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Genetics and Molecular Biology |
2Instituto de Botánica del Nordeste (UNNE—CONICET), Casilla de Correo 209, 3400 Corrientes, Corrientes Province, Argentina 3Miembro de la Carrera del Investigador Científico (CONICET), Facultad de Ciencias Exactas y Naturales y Agrimensura (UNNE), Corrientes, Corrientes Province, Argentina
Received for publication October 29, 2002. Accepted for publication February 4, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: concerted evolution • karyotypes • Lathyrus • Leguminosae • Notolathyrus • nucleotypes • South America
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). It is distributed throughout the temperate zones of the Northern Hemisphere and extends into tropical East Africa and South America. The main center of diversity is the eastern Mediterranean region, with two smaller centers in North and South America (Kupicha, 1983
; Allkin et al., 1985
).
Nearly 23 species of Lathyrus are endemic to South America, from Colombia to Tierra del Fuego, Argentina. Their habitats are highly variable, ranging from the subtropical Paranaense Forest, mesic hills, and flooded lowlands to the Patagonian Forest. In spite of the broad ecological range of these species, they constitute a fairly homogeneous group (Burkart, 1935
, 1942
), which is clearly distinct from the North American species (Kupicha, 1983
).
All South American species, together with L. pusillus Elliot of North America, were included in section Notolathyrus, while the remaining species of North America were kept in section Orobus (Kupicha, 1983
). However, in their cpDNA-based infrageneric classification, Asmussen and Liston (1998)
proposed that both sections should be combined, because section Orobus is monophyletic only when the South American species are included.
Cytological investigations have shown that the basic chromosome number of x = 7 is constant throughout the genus and that most of the species are diploid, with polyploids as rare exceptions (Senn, 1938
; Yamamoto et al., 1984
; Broich, 1989
; Battistin and Fernández, 1994
; Klamt and Schifino-Wittmann, 2000
; Seijo and Fernández, 2001
). Despite this stability in chromosome number, large variations in chromosome size have played an important role in the evolution of Lathyrus species, which are associated with a fourfold variation in 2C nuclear DNA amount (Narayan and Rees, 1976
).
Many karyotypic studies have been performed on Old World members of Lathyrus (Lavania and Sharma, 1980
; Yamamoto et al., 1984
; Sahin et al., 2000
), but there is a paucity of data for American species, with the karyotypes of only five South American entities described so far (Battistin and Fernández, 1994
; Klamt and Schifino-Wittmann, 2000
). From the available information, a number of conflicting observations have arisen. Some authors claim that, in addition to the numerical constancy, Lathyrus species display morphological uniformity of chromosomes and homogeneous karyotype arrangement (Lavania and Sharma, 1980
; Narayan and Durrant, 1983
; Klamt and Schifino-Wittmann, 2000
). However, others have found enough interspecific karyotype differences to allow species characterization (Yamamoto et al., 1984
; Murray et al., 1992; Battistin and Fernández, 1994
). Such discrepancy was also observed at the infraspecific level, mainly in the widely studied L. odoratus L. and L. sativus L. (Bhattacharjee, 1954
; Sharma and Datta, 1959
; Verma and Ohri, 1979
; Murray et al., 1992b
).
From a karyosystematic point of view, Yamamoto et al. (1984)
have noted that Old World species could be grouped according to their karyotype morphology and that some of them were coincident with the taxonomic sections proposed by Davis (1970)
. However, these authors did not propose any relationship, either among groups or considering the world infrageneric classification proposed by Kupicha (1983)
. Furthermore, none of the South American species were included in that analysis.
Thus, in this paper the karyotypes of 10 South American species are analyzed and compared with those of five species of the Northern Hemisphere with the following objectives: (1) to clarify the taxonomic relationships of some South American entities, (2) to gain insight into the evolutionary relationships of section Notolathyrus, and (3) to examine the patterns of chromosome variation in relation to the taxonomic position and the life cycle of the taxa.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Somatic chromosomes were studied in root meristems of germinating seeds, which were pretreated in distilled water at 0°C for 24 h, then fixed in ethanol : lactic acid (5 : 1) overnight (Fernández, 1973
) and stored in 70% aqueous ethanol. Root tips were stained according to the Feulgen technique, meristems were macerated in a drop of 3% acetic orcein before squashing, and slides were made permanent using Euparal (Asco Laboratories, Manchester, UK) as the mounting medium.
At least 10 metaphases were drawn for each population (including 3–8 individuals) using a Zeiss camera lucida (Carl Zeiss, Germany), selecting the five best for measurements. The nomenclature used for the description of the chromosome morphology is that proposed by Levan et al. (1964)
: the abbreviations m, sm, and st designate metacentric, submetacentric, and subtelocentric chromosomes, respectively. Satellites were classified as follows: (a) microsatellite, width less than the thickness of the chromosome; and (b) macrosatellite, width equal to that of the chromosome. Idiograms were drawn based on mean centromeric index and arranged in order of decreasing size.
