and amplified fragment length polymorphism (AFLP) markers has been used to establish the extent of genetic diversity and relatedness in plants. The utility of these methods to detect inter- and intra-specific variation in cotton (Gossypium spp.) has not been reported and could be useful in cultivar identification and in marker assisted selection. The objectives of this study were to: (i) determine the molecular organization of the rDNA genes by restriction enzyme mapping and (ii) assess the level of AFLPs in Old and New World species of cotton. A restriction site map of the rDNA gene structure of G. hirsutum L. cv. TM1 was constructed from DNA digested with 12 restriction enzymes and hybridized to heterologous probes. Four EcoRI-MseI primer-pair combinations were used for the AFLP analysis. The rDNA gene structure in cotton was found to be similar to that of most higher plants. The rDNA repeat size was 9.4 kbp in G. hirsutum and G. barbadense L., and 9.6 and 9.8 kbp in G. arboreum L. and G. herbaceum L., respectively. No intraspecific polymorphism was detected in the spacer. The presence of two SspI sites in G. arboreum and G. herbaceum and a single site in G. hirsutum and G. barbadense separated Old and New World cottons. The AFLP method produced a 10-fold increase in the number of DNA bands per plant, compared with random amplified polymorphic DNA (RAPD) methods. The AFLP data assigned the species–genotypes into groups that corresponded with their origin and/or pedigree relationships.

Abbreviations: AFLP, amplified fragment length polymorphism • PCR, polymerase chain reaaction • rDNA, ribosomal DNA • RAPD, random amplified polymorphic DNA • RFLP, restriction fragment length polymorphism


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
Materials and methods
 Results and discussion
 REFERENCES
 
FOUR SPECIES

of the genus Gossypium provide most of the world's textile fiber and are important sources of oil and cottonseed meal. These species include the Asian-African diploids (A genome), G. arboreum and G. herbaceum (2n = 26 ), and the New World tetraploids (AD genome), G. hirsutum and G. barbadense (2n = 4x = 52). A number of studies have been conducted to investigate genetic diversity in cultivated cotton at the DNA level (Wendel, 1989; Brubacker and Wendel, 1994; Multani and Lyon, 1995; Tatineni et al., 1996) and with respect to allozyme composition (Wendel et al., 1989, 1992). These studies, in general, revealed that cultivated cotton displays a very low level of genetic diversity. There still exists the need for cultivar-specific DNA markers in a cotton breeding program for (i) cultivar registration, plant patents, and breeder's right protection and (ii) early detection of agronomic and economic traits as an aid to marker assisted selection.

Ribosomal DNA (rDNA) is a well-characterized multi-gene family in plants which is organized in tandem repeats. Each repeat contains DNA sequences coding for the 18S, 5.8S, and 25S ribosomal RNA, and an intergenic region generally called the intergenic spacer region or IGS (Rogers and Bendich, 1987). The 5.8S coding region separates the 18S and 25S regions and is bordered by two internal spacer regions referred to as ITS1 and ITS2. Molecular studies of variability in rDNA show that the coding region is highly conserved while the spacer region is highly variable in sequence and length. Variation patterns in rDNA have been used : (i) to characterize genetic diversity in plants, (ii) to assess changes in the genetic composition of breeding populations, (iii) to determine phylogenetic relationships at different levels of the taxonomic hierarchy, and (iv) as important genetic markers.

AFLP is polymerase chain reaction (PCR) based marker technology that involves three essential steps: (i) digestion of genomic DNA with two restriction enzymes, (ii) ligation of adapter sequences to the restriction ends, and (iii) selective amplification of sets of restriction fragments by two successive PCR reactions. The PCR products are separated in denaturing polyacrylamide gels and usually results in 60 to 80 DNA bands per sample. Therefore AFLP is considered one of the most powerful high density marker systems and has several advantages over other marker systems including (i) a 10-fold increase in the number of informative markers per analysis, (ii) its ability to give highly reproducible banding patterns, and (iii) no a priori sequence information of the DNA is necessary. AFLPs have been used to estimate genetic relationships in many studies including lentil (Lens culinaris Medikus) (Sharma et al., 1996), soybean [Glycine max (L.) Merr.] (Maughan et al., 1996), lettuce (Lactuca spp. L.) (Hill et al., 1996), and hop (Humulus lupulus L.) (Hartl and Seefelder, 1998); construct linkage maps in potato (Solanum tuberosum L.) (Meksem et al., 1995), sugar beet (Beta vulgaris L.) (Schondelmaier et al., 1996), and barley (Hordeum vulgare L.) (Becker et al., 1995); and provide markers for disease resistance in Populus (Cevera et al., 1996).

