Chromosomal studies and evolution in Sapindaceae
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1 CARYOLOGIA Vol. 51, n. 1: 81-93,1998 Chromosomal studies and evolution in Sapindaceae RICARDO A. LOMBELLO * and ELIANA R. FORNI-MARTINS Departamento de Botanica, Instituto de Biologia, Universidade Estadual de Campinas, Caixa Postal 6109, Campinas , SP, Brasil. SUMMARY - Chromosome numbers and chromosomal ideograms were obtained for the Sapindaceae forest climbers Serjania caracasana, S. fuscifolia, S. meridionalis and Urvillea laevis (tribe Paulliniae) and the cerrado shrub Talisia obovata (tribe Melicocceae). Cytological preparations were obtained by Giemsa technique. Serjania and Urvillea showed 2n = 24, with chromosome length varying from 1.2 to 6.3I1m, large in relation to other Sapindaceae genera. Most chromosomes were submetacentric in Serjania and met acentric in Urvillea. The literature shows no interspecific variation of chromosome number in the genus Serjania, but it did occur in Urvillea. Talisia obovata showed 2n = 32, with small chromosomes (1.0 to 2.1I1m). A revision of chromosome numbers in 40 genera and 122 species showed great variation between species of Sapindaceae (2n= 14 to 2n=96). There is a small overlap of chromosome number between climbers and shrubs/trees: 74% of climbers so far studied have 2n=20, 22 and 24, and 82% of non-climbers have 2n=28, 30 and 32. The numeric variation of chromosomes indicates that the disploidy may have played a major role in the evolution of the whole family of Sapindaceae. Although the data in literature were not enough for a deep analysis we noted a tendency between smaller chromosome length and greater chromosome number. We propose that the derivation of climber habit (tribe Paullinieae) from non-climber involved mostly reduction in chromosome number and increase in absolute chromosome length. INTRODUCTION Sapindaceae has about 120 genera and more than 1000 species in the tropics and subtropics (HEMMER and MORAWETZ 1990). Almost a third of all the species are climbers (HEMMER and MORAWETZ 1990), but the most are shrubs and trees. The climbers belong to only seven genera in tribe Paullinieae (HUNZIKER 1978). HEMMER and MORAWETZ (1978), based on reports for about 60 species and 25 genera, pointed out that the karyological differentiation of Paullinieae is characterized by dysploid reduction of chromosome number and increase in chromosome size. * Curso de P6s-Granduaçao em Biologia Vegetal/IB/UNICAMP.
2 82 LOMBELLO and FORNI-MARTINS In general, climbers are considered derived in relation to shrubs and trees (RADFORD et al. 1974) due to morphological and anatomical characters. Anomalous secondary growth and greater diameter of vessel elements are derived, both having adaptive value for climbers, related to flexibility and more efficient transport (CARLQUIST 1991). Although morphological and anatomical differences between climber and non-climber species of the same or related genera are well known in literature, there is however no information on whether these adaptive changes in the plant structure could be related to any shift in the chromosomes. If such a shift could be noted, then it would indicate different evolutive pathways in the speciation of climber and nonclimber species. This paper aims at contributing to the knowledge of the karyotypic characters of Sapindaceae and investigating whether there is any relationship between the derivation of the climber habit and some alteration at chromosomal level, as in the chromosome number or in the chromosome morphology between species with different habits in the family Sapindaceae. MATERIALS AND METHODS Species of Serjania and Urvillea were collected in Santa Genebra Forest Reserve, municipality of Campinas, state of Sào Paulo. Talisia obovata was collected in a cerrado (savanna-like vegetation) area of Itirapina Experimental Station municipality of Itirapina, state of Sà.o Paulo. The voucher specimens are deposited in UEC, the herbarium of the Departamento del Botanica/IB/UNICAMP (Table 1). Root tips were pretreated in PDB-saturated solution, at C, for 3-6 hours, in order to get a better chromosomal condensation and arrangement on the slide. The material was fixed in 3:1 ethanol: glacial acetic acid (Carnoy's solution) for 24 h, and stored in 70% ethanol. Giemsa technique was used (GUERRA 1983) for cytological preparations. Measurements of chromosome lengths were carried out by means of camera lucida drawings based on 10 mitotic cells, allowing the chromosomal ideogram elaboration. The TCL (total chromatin length) and TF% (HUZIWARA 1962) were calculated. The chromosome morphology was classified according to the centromeric index (ci), following the TABLE 1 - Species of Sapindaceae studied with climber (c), shrub (s) or tree (t) habit; collected in Santa Genebra Forest (SGF) Campinas and Itirapina Experimental Station (IES), ltirapina; with respective collector number.