For the numerical characterization of the karyotypes the following parameters were calculated: (1) total chromosome length of the haploid complement (TCL); (2) mean chromosome length (CL); (3) mean centromeric index (CI); (4) intrachromosomal asymmetry index (A1) = 1 – [
(b/B)/n]; and (5) interchromosomal asymmetry index (A2) = s/x, where b and B are the mean length of short and long arms of each pair of homologues, respectively, n is the number of homologues, s is the standard deviation, and x the mean chromosome length. Karyotype asymmetry has been determined using the A1 and A2 indices (Romero Zarco, 1986
) and the categories of Stebbins (1971)
.
Means were compared by one-way ANOVA after Bartlett's test of homogeneity. Also, Tukey's test was carried out to measure differences between each pair of means. A cluster analysis of the karyotype data was carried out to examine karyotype similarity among species and sections. A data matrix of 16 OTUs (operational taxonomic units) x 10 variables was constructed. The TCL, CI, A1, and A2 indices, number of m, sm, and st chromosomes as well as the presence and position of satellites were considered. The NTSYS- PC program developed by Rohlf (1994)
was used to standardize the data matrix, to calculate the average taxonomic distance, and to generate a phenogram. Clustering was performed using the unweighted pair-group method (UPGMA). Phenogram distortion was measured by computing the cophenetic correlation coefficient (r). Additionally, to evaluate the contribution of each karyotypic parameter to the ordination of species, the entities were also subjected to a principal component analysis (PCA) based on data matrix of 16 OTUs times the four mentioned quantitative variables.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Satellites were detected in one or two chromosome pairs in all the analyzed species. South American specimens characteristically possess a macrosatellite on the long arm of the shortest chromosome (7) of the complement (Table 1 and Figs. 1–11, 17–27). The only species that lacks this type of SAT chromosome is L. macrostachys, which presents a macrosatellite in the short arm of the sm pair 4 (Figs. 4, 21). Lathyrus magellanicus var. magellanicus is unique within section Notolathyrus because it has two satellited chromosomes pairs (Fig. 22). Among species of the Northern Hemisphere, the position of the secondary constriction is more variable, and L. odoratus is the only species that presents microsatellites in two pairs of chromosomes (Table 1 and Figs. 12–16, 28–32).
The chromosomes of the analyzed species are of medium size according to the classification of Lima de Faría (1980)
. The mean chromosome length (ML) ranges from 4.56 µm to 7.25 µm, in a graded series within the complement. Haploid genome length (TCL) varies from 31.96 µm to 50.74 µm (Table 1), and the mean centromeric index (CI) of the complements varies between 30.16 and 37.84 (Table 1).
A statistical comparison of the populations demonstrates that there are no significant infraspecific differences for all the variables measured. Therefore, idiograms as well as the parameters presented in this paper represent the means of the populations analyzed for each species. However, at the interspecific level, TCL and CI significantly differentiate some species (Table 1).
Considering mean values, species of section Lathyrus have the greatest TCL and CI, those of Notolathyrus possess an intermediate TCL but the lowest CI, while the species of Orobus have the shortest TCL but a CI close to that of Lathyrus. The relationship between TCL and CI of each species is plotted in Fig. 33. ANOVA of TCL discriminated among species of the three sections analyzed (F = 45.95, P < 0.05), while only the CI did among species from different hemispheres (F = 86.17, P < 0.05). Considering the life cycle, perennial species have a greater TCL and lower CI than annuals, except L. japonicus (section Orobus), which has a similar TCL and CI to annuals. Perennials of the three sections have significant differences in TCL (F = 32.22, P < 0.05), but the CI only discriminates the Northern Hemisphere species from the South American ones (F = 75.89, P < 0.05). Among annuals, species of section Lathyrus presented a higher TCL (F = 22.78, P < 0.05) and CI (F = 20.82, P < 0.05) than L. crassipes of section Notolathyrus.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Krapovickas and Fuchs, 1957
; Lavania and Sharma, 1980
; Yamamoto et al., 1984
; Battistin and Fernández, 1994
; Klamt and Schifino-Wittmann, 2000
).
Karyotype formulae and quantitative analysis have a great uniformity among populations of any species, except those that correspond to different taxonomic varieties of L. magellanicus. These results support the hypothesis that claims infraspecific stability of karyotypes in Lathyrus species (Murray et al., 1992b
). At the interspecific level, quantitative and qualitative data allowed the differentiation of several of the taxa studied. Among species of section Notolathyrus, the most variable characters were the number of m chromosomes, as well as the number and position of satellites. In other sections, karyotype formulae were more similar, but species still could be differentiated mainly by the number, type, and position of satellites. These facts show that the karyotypes of Lathyrus species are not as fully constant as has been postulated (Narayan and Durrant, 1983
; Klamt and Schifino-Wittmann, 2000
) and that entities may be characterized by their chromosome features as was suggested by other authors (Yamamoto et al., 1984
; Murray et al., 1992a
; Battistin and Fernández, 1994
).