The objectives of this study were to: (i) determine the structure of and variability within the rDNA repeat unit in cotton by restriction endonuclease mapping and (ii) investigate the efficiency of AFLP markers in evaluating genetic diversity in cotton.


   Materials and methods
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 Materials and methods
Results and discussion
 REFERENCES
 
The plant material used in this study consisted of 11 accessions of G. hirsutum and two accessions from each of G. arboreum, G. barbadense, and G. herbaceum (Table 1) . A sub-sample of this material was used in the AFLP analysis. Seed material was obtained from the cotton-breeding program at Louisiana State University and from the USDA collection (College Station, TX). Seeds were germinated in 20-cm plastic pots in the greenhouse and young leaves harvested for DNA extraction. Total genomic DNA was isolated from 3 to 5 g of leaf material by the procedure of Paterson et al. (1994) with minor modifications.


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  		Table 1 List of cotton species and cultivars used in ribosomal DNA analysis

 
Ribosomal DNA Analysis
For an initial assessment of rDNA variation in cotton, approximately 3 to 5 µg of DNA from 16 accessions–cultivars (Table 1) was restriction digested with the enzymes BamHI, BglI, BstEII, DraI, EcoRI, EcoRV, HindIII, KpnI, NcoI, NdeI, NsiI, SacI, ScaI, SpeI, SspI, XbaI, and XhoI. The enzymes HindIII, KpnI, NdeI, ScaI, and XhoI were not used in further analysis because they either had no cleavage sites within the rDNA of cotton or produced fragment patterns that could not be resolved unambiguously. The cv. TM1 was selected for double digestions and physical mapping of the rDNA unit. TM1 is a long-term inbred upland cotton strain derived from `DeltaPine 14' (Kohel et al., 1970) and is a good standard. Double digestions were done with XbaI, NsiI, or SspI in combination with the other enzymes. Agarose gel electrophoresis and Southern transfer to nylon membranes were carried out as described previously (Pillay, 1996). Molecular hybridizations were done with the ECL direct nucleic acid labeling and detection system (Amersham, Buckinghamshire, England) based on enhanced chemiluminescence. Hybridizations were carried out in plastic pouches at 42°C. Two clones, pRY12 and pRY18, that comprise the entire rDNA of rice were used, sequentially, as hybridization probes. The location of these probes in relation to the rDNA repeat of cotton is shown in Fig. 1 . The sizes of the hybridization bands were estimated from the autoradiogaphs on X-ray film as described previously (Pillay, 1996).



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  		Fig. 1 Generalized ribosomal DNA unit structure and rDNA restriction site map of Gossypium hirsutum cv. TM1. The positions of the 12 restriction enzyme sites are indicated. The location of the two rice probes pRY12 and pRY18 is shown. The enzymes used are: X, XbaI; B, BamHI; Nc, NcoI; Sp, SpeI; E, EcoRI; S, SacI; Ev, EcoRV; Be, BstEII; D, DraI; Ns, NsiI; Ss, SspI; and Bg, BglI

 
AFLP Fingerprinting
The AFLP procedure was performed, with minor modifications, according to the protocol of Vos et al. (1995) that is supplied with the AFLP Analysis System I (Life Technologies, Gaithersberg, MD). From 10 accessions–cultivars (Table 1), approximately 250 ng DNA of each sample was digested simultaneously with EcoRI and MseRI at 37°C for 2 h. A small aliquot of the digested DNA was run on a 1.5% (w/v) agarose gel to check if the DNA digestion was complete. The digested samples were incubated at 70°C for 15 min to inactivate the restriction endonucleases. EcoRI and MseRI adapters were ligated to the digested DNA samples to generate template DNA for amplification. Preamplification was carried out with +1-primers each carrying one selective nucleotide (EcoRI +A, MseRI + C) in a thermocycler for 20 cycles set at 94°C denaturation (30 s), 56°C annealing (60 s), and 72°C extension (60 s). The initial denaturation was done at 94°C for 30 s and the final extension at 72°C for 8 min. The amplification products were diluted 20-fold in TE buffer and stored at -20°C. Selective AFLP amplification was carried out with EcoRI + 3 primers and MseRI +3 primers and 5 µL of the diluted PCR products from the preamplification. Four primer pair combinations of EcoRI + 3 (E-plus three nucleotides) and MseRI + 3 (M-plus 3 nucleotides) were tested and include: (i) E-AAG/M-CTC, (ii) E-AAG/M-CTG, (iii) E-ACC/M-CAC, and (iv) E-AAG/M-CAA. The PCR amplifications were carried out as follows: one cycle at 94°C for 30 s, 65°C for 30 s, and 72°C for 60 s; followed by 12 cycles of touchdown PCR in which the annealing temperature was decreased by 0.7°C every cycle until a `touchdown' annealing temperature of 56°C was reached. Once reached, another 20 cycles were conducted as described above for preamplification.