3 CHROMOSOMAL STUDIES IN SAPINDACEAE 83 nomenclature of LEVAN et al. (1964) modified by GUERRA (1986). The mean, standard deviation, coefficient of variation for chromosome lengths and TF% in the species studied were calculated following usual statistical methods (SOKAL and ROHLF 1969). The values of TCL (10 cells per species) and TF% (4 cells per species) of the climber species were compared by means of analysis of variance and Tukey test. The survey of the chromosome numbers of species of Sapindaceae was based on BOLKHOVSKIKH et al. (1969), MOORE (1973, 1974, 1977), GOLDBLATT (1981, 1984, 1985,1988) and GOLDBLATT and JOHNSON (1990,1991,1994). This survey allowed the calculation of the percent frequency (Fi,g) of a chromosome number i in a genus g with T species studied by the formula: where Si = number of species with i chromosomes in genus g. The Fi,g values were used to calculate the weighted relative frequency (RFJ of each chromosome number of climber and non-climber species, following the formula: where G = number of frequencies calculated for a same chromosome number i, and L = number of total frequencies for all the species with the same habit. RESULTS Serjania species and Urvillea laevis showed diploid number 2n = 24 (Table 2, Fig. 1). The chromosome lengths varied from 1.4 to 4.5~m. The TCL value was higher for Serjania meridionalis and Urvillea laevis (Table 2). The chromosome length showed a gradual variation in the studied species. In Serjania the chromosome were mostly metacentric and submetacentric, but always there was at least one acrocentric (Figs. 2, 3,4). In Urvillea laevis most chromosomes TABLE 2 - Chromosomal parameters ofspecies of Serjania, Urvillea and Talisia. LC and SC indicate, respectively, the longest and the shortest chromosome for the species (in I1m). Different letters in Tukey test mean significant differences at 5% level.
4 84 LOMBELLO and FORNI-MARTINS Fig Mitotic metaphase of Sapindaceae. a) Serjania carcasano; b) S. meridionolis; c) Urvillea laevis; d) Talisia obovata. Bar: 10 ìm. were submetacentric, but some were metacentric (Figs. 1, 5). The TF% index was the lowest in Serjania meridionalis (Table 2). For Talisia obovata the chromosome number was 2n = 32, the chromosomes were small, attaining m at maximum. The revision of chromosome numbers of species of Sapindaceae showed a great variation between genera (2n = 14 to 2n = 96). The genera are arranged in the respective tribes (based on RADLKOFER 1956) in Table 3. The distributions of the weighted relative frequency (RFJ of chromosome numbers of climber and non-climber (shrubs and trees) species of Sapindaceae are presented in Fig. 6. In nonclimbers the distribution was strongly asymmetrical, beginning with 2n = 18 (1.0%) and ascending without interruptions to
5 CHROMOSOMAL STUDIES IN SAPINDACEAE 85 Figs Idiograms of the haploid complements of four taxa of Sapindaceae. 2. Serjania caracasana, 3. Serjania fuscifolia, 4. Serjania meridionalis, 5. Urvillea laevis. 2n = 32 (almost 34% ). About 80% of the distribution centered in 2n = 28, 30 and 32. There were isolated groups with very little frequencies, at 2n = 36 (0.7%), 2n=56 (0.7%) and 2n=96 (1.5%). In climbers the distribution was very disperse, having five modes. Four modes were isolated groups with 2n= 14 (1.2%),28 (16.6%) and 44 and 86, both with 4.2% weighted relative frequency. The other mode was 2n=24 (54.2%) in a very narrow distribution from 2n=20 (6%) to 2n=24 (13.7%), a range that included around 73% of the total distribution.