In relation to the genome size variation, the maximum ratio between the length of the longest and the shortest complements of Notolathyrus species is 1.43, while that calculated from data supply by Yamamoto et al. (1984)
for species of five sections is 2.31. These differences among complement length of diploid species are in accordance with that cited for nuclear DNA amounts of Old World species of Lathyrus (Rees and Hazarika, 1969
; Narayan, 1982
) and support the statement that variation in genome size is, perhaps, one of the more striking changes that have occurred during the divergence and evolution of the chromosome complements of this genus (Narayan and Rees, 1976
).
As a whole, Lathyrus is characterized by symmetrical karyotypes, with a predominance of sm chromosomes (Yamamoto et al., 1984
). This is also true for species of section Notolathyrus, but they have a greater degree of asymmetry than those of the Northern Hemisphere because of the presence of an st pair and fewer m chromosomes in most complements.
In spite of the observed interspecific variation, the bulk of karyotype data—formula, TCL, CI, A1, and A2—also showed a conservative tendency toward the maintenance of the general structure of the karyotypes among different clusters of species, in accordance with observations by Yamamoto et al. (1984)
in species of the Northern Hemisphere.
Chromosomes and systematics
Results obtained from this research have allowed us to compare for the first time the karyotypes of several South American species with those of the Northern Hemisphere. Analysis of karyotype formulae showed that, in general, species of section Notolathyrus form a homogeneous group and that they differ from the Northern Hemisphere entities of sections Lathyrus and Orobus, mainly in the following aspects: (1) lower number of m chromosomes, (2) presence of one st chromosome, (3) presence of a macrosatellite in the long arm of the shortest chromosome (except in L. macrostachys), and (4) lack of a short m chromosome. This fact is relevant because section Notolathyrus was established mainly on the basis of geographical distribution, and clearcut diagnostic exomorphological character are lacking. Therefore, if the results obtained in this report are maintained for the still-unstudied entities of the section, karyotype features may become good taxonomic characters to define members of Notolathyrus.
Among the species of the Old World, Yamamoto et al. (1984)
observed five different karyotypes and proposed a basal formula for the genus because it was detected in all the sections of Lathyrus sensu Davis (1970)
. The fact that neither the common formula nor the others described for Northern Hemisphere species were observed in species of section Notolathyrus would support the derived state of this section.
Cladistic analysis of cpDNA data indicates that South American species form a very homogeneous cluster of entities and that section Notolathyrus should be combined with the ancestral section Orobus (Asmussen and Liston, 1998
). From a karyological point of view, assessing this hypothesis is difficult because detailed karyotype information is very scarce for section Orobus (Broich, 1989
; Gutiérrez et al., 1994
; Seijo and Fernández, 2001
). However, from available chromosome data, species of section Notolathyrus and of section Orobus have enough infragroup homogeneity and significant differences between them for the sections to be maintained as distinct until more data become available.
The bulk of available karyotype data showed that most of the karyotype groups found in Lathyrus could be related either to different sections sensu Kupicha (1983)
or to the life cycle of the entities. The phenetic and principal component analyses of karyotype characters support this postulate. At the interspecific level, within section Notolathyrus, some species can be distinguished clearly by their karyotype formulae, and when quantitative karyotype data and the characteristics of SAT-chromosome are added, the majority of entities can be differentiated. Furthermore, for the particular case of L. magellanicus, satellites were useful to differentiate var. magellanicus from var. tucumanensis. This fact, together with the differences observed in karyotype formula between the varieties, indicate that the status of these entities should be revised, mainly considering the uniformity of karyotype at the infraspecific level.
Chromosomes and evolution
The constancy in chromosome number observed in the species studied here and in those cited in the literature (Senn, 1938
; Battistin and Fernández, 1994
; Klamt and Schifino-Wittmann, 2000
) indicates that numerical changes have not been important in the evolution of South American species, as noted for most of the entities of Lathyrus (Hitchcock, 1952
; Yamamoto et al., 1984
; Sahin et al., 2000
). However, this constancy differs from the situation described for North America, where several endemic polyploid species were found, so that North America was considered as a center of polyploid origin for Lathyrus (Broich, 1989
).