The reaction product (2 µL) was mixed with an equal volume of formamide loading buffer (98% [v/v] formamide, 10 mM EDTA, 0.005% [v/v] of each of xylene cyanol and bromophenol blue) denatured by incubating at 90°C for 5 min and quickly cooled on ice. The products were analyzed on 5% (w/v) denaturing polyacrylamide gels. The gel was run at constant power (50–55 W) until the xylene cyanol was about two-thirds down the length of the gel. The gel was silver stained according to a protocol developed at the Laboratory for Crop Genome Analysis, Texas A&M University (Dr. S. Reddy, 1997, personal communication).

Bands that showed clear polymorphisms were scored visually as present (`1') or absent (`0'). Jaccard's coefficient of similarity (Jaccard, 1908) was used to obtain estimates of genetic similarity for phenetic analysis. A genetic similarity (GS) value of 1 indicates identity between plant x and plant y, while a GS value of 0 indicates maximum diversity between x and y. A dendrogram was constructed by the UPGMA clustering algorithm from the SAHN option of NTSYS-PC (Rohlf, 1985).


   Results and discussion
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 Materials and methods
 Results and discussion
REFERENCES
 
Ribosomal DNA
Digestion of the DNA from each of the 16 accessions–cultivars with BglI, BsteII, DraI, EcoRV, NcoI, NsiI, SpeI, and XbaI produced a single hybridization band with both pRY12 and pRY18 probes. This pattern suggests that there is a single cleavage site for these enzymes within the rDNA repeat unit of cotton. Such digestions are useful in determining the size of the complete rDNA repeat unit. Digestion with BamHI produced three hybridization bands in all plants. Two constant fragments of 3.9 and 0.6 kbp were present in all species. The 3.9 kbp fragment hybridized only to pRY18 while the 0.6 kbp fragment hybridized only to pRY12. These results suggested that the 3.9 and 0.6 kbp fragments were within the coding region. The third fragment varied from 4.9 to 5.3 kbp. Digestion with SacI produced three hybridization bands of 4.7 to 5.1, 2.8, and 1.9 kbp, while EcoRI produced two bands of 5.1 to 5.5 and 4.3 kbp. The enzyme SspI produced a single fragment in G. barbadense and G. hirsutum and two fragments of 5.4 to 5.6 and 4.2 kbp in G. arboreum and G. herbaceum. The NdeI digestions produced a single band after hybridization to both probes. However, this fragment was only 6.7 kbp in the New World tetraploid cottons, while it was 9.6 to 9.8 kbp in the Old World, diploid cottons. A complementary fragment for the NdeI digest in G. barbadense and G. hirsutum was not detected. An exact reason for this anomaly is unknown. The sizes of the various hybridization bands from the single and double digestions were used to construct a physical map for 12 restriction enzymes (Fig. 1). The complete rDNA repeat unit structure in cotton ranged in size from 9.4 kbp in G. barbadense and G. hirsutum to 9.6 kbp in G. arboreum and 9.8 kbp in G. herbaceum. No intraspecific polymorphism was detected.

The rDNA genes in cotton have the same general structure as those of most higher plants. Since this is the first report of rDNA gene structure in the family Malvaceae, a comparison with other closely related genera is not possible at this stage. However, the placement of many restriction sites (XbaI, BamHI, SacI, EcoRI, EcoRV) within the coding region of cotton rDNA (Fig. 1) is similar to those found in other dicotyledonous species such as pea (Pisum sativum L.) and pumpkin (Cucurbita spp.) (Jorgensen et al., 1987), tomato (Lycopersicon esculentum Miller) (Levesque et al., 1990), Brassica spp. L. (Delseny et al., 1990), sunflower (Helianthus spp. L.) (Rieseberg, 1991), Erianthus Michx. (Besse et al., 1996), and monocotyledonous species such as maize (Zea spp. L.) (Zimmer et al., 1988), sorghum [Sorghum bicolor (L.) Moench] (Springer et al., 1989), Bromus spp. L. (Pillay, 1996), and Eragrostis tef (Zucc.) Trotter (Pillay, 1997). The similarities between cotton rDNA gene structure and the rDNA gene structure in many other higher plants supports the conservative nature of the Nor family of genes.