6 86 LOMBELLO and FORNI-MAR11NS TABLE 3 - Tribes and genera of Sapindaceae (based on RADLKOFER 1956) with habit (c-climber, sshrub, t-tree), percent of species studied in relation to the total number of species in the genus - sp (%), and chromosome number (n and 2n) reports based on BOLKHOVSKIKH et al. (1969), MOORE (1973, 1974, 1977), GOLDBLATT (1981, 1984, 1985, 1988), GOLDBLATT and JOHNSON (1990, 1991, 1994) NEFFA and FERRUCCI (1994), followed by the percent frequency in each genus (Fi,g).
7 CHROMOSOMAL STUDIES IN SAPINDACEAE 87 DISCUSSION Cytological studies in Serjania. The genus Serjania comprises about 226 species, of which about 80 are found in Brazil (NOGUEIRA et al. 1995). Chromosome numbers (n = 12 or 2n=24) were found in 21 Serjania species (GUERVIN 1961; FERRUCCI 1981, 1985; HEMMER and MORAWETZ 1990; FORNI- MARTINS et al. 1995; NOGUEIRA et al. 1995). There is no divergence in the literature data (Table 4), neither between these and the present results. FERRUCCI (1981) suggested the basic number x = 12, which was confirmed by NOGUEIRA et al. (1995). Although no variation was found for chromosome number in Serjania, NOGUEIRA et al. (1995) noted considerable inter- and intraspecific variation of chromosome length, indicating a karyotipic evolutionary trend based on chromosomal rearrangement. In a population of S. fuscifolia they observed 9 met acentric pairs, with average length range of the chromosomes between 1.3 ìm and 2.3 ìm. They found in other populations of S. fuscifolia 8 metacentric pairs, and a chromosome average length ranging from 1.6 to 2.7 ìm. In the present paper the average length of the smallest chromosome of S. fuscifolia was 1.4 ìm and that of the longest was 3.3 ìm (Table 2). Most chromosomes were submetacentric (7 pairs). Despite the different terminology used by those authors to classify chromosomes, the average chromosome length showed notable variation between their populations and ours. There are no data in literature on karyomorphology of S. caracasana and S. meridionalis. The chromosome measurements presented here (Table 2) differ of those showed by HEMMER and MORAWETZ (1990) based on FERRUCCI (1981) drawings. For S. caracasana HEMMER and MORAWETZ (1990) cited a variation in chromosome size about ìm, values which disagree with those presented in Table 2 ( ìm). The authors mentioned that the chromosomes of S. meridionalis rarely attain 2.25 ìm, yet Table 2 shows a length up to 4.2 ìm. TF% values near 50% indicate karyotipic symmetry, while values lesser than that indicate asymmetry. The karyotipic asymmetry is related with the terminal position of the centromeres or with great differences in length of different chromosomes. Accepting the evolutionary trend to asymmetry postulated by STEBBINS (1971) in angiosperms, S. meridionalis (TF% = 34.7) may be considered the most derived species of the three studied species of Serjania, followed by S. fuscifolia (TF% = 36.2) and S. caracasana (TF% = 39,7) (Table 2, Figs. 2, 3, 4). Cytological studies in Urvi11ea. The genus Urvillea is represented by 13 species (NOGUEIRA et al. 1995), but only three of them were reported for chromosome number: U. chacoensis
8 88 LOMBELLO and FORNI-MARTINS TABLE 4- Chromosome numbers in Serjania (x= 12). 2n = 22 and U. uniloba var. uniloba 2n = 44 (FERRUCCI 1981), and U. ulmacea 2n = 86 (NOGUEIRA et al. 1995). Our counting in Urvillea laevis (2n = 24) is so far unpublished. For the polyploid species U. uniloba var. uniloba (2n = 44) FERRUCCI (1981) presented a schematic drawing of chromosomes showing a length range of ~m. NOGUEIRA et al. (1995) cited 2n=86, chromosome lengths from 0.6 to 2.4 ìm and TCL of ìm for U. ulmacea, which showed 29 met acentric pairs, 13 submetacentric pairs and only one telocentric pair, with TF% of (NOGUEIRA et al. 1995). U. laevis showed chromosome lengths from 1.9 to 4.5 ìm and the same metacentric predominance (7m+5sm, TF% = 41.5) of U. ulmacea, even considering the different morphological classification system used by these authors. Besides the numerical variation, it seems that there is an interpsecific variation of chromosome size. The species with the smaller chromosomes (U. ulmacea) showed, on the other hand, the greater chromosome number, probably originated by a polyploidy followed by reductional aneuploidy (NOGUEIRA et al. 1995).