Differences in karyotype formulae and asymmetry indices found among species of different sections suggest that structural changes may have contributed to the diversification of the genus. On the other hand, the fact that species formed groups that share major karyotype characteristics may indicate that if the mechanisms of speciation within each group involved chromosome rearrangements, these may not have been large structural mutations, but small or cryptic changes. Alternatively, if speciation has occurred as a consequence of large chromosome modification, these may have been changes that did not modify the karyotype morphology, such as paracentric inversions or reciprocal translocations with segments of equal size.
The existence of a similar karyotype in Notolathyrus species suggests that chromosome evolution in this section may be constrained to nonrandom changes with particular restrictions for the occurrence or fixation of structural rearrangements. The stability of complements among a group of species was first explained by orthoselection, which considers the occurrence of random chromosome mutation, but with the fixation of a restricted type of rearrangement (White, 1978
). An alternative hypothesis was offered by King (1993)
, who considered the nonrandom nature of chromosomal evolution. This model contemplates that structural characteristics of the genome restrict the position and number of breaks that could occur and the type of rearrangements that could form. Even though both mechanisms would have similar results, a bulk of molecular and chromosome data is accumulating in favor of the position that claims that chromosomal mutations are not only nonrandom but are constrained by the chromosome structure to the type of change that can be produced (Peters, 1982
; Shaw et al., 1983
; King, 1993
; Narayan, 1988
).
Our findings that TCL varies without significant changes in karyotype formula, as seen among annual and perennial species of sections Notolathyrus and Lathyrus, suggest that changes in genome size may have been nonrandom and that the variation in DNA amounts is equally distributed among all chromosomes of the complements. These observations agree with those cited for Old World species of Lathyrus, in which variation of genome size was attributed to proportional distribution of mainly moderately repetitive DNA throughout the complement (Narayan and Durrant, 1983
). Data obtained from banding patterns also support the nonrandomness of genomic change in Lathyrus because bands with similar base composition tend to have equilocal disposition in the karyotypes (Ünal et al., 1995
; Seijo, 2002
). This pattern of evolution at molecular and subchromosomal levels suggests that species within each group evolved in a concerted fashion, maintaining the karyotype morphology.
It is common to assume that for a determined group of angiosperms, the karyotypes with more asymmetry have a derived status compared with those more symmetrical. Our results are not fully in accordance with this statement. Considering perennial species of different sections, no clear pattern emerges because the karyotype of L. japonicus of the ancestral section Orobus is more symmetrical than those of Notolathyrus species, but similar to those of Lathyrus species, both sections considered as derived (Kupicha, 1983
). Moreover, annual species of sections Notolathyrus, which are considered derived (Ehrendorfer, 1970
; Stebbins, 1971
), had more symmetrical karyotypes than perennials. Our results suggest that during the speciation and divergence of the genus, cycles toward symmetry and asymmetry may have occurred, as has been pointed out for different groups of angiosperms (Jones, 1970
; Stebbins, 1971
). Differences in TCL also indicate that during the diversification of the genus, cyclic changes in genome size may have occurred. These facts suggest that the utilization of asymmetry indices for the establishment of the evolutionary relationships in Lathyrus may not be straightforward, that variation in genome size may have not be unidirectional, and that both increments and decreases of genome size may have participated in the evolution and diversification of the genus, even within a related group of species.
The reduction of genome size that accompanied the evolutionary change from perennial to annual in Notolathyrus species coincides with different reports on angiosperm groups (Price and Bachmann, 1976
; Greilhuber and Ehrendorfer, 1988
). Moreover, annual species of this section, in addition to having lower TCL, present smaller pollen grains and lighter seed than perennials (Seijo, 2002
). These observations are in agreement with a considerable amount of data that show that the size of reproductive organs may be related to the genome size (Choi, 1971
; Chung et al., 1998
), as was postulated in the nucleotype hypothesis (Bennett, 1972
).
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Asmussen C. B. A. Liston 1998 Chloroplast DNA characters, phylogeny, and classification of Lathyrus (Fabaceae). American Journal of Botany 85: 387-401[Abstract]
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Battistin A. A. Fernández 1994 Karyotypes of four South America native species and one cultivated species of Lathyrus L. Caryologia 47: 325-330[ISI]
Bennett M. D. 1972 Nuclear DNA content and minimum generation time in herbaceous plants. Proccedings of the Royal Society of London, Series B, Biological Sciences 181: 109-135
Broich S. L. 1989 Chromosome numbers of North American Lathyrus (Fabaceae). Madroño 36: 41-48
Burkart A. 1935 Revisión de las especies de Lathyrus de la República Argentina. Revista de la Facultad de Agronomía y Veterinaria. Buenos Aires 8: 41-128
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Choi W. Y. 1971 Variation nuclear DNA content in the genus Vicia. Genetics 68: 195-211
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= Section Lathyrus, annual; • = Section Lathyrus, perennial; 
= Section Orobus, perennial; 
= Section Notolathyrus, annual; 
= Section Notolathyrus, perennial