A striking feature of this study is the absence of intraspecific variation, especially in the spacer region of the plants under study. Investigations of rDNA structure among plants generally show considerable spacer length variation within and among species. For example, 42 spacer length variants were detected in wild and cultivated rice (Oryza spp. L.) (Liu et al., 1996), 20 variants were detected in barley (Saghai-Maroof et al., 1990), and 20 variants were observed in a single Vicia faba L. plant (Rogers et al., 1986). The results of this study are similar to those of a more extensive one of Australian species of Gossypium (Wendel et al., 1991). The latter study detected no intraspecific polymorphisms in rDNA structure in 5 species of Gossypium in which 17 accessions from a very wide geographical range were studied. Considering the complexity of the cotton genome, allopolyploidy of New World cottons, and the diverse eco-geographical growing conditions, it was expected that cotton would have evolved great genetic diversity. Therefore, it appears that fixation of rDNA repeat type has occurred in cotton. Fixation of rDNA repeat type has been reported in many plants including Lupinus luteus L. (Rafalski et al., 1983), some species of Vicia (Lamppa et al., 1984), and Glycine (Doyle and Beachy, 1985). The rDNA repeat sizes varied slightly among the cotton species by increments of 200 bp from 9.4 to 9.8 kbp. This is comparable to repeat sizes in the Australian species that ranged from 9.4 to 10.6 kbp (Wendel et al., 1991). Since the length of the coding region is highly conserved in plants, variation in rDNA repeat size is attributed to variability in the intergenic spacer region. This was true in cotton since the fragments that varied in size hybridized only to the pRY12 probe that spans the intergenic spacer region.

The relatively homogeneous nature of the rDNA genes in cultivated cotton may be ascribed to concerted evolution and/or domestication. Concerted evolution or molecular drive tends to reduce variability between gene copies by mechanisms such as gene conversion and unequal crossing-over (Arnheim et al., 1980; Ohta and Dover, 1984). Some studies (Cordesse et al., 1990) have invoked domestication as a factor associated with a reduced variability of the rDNA spacer. This may be true also for cotton. However, while domestication cannot be discounted as a factor, other mechanisms such as natural and/or artificial selection (Flavell et al., 1986; Rocheford, 1994), genetic drift accompanied by limited gene flow, small population size, and geographical isolation (Sytsma and Schaal, 1990; Jellen et al., 1994) may be involved since wild species of cotton also have rather homogeneous rDNA repeat lengths.

The presence of two SspI sites in G. arboreum and G. herbaceum (not mapped) and a single site in G. barbadense and G. hirsutum is useful in separating the Old and New World cottons. Further study is necessary to determine whether the extra SspI site could be a representative marker for the A genome species. Previous studies have shown that G. arboreum and G. herbaceum are also similar with respect to flavonoid constituents (Parks et al., 1975), seed protein profiles (Cherry et al., 1972), and chloroplast genomes (Wendel, 1989). The identical rDNA gene structure in G. barbadense and G. hirsutum is explainable by the extensive introgression between these two species. The initial genetic source of high fiber strength and Verticillium wilt (caused by Verticillium dahliae Kleb) tolerance in G. hirsutum cv. Acala is thought to be derived from G. barbadense introgression (Hyer and Bassett, 1985). Significant introgression of G. hirsutum into wild and cultivated G. barbadense was documented by allozyme loci (Percy and Wendel, 1990). The pedigree of the lines NM24016 and NM24022 is known to include a G. barbadense background (Tatineni et al., 1996). Although similar in rDNA patterns, these New Mexico lines were found to be very divergent in their RAPD banding patterns (Tatineni et al., 1996).

The low level of genetic diversity in the rDNA genes conforms with data from other molecular and protein studies in cultivated cotton. Very limited genetic diversity was identified in a large set of modern G. hirsutum cultivars by restriction fragment length polymorphisms (RFLPs) (Wendel and Brubacker, 1993) and allozymes (Wendel et al., 1992). It therefore appears that, despite their morphological and ecological diversity, cultivated cottons have a narrow genetic base. Esbroeck et al. (1998) have shown that genetic uniformity of cotton in the United States is greater today than it was 25 yr ago. Although there is a high degree of diversity within the germplasm, only a few cultivars are grown widely in the USA. A similar finding was reported for cotton cultivars grown in Pakistan (Iqbal et al., 1997). It is generally accepted that crops with a uniform or narrow genetic base are more susceptible to pathogens causing natural disasters and should be of concern to cotton breeders. A typical example is the epidemic of cotton leaf-curl virus disease in Pakistan (Iqbal et al., 1997).