9 CHROMOSOMAL STUDIES IN SAPINDACEAE 89 The literature indicates a polyploid series for Urvillea based on x = 11. This basic number seems a derivation of the generic basic number x = 12 found in tribe Paullinieae. If x = 11 is accepted for the genus, then it might have occurred an additional aneuploidy, not followed by a polyploidy in U. laevis (2n = 24), thus changing its diploid number. Polyploidy seems to be a natural pathway in the genus Urvillea (FERRUCCI 1981). Cytological studies in Talisia. The genus Talisia comprises about 50 species of shrubs and trees, mostly dispersed in tropical regions of South and Central America (RADLKOFER 1956). There is no chromosomal study for Talisia species beside ours. The diploid number (2n = 32) found for Talisia obovata (Table 2) is also cited for Melicocca, a close related genus that belongs to the same tribe Melicocceae. Chromosomal and habit evolution in Sapindaceae. Despite the large size of the family, there is still few chromosomal information (40 genera and 122 species), but it is sure that chromosome numbers generally vary in Sapindaceae (T able 3) : 2n = 14 in Cardiospermum integerrimum (FERRUCCI 1989) to 2n = 96 in Melicoccus lepidopetalus (NEFFA and FERRUCCI 1994). This variation is greater than that previously related by HEMMER and MORAWETZ (1990): 2n=20 to 2n=32. The investigation on the relationship between the climber habit evolution and chromosome differentiation within the three genera studied (Table 2) is facilitated by the fact that each genus has constant habit (Serjania and Urvillea are only climbers, while Talisia are shrubs or trees) and there is a constancy of chromosome number in the majority of genera, as in Serjania. Moreover there is an apparent relationship between the plant habit and the grouping of chromosome numbers in the tribes of Sapindaceae. In the climber genera, represented by Cardiospermum, Paullinia, Serjania, Thinouia, Houssayanthus and Urvillea (tribe Paullinieae), the chromosome numbers vary from 2n = 14 to 2n = 86 (Table 3), but it is most frequently 2n = 24 (Paullinia and Serjania shows only this counting). The Urvillea diploid numbers 2n = 44 or 86 are due to polyploid derived species and are not frequent. On the other hand, in the non-climber species the variation of chromosome numbers ranges from 2n = 18 to 2n = 96, but the most frequent is 2n = 32. The counting for T alisia obovata (2n = 32) agrees with the shrub and arboreous pattern. There is a small overlap of chromosome numbers 2n = 20, 22 and 24 between climber- and nonclimber species, but the RFi of climbers are very high (a little over 80%) in relation to the RFi of non-climbers (a little less than 9%, Fig. 6). For 2n = 28 climbers and non-climbers show similar RFi, but there
10 90 LOMBELLO and FORNI-MARTINS Fig Relative frequency (RF;) of chromosome numbers (i = 2n) in climber and non-climber species of Sapindaceae. is a unique climber species (Thinouia mucronata, NEFFA and FERRUCCI 1994) against several species and genera mentioned in Table 3. This bias results from the formula used to calculate RFi. Formula 1 is strongly influenced by the number of species studied in the genus, and the number of species with the same chromosome number used to calculate G (in formula 2) may be very different. The center of the distribution of chromosome numbers in climbers ranges from 2n=24 (54%), followed by 2n=22 (14%) and 2n=20 (6%). On the other hand, more than 80% of the nonclimbers studied have between 2n = 28 and 2n = 32, showing a distribution of RFi quite different from climber species. Dysploidy may have operate in the evolution of the family as a whole, e.g., in species of Urvillea (2n = 22 and 2n = 24). Polyploidy is a much less frequent event, both in climbers, with 2n = 44 and 86 (RFi = 6% ) and in shrubs/trees with 2n = 56 and 96 (RFi = 1.7%). The family Sapindaceae is considered to have a monophyletic origin and the habit of climber to be derived and the most specialized (RADFORD et al. 1974). We suggest therefore that the climber habit in Sapindaceae are derived from non-climber through a chromosomal evolution based mostly on reduction