AFLP Analysis
Four primer-pair combinations were used to assay 10 cotton plants from each of the 10 accessions for AFLP analysis. An average of 40 to 80 scorable bands were detected after selective PCR amplification with each primer combination. The bands ranged in size from 50 to 500 bp. The dendrogram of genetic relationships (Fig. 2) from UPGMA cluster analysis of similarity coefficients (Table 2) resulted in three major groups. The diploid species G. arboreum and G. herbaceum grouped into one unit. The G. hirsutum genotypes T582, T586, and NM 24016 clustered with G. barbadense into another group. Within this group, the genetic marker stocks T582 and T586 formed a separate subgroup. The third group was comprised of G. hirsutum genotypes Acala SJ-2, Stoneville 2, TM1, and Coker 312. Within this group, TM1 and Stoneville 2 formed a sister-group relationship.



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  		Fig. 2 Dendrogram based on Jaccard's similarity coefficients showing genetic relatedness among species and cultivars of cotton

 

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  		Table 2 Genetic similarity matrix based on Jaccard's coefficient (x100) for species and cultivars of cotton from AFLP data

 
Although both the sample size and the number of primer-pairs used in this study were not comprehensive, this study showed that AFLP is a very sensitive technique for detecting markers for genetic studies in cotton. Banding patterns obtained with AFLP were highly reproducible when the same sample DNA is used in independent experiments. Other PCR based techniques such as RAPDs are often associated with problems of stability and reproducibility of banding patterns. Compared with our unpublished RAPD data of the same samples, a 10-fold increase in the number of bands was produced with AFLP presenting a greater opportunity to detect polymorphisms among closely related genotypes. In contrast to radio-labeling, silver-staining overcomes the need to work with high levels of radio-isotopes. Silver stained AFLP gels are considered to produce a larger number of better-defined bands than 32P-labeled gels (Cho et al., 1996). The silver staining procedure also enables isolation of specific AFLP fragments for cloning (Cho et al., 1996).

The AFLP dendrogram (Fig. 2) assigned the species–genotypes into groups corresponding with their origin and/or pedigree relationships. The pedigree of NM24016 is H12156/2/77-505/ Russian 5904 (Tatineni et al., 1996). It is known that the cultivar Russian 5904 is a selection from G. barbadense. This could explain the clustering of NM24016 with the G. barbadense group. The clustering of Coker 312 and TM1 finds support in that both genotypes have Deltapine 14 in their pedigrees. Similarly, the association of Coker 312 with Stoneville 2 is not unexpected since Coker 100, a progenitor of Coker 312, is a selection out of Stoneville 2. The exact pedigrees of T582 and T586 are complex since both originated from breeding work that began in the early 1950s (R. Kohel, 1997, personal communication). The close affinity of T582 and T586 may be explained by similar breeding origins. The placement of TM1 and NM24016 in two different clusters is supported by RAPDs (Tatineni et al., 1996).

A unique feature of the AFLP data is its ability to discriminate all the taxa used in this study making it a very promising marker system in cotton especially since modern cotton cultivars are closely related and have a high level of genetic uniformity (Esbroeck et al., 1998). For example, no chloroplast DNA mutations were detected between G. arboreum and G. herbaceum and only five mutations were detected between diploid and tetraploid species (Wendel, 1989). AFLP data clearly differentiated the two diploid species from each other as well as from the tetraploid taxa (Fig. 2). Comparative studies of currently available DNA marker systems (RAPD, RFLP, AFLP) in rice (Oryza sativa L.), barley, and maize also indicate that a higher degree of polymorphism can be detected by AFLPs (Mackill et al., 1996; Russell et al., 1997; Marsan et al., 1998).

In conclusion this study showed that (i) the rDNA gene structure in cotton is similar to those of most other plants, (ii) a low level of rDNA variability was detected in cotton, and (iii) restriction site variation in the ribosomal RNA genes is useful in distinguishing New and Old World cottons. The AFLP technique is able to discriminate closely related taxa in cotton and provides sufficient numbers of polymorphic markers in a few experiments.Brubaker Wendel 1994


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ABSTRACT
 INTRODUCTION
 Materials and methods
 Results and discussion
 REFERENCES
 
Contribution from the Louisiana State Univ. Agric. Center, Louisiana Agric. Exp. Stn. Approved for publication by the director of the Louisiana Agric. Exp. Stn. as manuscript no. 98-09-0234.

Received for publication August 27, 1998.


   REFERENCES
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 ABSTRACT
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