11 CHROMOSOMAL STUDIES IN SAPINDACEAE 91 of chromosome number, as observed in tribe Paullinieae (Table 3). Almost all Paullinieae have somehow climber habit (RADLKOFER 1956). HEMMER and MORAWETZ (1990) also suggested that the tribe Paullinieae is characterized by low chromosome number, probably due to reduction by dysploidy. A survey of the pollen morphology of 31 species of Sapindaceae also supported the hypothesis of derivation of Paullinieae from a Cupanieae-like ancestor (VAN DER HAM and TOMLIK 1994). The number 2n= 14, related for Cardiospermum integerrimum (FERRUCCI 1989), is the unique in the family. Considering the presence of some morphological characters, FERRUCCI (1989) concluded that it was a primitive species. However, our data shows that the asymmetrical karyotype may indicate that this species is derived, probably from other with 2n = 20. So, numeric reduction may be occurred in this case too. Plant evolutionary pathways may lead to decrease or increase in the absolute chromosome size (STEBBINS 1971). Comparing chromosome lengths between climber and shrub/three species, some considerations can be done on the evolution of habit in Sapindaceae. The karyology of Paullinieae is characterized by an increase of chromosome length, when compared with other Sapindaceae, as pointed out by HEMMER and MORAWETZ (1990). Most non-climber species of Sapindaceae studied show very small chromosomes ( ìm), as in Diplokeleba (tribe Cupanieae, FERRUCCI 1989), Litchi sp. {tribe Nephelieae), Sapindus sp. (tribe Sapindeae) and Koelreuteria sp. (tribe Koelreuterieae) (HEMMER and MORAWETZ 1990). These results are similar to those mentioned for Talisia obovata (tribe Melicocceae) in Table 2 and Fig. 1. Among non-climber species, Llagunoa glandulosa is an exception, having large chromosomes (GUERVIN 1961). In general, it is likely that the increase of chromosome length in climbers is associated to the reduction of chromosome number. The difference in chromosome sizes, associated with chromosome numbers, between climbers and shrubs/trees possibly indicates that speciation may have been caused by structural alterations, like inversions and translocations, which usually leads to dysploidy (GUERRA 1988). It would be very important to quantify by cytophotometric analysis the real DNA variation and the average packing ratio of these species, to confirm the difference in the amount of DNA between them. More studies on different species of Sapindaceae are needed, once so few information exists for a so great family. New data can be useful to confirm this hypothesis about the relationship between evolution of climber habit and the derivation of chromosome characters, mainly involving the decrease of chromosome number and the increase of absolute chromosome size. Acknowledgements. - The authors are grateful to Dra. Maria Silvia Ferrucci (Instituto de Botanica del Nordeste, Corrientes, Argentina) for the identification of the species of Serjania and Urvillea and to Dr. Fernando Roberto Martins (Departamento de Botanica/IB/UNICAMP, Campinas, Brasil) for suggestions and critic reading of manuscript.
12 92 LOMBELLO and FORNI-MARTINS REFERENCES BOLKHOVSKIKH Z., GRIF V., MATVEJEVA T. and ZAKHARYEVA O., Chromosome numbers of flowering plants. In: V.L. Komarov (ed.), Botanical Inst., Academy ot Sciences ot the URSS, 926 pp. CARLQUIST S., Anatomy of vine and liana stems: a review and synthesis. In: F.E. Putz and H.A. Mooney "The biology of vines", pp , Univ. Cambridge press, New York. FERRUCCI M.S., Recuentos cromos6micos en Sapinddceas. Bonplandia, 5(11): ' Recuentos cromos6micos en Allophylus y Serjania (Sapindaceae). Bol. So. Argent. Bot., 24: ' Chromosomas en Cardiospelmum y Diplokeleba (Sapindaceae), significado taxon6mico y evolutivo. Bonplandia, 6: FORNI-MARTINS E.R., PINTO-MAGLIO C.A.F. and CRUZ N.D., Chromosome number in Brazilian cerrado plants. Rev. Brasil. Genetica, 18: GOLDBLATT P., Index to plant chromosome numbers, Monographs in Systematic Botany from The Missouri Botanical Garden, v. 4, St. Louis. -' Index to plant chromosome numbers, 1979, Monographs in Systematic Botany fromthe Missouri Botanical Garden, v. 8, St Louis. -' Index to plant chromosome numbers, Monographs in Systematic Botany from The Missouri Botanical Garden, v. 13, St. Louis. -, Index to plant chromosome numbers, Monographs in Systematic Botany fromthe Missouri Botanical Garden, v. 23, St. Louis. GOLDBLATT P. and JOHNSON D.E., Index to plant chromosome numbers, Monographs in Systematic Botany from The Missouri Botanical Garden, v. 30, St. Louis. -' Index to plant chromosome numbers, Monographs in Systematic Botany fromthe Missouri Botanical Garden, v. 40, St. Louis. -, Index to plant chromosome numbers, Monographs in systematic Botany fromthe Missouri Botanical Garden, v. 51, St. Louis. GUERRA M.S., O uso do corante Giemsa na citogenetica vegetal- comparas:iio simples e o bandeamento. Cienc. Cult., 35: , Reviewing the chromosome nomenclature of Levan et al. Short Communication, Rev. Brasil. Genet., 9: ' Introdus:iio a citogenetica geral. Ed. Guanabara S.A., Rio de Janeiro. GUERVIN C., Contribuition a l'etude cyto-taxonomique des Sapindacees et caryologique des Melianthacees et des Didieracees. Rev. Cytol. BioI. veg., 23: HEMMER w. and MORAWETZ W., Karyological differentiation in Sapindaceae with special reference to Serjania and Cardiospelmum. Bot. Acta, 103: HUNZIKER A.R., Notas criticas sobre sapindaceas a1&entinas. III. Houssayanthus, genus novum Sapindacearum. Kurtziana, 11: HUZIWARA Y., Karyotype analysis in some genera of Compositae. VIII. Further studies on the chromosome of Aster. Amer. Jour. Bot., 49: LEVAN A., FREDGA K. and SANDBERG A.A., Nomenclature for centromeric position on chromosomes. Hereditas, 52: MOORE R. V., Index to plant chromosome numbers, Regnum Vegetabile, v. 90, pp: ' Index to plant chromosome numbers, Regnum Vegetabile, v. 91, pp: ' Index to plant chromosome numbers, Regnum Vegetabile, v. 96, pp: NEFFA V.G.S. and FERRUCCI M.S., Analisis cromosomico em Sapindaceae de Sudamerica.. VI Congreso Latinoamericano de Botanica, Mar del Plata, Argentina. Libro de Resumenes: 284. NOGUEIRA C.Z., RUAS P.M., RUAS C.F. and FERRUCCI M.S., Karyotypic study of some species of Serjania and Urvillea (Sapindaceae; tribe Paullinieae). Am. Jour. Bot., 82: RADFORD A.E., DiCKSON W.C., MASSEY J.R. and BELL C.R., Vascular plant systematics. Harper & Row Publ., N.Y.
13 CHROMOSOMAL STUDIES IN SAPINDACEAE 93 RADLKOFER L., Sapindaceae. In: Engler A. (ed), "Das Ptlanzenreich", Weinheim, 98 (1,2): SOKAL R.R. and ROHLF F.J., Biometry. W.H. Freeman Co., San Francisco. STEBBINS G.L., Chromosomal variation in higher plants. Edward Arnold, London. VAN DER HAM R. W.J.M. and TOMLIK A. - Serjania pollen and the origin of the tribe Paullinieae (Sapindaceae). Rev. Paleobot. Palynol., 83: Received 29 September 1997; accepted 12 January 1998
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